ISSN 10623590, Biology Bulletin, 2010, Vol. 37, No. 7, pp. 741–747. © Pleiades Publishing, Inc., 2010. Original Russian Text © N.N. Livanova, S.G. Livanov, 2010, published in Zoologicheskii Zhurnal, 2010, No. 1, pp. 93–100.
Zoological Prerequisites of Human TickBorne Infections in the Northern Urals N. N. Livanova and S. G. Livanov Institute of Animal Systematics and Ecology, Russian Academy of Sciences, Novosibirsk, 610091 Russia; email:
[email protected] Received July 11, 2009
Abstract—The results of studies in the pessimum of the taiga tick (Ixodes persulcatus Sch., 1930) range in the Urals have shown that this species occurs in the regions at latitudes of up to 60°50' N. In Northern Ural mountains, the ticks show preference for secondary smallleaved forests growing on southern slopes, where their abundance along census routes reaches 7 ind./km. The abundance and distribution of taiga ticks hosts, birds and small mammals, have been estimated in the main types of their habitats. Larvae and nymphs of the taiga tick have been found on nine bird and seven small mammal species, with the main parasitic load falling on the northern redbacked vole (Clethrionomys rutilus P., 1779), which is widespread and abundant in the greater part of the study area. Molecular biological analysis of I. persulcatus ticks and blood samples from their hosts has revealed the presence of nucleic acids of pathogenic microorganisms A. phagocytophilum, E. muris, and A. burgdorferi sensu lato, the RNA of tickborne encephalitis virus, and the DNA of Babesia microti. DOI: 10.1134/S1062359010070101
INTRODUCTION The theory of natural focality of diseases (Pav lovsky, 1939; 1964) has demonstrated the significance of studying individual components of a natural focus, including the modes of life of vectors and their hosts. Since the list of obligate arthropodborne infections transmitted by ixodid ticks is expanding, studies on the spatiotemporal dynamics of corresponding natural foci are highly relevant. To date, it has been shown that not only tickborne encephalitis virus and borreliae of the Borrelia burgdorferi sensu lato complex, but also anaplasms Anaplasma phagocytophilum causing granu locytic anaplasmosis and even ehrlichiae Ehrlichia muris, etiological agent of monocytic ehrlichiosis, form homonymic natural foci of arthropodborne human infections (Prirodnaya…, 2003). They are widespread on the Eurasian continent (Parola and Raoult, 2001) as well as within the range of the taiga tick Ixodes persulcatus (Korenberg, 1996; Telford III et al., 2002; Alekseev et al., 2001; Shpynov et al., 2006). Moreover, the agent of babesiosis was is isolated from Clethrionomys voles (Telford III et al., 2002), and its DNA was detected in I. persulcatus ticks (Alekseev et al., 2003). Territories with natural foci of obligate arthropod borne infections are usually nonuniform, and circula tion of pathogens can be maintained by various animal species and under different habitat conditions. In many respects, the significance of certain host and vector species depends on their abundance and distri bution pattern (Naumov, 1964). It has been repeatedly shown that foci of infections sustainably function on
territories where populations of not only vectors but also reservoir hosts are consistently abundant (Nau mov et al., 1957; Naumov, 1964; Bernstein et al., 1987; etc.). Many studies performed in the past few decades are devoted to analysis of pathogens recently described in different regions and their occurrence in vectors and hosts (Schouls et al., 1999; Liz et al., 2002; Petrovec et al., 2002; Ohashietal., 2005; etc.). We are aware of only one series of papers in which not only the diversity of microorganisms but also the main components of par asitic systems in natural foci are characterized in detail (Korenberg et al., 2002a, 2002b; Telford III et al., 2002; Kovalevskii et al., 2004; Nefedova et al., 2004; Morozov et al., 2007). These studies provide an insight into the diversity of natural foci and the general mech anism of the maintenance of their sustainable exist ence under natural–climatic conditions of the Middle Ural taiga zone. At the same time, there are no data on the diversity and occurrence frequency of agents caus ing arthropodborne infections and on the abundance and specific features of the distribution of ticks and their main hosts in the part of I. persulcatus range with pessimal habitat conditions. The purpose of this study was to estimate the degree of involvement of birds and small mammals in taiga tick feeding and circulation of pathogenic microorganisms in the Northern Urals. To this end, it was necessary to study the abundance and spatial distribution of ticks; species diversity of poten tial reservoir hosts (birds and small mammals), and their abundance and distribution in basic types of hab itats characteristic of the study region.
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MATERIAL AND METHODS Studies were performed in the Denezhkin Kamen’ Nature Reserve and its vicinities (Severoural’skii and Ivdel’skii districts, Sverdlovsk Region) from 2003 to 2008. The key plot was located on the eastern macros lope of the Urals, within the Northern Ural physio graphic province (59°30′–60°00′ E, 60°00′–61°30′ N), at elevations of 200 to 1500 m a.s.l. Changes in vertical plant distribution are manifested in the presence of welldefined mountaintundra, crooked–light forest, and forest belts, with the last one obviously prevailing in area (Prirodnye…, 1968). The abundance and spatial distribution of I. persul catus have been investigated in 2005 to 2008. Counts were taken by the conventional flagging method (Taezhnyi kleshch…, 1985). Three plots with a total area of no less than 60 km2 were surveyed, with basic mesorelief elements and vegetation variants typical of the study region being found within its boundaries. They ranged from mountain analogues of middle and northern taiga forests to crooked forests and tundras (cliffs and screes were not examined). Surveys were made with reference to the existing network of rides. Routes were laid out in a uniform random pattern but so that no less than 5 km were surveyed in every dis tinctive tract of land within a given plot. On the whole, 12 landscape tracts were surveyed, with the total route length being 283.5 km. Bird surveys were made along the routes laid within the reserve, in its protection zone, and in the vicinities of the VsevolodoBlagodatskoye village and Sever ouralsk town in 2003 to 2008, in the period when bird distribution is most stable (June to the first half of July). No less than 5 km of census routes per habitat were covered over each 15day observation period. On the whole, 15 unbuilt habitats were surveyed, with censuses in four habitats being repeated every year. The total route length reached 405 km. Calculations of bird species abundance per square kilometer were made with regard to groupaverage range of spotting (Ravkin and Dobrokhotov, 1963; Ravkin, 1967). Censuses of small mammals were taken using 50m catching fences with five cylinder traps (Okhotina and Kostenko, 1974) in the periods of their highest abun dance (July 16–August 31, 2004–2008). On the whole, 25 habitats were surveyed, with censuses in four habitats being taken every year. The total amount of work reached 9960 trap–days. To level off annual differences and make data more reliable, the results of bird and small mammals cen suses were averaged over six groups of habitats: low mountain Siberian stone pine–spruce forests with pine along small river valleys; unevenaged low mountain pine–birch and birch–pine forests with an admixture of aspen; mediumaged lowmountain pine–larch–spruce and Siberian stone pine–spruce– pine forests; lowmountain Siberian stone pine–fir– spruce primary forests; open and crooked birch and
larch forests with Siberian stone pine; moss–lichen tundras combined with dwarf birch and willow scrub, with sparse and suppressed spruce and Siberian stone pine trees. The abundance and distribution of birds and small mammals were scored according to Kuzyakin (1962). The species names of birds are given according to Stepanyan (2003); of small mammals, according to Catalogue of Small Mammals of the Soviet Union (Kata log…,1981), except for the arctic shrew (Sorex arcticus K. 1792), which we name tundra shrew (Sorex tundrensis Merriam 1900) after Okhotina (1983) To revealing DNA of pathogenic microorganisms, unfed adult taiga ticks (about 700 ind.) were collected every year (2004–2008). For parasitic examination and collection of biological samples, small mammals were livetrapped in plots with the highest abundance of I. persulcatus in June to the first half of August (2004, 2005). Birds were caught with mist nets or shot in July to the first half of August (2006, 2007). The ani mals were examined for infestation by ixodid ticks, which were preserved in 70% ethanol for species iden tification. Blood samples of birds and small animals were taken in individual tubes with anticoagulant and cytostatic agents and stored before examination at 4°C (Livanova et al., 2005). A total of 101 birds and 207 small mammals were caught. Seven I. persulcatus lar vae and 61 nymphs were collected from birds; small mammals yielded 97 I. persulcatus larvae and 62 nymphs and, in addition, 9 larvae, 4 nymphs, and 24 adults of the shrew tick, Ixodes trianguliceps Birula, 1895. Indication of nucleic acids of tickborne encepha litis (TBE) virus was carried out only in the samples received from live unfed adult ticks; DNAs of borre liae, anaplasms, ehrlichiae, and babesiae were detected in ticks and blood samples from birds and small mammals by means of PCR followed by sequence analysis of amplicons (Livanov et al., 2005; Tkachev et al., 2007; Fomenko et al., 2008; Rar et al., 2005, 2008). RESULTS Diversity of pathogens The biological materials collected over the period of research in Northern Urals proved to contain the RNA of tickborne encephalitis virus (Far East and Siberian genetic types) and the DNAs of A. phagocytophi lum (genetic variant 2), E. muris, Borrelia garinii, Borre lia afzelii, and Babesia microti (Livanova et al., 2005; Rar et al., 2006; Tkachev et al., 2007, Rar et al., 2008). BIOLOGY BULLETIN
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Distribution of taiga ticks and their probable participation in circulation of pathogenic microorganisms Flagging samples consisted only of taiga ticks According to our data, sustainable populations of this species occur in the Northern Urals up to a latitude of 60°50'. Only single findings were reported from areas lying farther north (up to 61°20') (Livanova, Livanov, 2006). Over the entire study period, the relative abun dance of I, persulcatus ticks within their sustainable range averaged 7 ind./flag–km, ranging from 0.4 to 18 ind./flag–km. Its relatively high values (3.5– 7.2 ind./flag–km) were recorded on the southern slopes overgrown with pine–birch and birch–pine unevenage forests with aspen. The distribution of ticks in young (up to 70 years) birch–pine and pine– birch forests and forest plantations was relatively even. In young cutover areas being overgrown mainly by smallleaved tree species, ticks occurred in small patches alternating with tickfree areas. Their abun dance was reduced to 0.23.5 ind./flag–km in over growing areas of different ages on northeastern slopes and also in mature and ripening pine forests on slopes of different exposure. In mediumaged pine–larch– spruce, Siberian stone pine–spruce–pine, and Sibe rian stone pine–fir–spruce primary forests, ticks occurred only along overgrowing tracks. All the above habitats were at elevations of no more than 300 m a.s.l. Nucleic acids of pathogenic microorganisms were found in ticks from year to year. Slightly more than 16% of all ticks examined (52 ind.) contained DNA of a certain pathogen. The RNA of TBE virus was revealed in six samples (2%); the DNA of A. phagocy tophilum, in one tick (0.3%); and the DNA of Å. muris, in 17 ticks (5.4%). As compared to anaplasms and ehr lichiae, borreliae of the B. burgdorferi s. I. group occurred in ticks more often: over the study period, their DNA was detected in 34 ticks (10.7%). Distribution of warmblooded hosts, their roles in taiga tick feeding, and pathogen species associated with them A total of 144 bird species were recorded in the study region. Their total abundance in the forest belt varied from 263 to 447 ind./km2; its values in the crooked–light forest and tundra belts were 284 and 68 ind./km2, respectively. In forests (including crooked and light forests), dominant species occurring in different combinations were as follows: the willow tit (Parus montanus Baldenstein), green warbler (Phyl loscopus trochiloides Sundevall), brambling (Fringilia montifringilla L.), olivebacked pipit (Anthus hodgsoni Richmond), and red crossbill (Loxia curvirostra L.). Species dominating in midmountain moss–lichen tundras of the goltsy belt included common redpoll (Acanthis flammea L.), rock ptarmigan (Lagopus mutus Montin), nutcracker (Nucifraga caryocatactes L.), BIOLOGY BULLETIN
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and, in some years, meadow pipit (Anthus pratensis L.) and golden plover (Pluvialis apricariah.). Larvae and nymphs of I. persulcatus were found on birds of 9 out of 25 species examined. The larvae were collected from about 7% of birds, their abundance index varying from 0.08 to 0.6. Infestation by single larvae was noted for the robin (Erithacus rubecula L.), the bird common in all forests (2–7 ind./km2), as well as for the redwing (Turdus iliacus L.) and song thrush (Turdus philomelos C.L. Brehm), which are also com mon in forested habitats (2–7 ind./km2). The larval abundance index for these birds was no more than 0.08. Infestation by nymphs was slightly higher, with their abundance index for all birds averaging 3.7. For the dunnock (Prunella modularis L.), recorded only in forests with prevalence of dark conifers, the abun dance index of nymphs was 5. For the redwing and common rosefinch (Carpodacus erythrinus Pallas), a typical inhabitant of forest margins, this index was 3. Nymphs were found on the bullfinch (Pyrrhula pyr rhula L.), a widespread and numerous species in all forested habitats (13–22 ind./km2). The nymph abun dance index for the olivebacked pipit was 5. Birds of this species are ubiquitous and, as a rule, fairly numer ous (2–36 ind./km2). Fourteen nymphs were collected from the little bunting (Emberiza pusilla Pallas), which was recorded in pine–larch–spruce and Siberian stone pine–spruce–pine forests, where it was rare (0.3 ind./km2), and also in light mixed forests, crooked forests, and tundras (3 ind./km2). A notewor thy fact is that ticks were found on the nightjar (Caprimulgus europaeus L.), an extremely rare species in the study region. Thus, taiga ticks in the Northern Urals were collected from 15 birds of 9 species (14.9% of the total). Blood analysis revealed the presence of the DNA of Erlichia spp. in only one sample, which was taken from a little bunting. Eight species of insectivores and nine species of murine rodents were recorded in the study area. Their total abun dance in forests varied from 40 to 147 ind./100 trap–days, reaching peak values in lowmountain Siberian stone pine–fir–spruce forests with patches of pine stands along small river valleys. In crooked and light forests, their abundance was 97 ind./100 trap–days, and in tundras, 93 ind./100 trap–days. Species dominating in forest included the common (Sorex araneus L.), Lax mann’s (S. caecutiens L.), taiga (S. isodon Ò.) and pygmy (S. minutus L.) shrews; northern redbacked (Clethrionomys rutilus P.), bank (Cl. glareolus Schreber), and gray redbacked (Cl. rufocanus Sun dervall) voles; and northern birch mouse (Sicista betu lina P.). In birch forests and crooked and open larch and stone pine forests, and light forests, the group of dominants included three shrew species (S. araneus, S. caecutiens, and S. isodon) and two vole species, Cl. glareolus and Cl. rutilus. The above three shrew spe cies were also dominant in tundras.
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Table 1. Role of small mammals as feeding hosts for larvae and nymphs of the taiga tick in the Northern Urals (2004–2005) Number of animals Species
Abundance index
examined
parasitized by ticks, %
larvae
nymphs
60 2 8 41 96 207
2.9 0.9 0.9 5.8 13.0 22.7
0.5 1 0.8 0.4 0.9 0.5
0.02 0 0 0.3 0.5 0.3
Common shrew (Sorex araneus) Tundra shrew (S. tundrensis) Gray redbacked vole (Clethrionomys rufocanus) Bank vole (Cl. glareolus) Northern redbacked vole (Cl. rutilus) Total
Table 2. Occurrence of DNAs of different microorganisms in blood samples from small mammals (2004–2005) Number of positive samples voles DNA
Anaplasma Ehrlichia Borrelia Babesia Total by species
common shrews (n = 60) 6 1 0 8 15
gray redbacked (n = 8)
bank (n = 41)
northern redbacked (n = 96)
total (n = 207)
2 1 0 5 8
5 2 5 13 25
26 7 5 22 60
39 11 10 48 –
Preimaginal phases of the taiga tick were found on small mammals of seven species. Over the study period, 97 larvae and 62 nymphs were collected from approximately 23% of these animals. Larvae were found on 15% of small mammals belonging to five spe cies (Table 1), including 3% of common shrews (abun dance index 0.5). These insectivores are widespread and numerous throughout the study region (29– 61 ind./100 trapdays), reaching a peak of abundance in tundras (101 ind./100 trap–days). Likewise, tick larvae were collected from 17% of northern red backed voles, with their abundance index being slightly below 1 (Table 1). Northern redbacked voles are widespread in Northern Urals. In particular, they were common in unevenaged lowmountain pine– birch and birch–pine forests (6 ind./100 trap–days) and tundras (5 ind./100 trap–days) and abundant in other landscape compartments (16–33 ind./100 trap– days). Bank voles were attacked by tick larvae half less frequently than northern redbacked (7%). This spe cies could be classified as common in the greater part of the study region (2–9 ind./100 trap–days), being abundant only in lowmountain Siberian stone pine– fir–spruce forests along small river valleys (14 ind./100 trap–days). Among gray redbacked voles, tick larvae were found on one out of eight animals examined. This species was common almost everywhere (2–4 ind./100 trap–days). However, it was rare in unevenaged birch
forests and pine forests with birch and aspen (0.9 ind./100 trap–days) and abundant in dark conifer forests along small river valleys (16 ind./100 trap– days). The role of shrews in the feeding of taiga tick nymphs in the Northern Urals is negligible: over the entire study period, only one nymph was collected from a common shrew. The prevalence of nymphs on northern redbacked voles reached 32%. Indices of their abundance on various small mammal species are shown in Table 1. In the bank vole, compared to the previous species, the proportion of individuals parasit ized by tick nymphs was half smaller (15%) In addi tion, by one nymph was collected from a northern birch mouse and a field vole (Microtus agrestis L.). Northern birch mice were found in all habitats sur veyed (0.5–5 ind./100 trap–days), with their abun dance reaching a peak of 17 ind./100 trap–days in light and crooked forests. Field voles, being common almost everywhere (1–5 ind./100 trap–days), were rare in forests near rivers (0.9 ind./100 trap–days) and absent in mountain tundras. It is noteworthy that larvae and nymphs of the taiga tick were found on the tundra shrew, a very rare species in the study area: only two animals were livetrapped accidentally (not during census) in lowmountain spruce forest near a river in 2005. BIOLOGY BULLETIN
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Table 2 shows data on the occurrence of DNAs of pathogenic microorganisms in blood samples from different small mammal species. In common shrews, the DNA of Babesia microti was detected most fre quently (in 13% of animals examined); 10% of animals contained the DNA of anaplasms, and the DNA of ehrlichiae was detected in only one blood sample. Gene fragments from all test pathogens were found in blood samples from voles of the genus Clethriono mys, especially northern redbacked voles (62.5%). Blood samples from this species contained the DNAs of anaplasms (27.1%), babesiae (22.9%), and ehrli chiae (E. muris), with the last one occurring four times less frequently than the DNA of A. phagocitophilum. Borrelia infection could be suspected in slightly more than 5% of northern redbacked voles. The analysis of blood samples from bank voles has shown that animals of this species probably participate in the maintenance of circulation of all pathogenic microorganisms whose DNA has been detected. In gray redbacked voles, analysis for Borrelia DNA of the B. burgdorferi s. l. group produced no positive results, which could be explained by an insufficient number of animals tested. DISCUSSION AND CONCLUSIONS As follows from our data, the population of adult taiga ticks in the Northern Urals is not large. In the Cisural region, for example, this indices of I. persulca tus abundance in overgrowing cutover areas vary from 139 to 547 ind. per kilometer of the census route (Lykov and Mitrofanova, 1971); in pine–birch and mixed conifer–broadleaf forest of the Middle Urals, this parameter is 12–31 ind./flag–hour (Ponomarev, 1974). In the region of our study, the highest indices of abundance are characteristic of wellwarmed habitats with prevalence of birch and aspen. The abundance of ticks decreases upon transition from southern to northern slopes and with increase in elevation. In contrast to more southern regions, where humidity plays an especially important role, the distri bution of taiga ticks in the Middle Ural largely depends on heat supply. Economic activities in forests apparently contribute not only to the expansion of ticks northward but also to the maintenance of natural foci of infections. In comparison with the Middle and Southern Urals (Livanov et al., 2004), the bird community of the Northern Urals is generally less abundant. Moreover, none of the nine species found to be parasitized by tick larvae and nymphs, except for the olivebacked pipit, is dominant in the habitats surveyed. The abundance of the majority of such species is relatively low (no more than 7 ind./km2). Unlike in the Northern Urals, preimaginal phases of ticks in the Middle Urals were found birds of 26 spe cies, with their abundance index varying from 0.01 to 1.6 and occurrence frequency in some species reach ing 80% (Shilova et al., 1963). BIOLOGY BULLETIN
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The absence of DNAs of pathogenic microorgan isms in blood samples from birds caught in the North ern Urals is most probably explained by a low tick infestation rate. No positive results were also obtained in studies on assessing the prevalence of Borrelia in birds in the central Cisural region (Korenberg et al., 2002). On the other hand, the results of studies in the range of the sheep tick (Ixodes ricinus L.) provide evi dence for the ability of birds to receive and successfully transmit various pathogens to ticks feeding on them (Bjorsdorf et al., 2001; Pichon et al., 2006). Thus, the role of birds as reservoir hosts for pathogenic microor ganisms and feeding hosts food support for the taiga tick in the study region is insignificant. In general, the species richness of small mammals in the Northern Urals is lower than in the Middle and Southern Urals (Chernyavskaya, 1959; Berdugin, 1999). Bolshakov et al. (1986) recorded 28 species of small mammals in different parts of the Southern Urals. In the Middle Urals, the fauna of insectivores and murine rodents is represented by 9 and 15 species, respectively (Flora…, 2003). In the Northern Urals, common shrew is a ubiquitous dominant, with its rel ative abundance in late July and August being signifi cantly than that of any other insectivore or murine rodent species and the degree of its dominance in communities increasing in the Northern Urals, com pared to the Southern Urals (Bol’shakov et al., 1996). At the same time the role of these animals as feeding hosts for taiga tick larvae and nymphs is insignificant, since these arthropods parasitize mainly Clethrionomys voles, Cl. rutilus and Cl. rufocanus. The former species in the study area regularly occurs in all habitats sur veyed, with primary dark conifer forests being optimal for it. In plots consistently inhabited of taiga ticks (unevenaged lowmountain pine–birch and birch– pine forests with aspen), the abundance of northern redbacked voles is lower than in other forested land scape tracts, but it is sufficient for providing preimagi nal ticks with food. Bank voles are less abundant but also occur everywhere in the study region. They prefer forests growing in mountain valleys and are relatively sparse in areas consistently inhabited by ticks. There fore, bank vole play a secondary role as their feeding hosts. In general, the range of small mammals providing food for preimaginal phases of the taiga tick in the Northern Urals is approximately the same as in the Middle Urals (Zalutskaya, 1967; Kovalevskii et al., 2004). However, the abundance of ticks on these hosts in the Middle Ural province is significantly higher: in the Sverdlovsk and Perm regions, for example, the abundance index reaches 10 in certain years (Shilova et al., 1963; Zalutskaya, 1967). Relatively rare occurrence of B. burgdorferi s. l. DNA in small mammals of the Northern Urals is probably due to low abundance of taiga tick nymphs on murine rodents and their almost complete absence on shrews. For comparison, bacteriological data show
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that the occurrence frequency of animals infected by Borrelia in the central Cisural region reaches 50% (Kovalevskii et al., 2004). The occurrence frequency of A. phagocytophilum DNA in the blood of small mammals in the Northern Ural proved to be relatively high (17%) against the background of its extremely low values in vectors. In the Khabarovsk Region, where this DNA occurs in small mammals with approximately the same fre quency (18%), the proportion of anaplasmpositive taiga ticks is markedly higher and reaches 4% (Rar et al., 2008). Small mammals in the Northern Urals probably participate in the maintenance of natural foci of monocytic ehrlichioses. The DNA of these microor ganisms occurs most frequently in blood samples from northern redbacked voles. As follows from our results, the main role in the circulation of babesiae in the Northern Urals is apparently played by northern redbacked and bank voles. These microorganisms were recorded for the first time in the blood of bank voles from the Central Urals (Telford et al., 2002). In the same region, the DNA of B. microti was revealed in seven more species of small mammals (Morozov et al., 2007). Thus, the abundance of tick vector and small mam mals in the surveyed region of the Northern Urals is lower than in more southern parts of the Urals, but pathogenic microorganisms transmitted by ticks are the same. The data obtained in this study indicate that natural foci of TBE, ixodid tickborne borrelioses, and human monocytic ehrlichiosis possibly exist in the Northern Urals. Relatively high frequency of A. phagocytophilum DNA in blood samples from small mammals and rare cases of its detection in the vector suggest that this pathogen can circulate in the study region. Specific features of circulation of babesiae, whose DNA has been detected in the blood of many animals but not in any sample of taiga ticks, require further study. REFERENCES Alekseev, A.N., Dubinina, H.V., van de Pol, I., and Schouls, L.M., Identification of Ehrlichia spp. and Borrelia burgdorferi in Ixodes Ticks in the Baltic Regions of Russia, J. Clin Microbiol., 2001, vol. 39, pp. 2237–2242. Alekseev, A.N., Semenov, A.V., and Dubinina, H.V., Evi dence of Babesia microti Infection in MultiInfected Ixodes persulcatus Ticks in Russia, Exp. Appl. Acarol., 2003, vol. 29, pp. 345–353. Berdyugin, K.I., Rodent Communities of the Northern Urals, Ekologiya, 1999, no. 2, pp. 138–144. Bernshtein, A.D., Apekina, N.S., Kopylova, L.F., Myasni kov, Yu.A., and Gavrilovskaya, I.N., Comparative Ecologi cal–Epizootiological Characterization of Clethrionomys Voles in the Middle Cisural Region, Zool. Zh., 1987, vol. 66, no. 9, pp. 1397–1407.
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