Annals of Parasitology 2012, 58(3), 125–155 Copyright© 2012 Polish Parasitological Society

Review articles

Ticks of . Review of contemporary issues and latest research.

Magdalena Nowak-Chmura, Krzysztof Siuda

Department of Invertebrate Zoology and Parasitology, Institute of Biology, Pedagogical University of Cracow, 3 Podbrzezie Street, 31-054 Kraków, Poland

Corresponding author: Magdalena Nowak-Chmura; E-mail: [email protected]

ABSTRACT. The paper presents current knowledge of occurring in Poland, their medical importance, and a review of recent studies implemented in the Polish research centres on ticks and their significance in the epidemiology of transmissible diseases. In the Polish fauna there are 19 species of ticks (Ixodida) recognized as existing permanently in our country: reflexus, Argas polonicus, Carios vespertilionis, trianguliceps, Ixodes arboricola, Ixodes crenulatus, Ixodes hexagonus, Ixodes lividus, Ixodes rugicollis, Ixodes caledonicus, Ixodes frontalis, Ixodes simplex, Ixodes vespertilionis, Ixodes apronophorus, Ixodes persulcatus, , punctata, Haemaphysalis concinna, reticulatus. Occasionally, alien species of ticks transferred to the territory of Poland are recorded: sphenodonti, Amblyomma exornatum, Amblyomma flavomaculatum, Amblyomma latum, Amblyomma nuttalli, Amblyomma quadricavum, Amblyomma transversale, Amblyomma varanensis, Amblyomma spp., Dermacentor marginatus, aegyptium, , Ixodes eldaricus, Ixodes festai, rossicus, Rhipicephalus sanguineus. The most common species of the highest medical and veterinary importance in Poland is invariably Ixodes ricinus . The review also sets out information on the risks of - borne diseases in recreational areas of large cities in Poland, ticks as the cause of occupational diseases and dangerous species of ticks attacking people outside the Polish borders. Selected problems of the biology of ticks, the spread of alien species transferred on hosts and prevention of tick attacks have also been presented. The Polish studies on ticks are a valuable contribution to global research on the Ixodida.

Key words: tick, Ixodida, Poland, epidemiology

The aim of this paper is to present up-to-date their numerous species attack also , their state of knowledge about the fauna of ticks in parasitizing can cause very serious negative Poland and their ability to transmit pathogens. The medical, veterinary and economic consequences. latest release of the full list of ticks occurring in Two life phases are distinguished in the Poland was published as a monograph 19 years ago development of each active stage of ticks: the [1]. The fauna of ticks does not change remarkably parasitic phase, in which the tick embedded in the fast, and in the zoological and parasitological host gets the food, especially blood from the body of literature there is still relatively little work in the the host, and the non-parasitic phase in which the field of , systematics and faunistics of tick usually lives in nature without close association ticks. However, noteworthy information is with the host. Adaptation to external and temporary continually collected about the biology and ecology, parasitic lifestyle of ticks is clearly marked in the the transfer of alien species of these parasites into formation of sensory organs, the structure of the the Polish territory and the epidemiological integument and digestive system, as well as feeding importance of ticks occurring in Poland. strategy and association of the habitat with the host. Because ticks are obligate, external and An invariably important aspect increasingly temporary parasites of terrestrial vertebrates, and promoted in Poland is prophylaxis against ticks and 126 M. Nowak-Chmura, K. Siuda dissemination of information to society groups who, occasionally recorded as transferred to the Polish for professional, tourist or other reasons, stay in territory are entered into the database „Alien species areas of occurrence and feeding grounds of ticks. in Poland” (www.iop.krakow.pl/ias). The most Enhancing public awareness about the dangers common species of the highest medical and posed by tick attacks and disease transmission is veterinary importance in Poland and almost all over increasingly being promoted by various media, is still Ixodes ricinus (Linnaeus, 1756). which is beneficial and essential in prophylaxis. However, the main responsibility lies with academic Distribution of ticks on Earth and in Poland lecturers who prepare teachers of biology and nature to work in schools with children and adolescents, as Ticks inhabit all types of terrestrial well as doctors of medical and veterinary sciences. environments, from tropical to sub-polar regions, from the sea level to high mountain ice zone, in Systematic classification of ticks and highly humid habitats, but also on the steppes, semi- representatives in the world fauna deserts and deserts where few other haemato - phagous survive. In tropical countries Ticks are classified in a separate order Ixodida, tick species representation is richer, but in our superorder , class Arachnida, latitudes with a small number of species they can subphylum , phylum Arthropoda. also reach very high abundance. An example would Currently, the order Ixodida is divided into two be the size of the Polish common tick population. suborders: Argasina and Ixodina. Suborder Cases were recorded when propitious for ticks Argasina with one family and two microclimatic conditions in the habitat and host subfamilies: Argasinae with one genus Argas (57 availability resulted in abundance of I. ricinus species) and Ornithodorinae with genera Carios (88 exceeding 100 specimens per 100 square meters. species), (37 species) and Otobius (3 Argasidae are more thermophilic. It is generally species); suborder Ixodina with three families; accepted that the northern border of their range in Nuttalliellidae with subfamily Nuttalliellinae Europe extends along the 50 °N, but in Poland two including a single genus and species Nuttalliella species expand further to the north: Argas reflexus namaqua Bedford, 1931; with subfamily Fabricius, 1794 and Carios vespertilionis Latreille, Ixodinae and one genus Ixo des (249 spe cies); Am- 1802. Ixodidae have a more global range reaching blyom mi dae with sub fa mi lies and ge ne ra: Am - beyond the polar circles, where exists widespread blyom mi nae: Am blyom ma (142 spe cies), Cor nu pal- Ixodes (Ceratixodes ) uriae White, 1852, a pa tum (1 spe cies Cor nu pal pa tum bur ma ni cum Po - nidicolous parasite of marine birds. inar et Bron, 2003), Bo th rio cro to ni nae: Bo th rio cro - All species of ticks occurring in Poland have ton (5 spe cies), Ha ema phy sa li nae: Ha ema phy sa lis probably been already identified, but knowledge of (166 spe cies), Hy alom mi nae: Hy alom ma (25 spe- their distribution in our country is inadequate. Most cies) and No som ma (1 spe cies – No som ma mon stro- information is available on I. ricinus – the most sum (Nut tall et War bur ton, 1908)), Rhi pi ce pha li nae common and most easily collected species in with ge ne ra: Ano ma lo hi ma laya (3 spe cies), Co- Poland. Likewise, distribution of Dermacentor smiom ma (1 spe cies – Co smiom ma hip po po ta men- reticulatus (Fabricius, 1794) in Poland is relatively sis (Den ny, 1843)), Der ma cen tor (36 spe cies), Mar- well-known, and recent studies have shown that its ga ro pus (3 spe cies), Rhi pi cen tor (2 spe cies) and range of occurrence is much more extended in Rhi pi ce pha lus (79 spe cies). western Poland than expected [3,4]. There are also other monographs on world’s tick Specific microclimatic conditions of the habitat fauna in which researchers generally agree on the have an effect on selection of living space by ticks. actual existence of 896 species of ticks, while still Consequently, in case of many species their debatable is the taxonomic division into genera and presence in the area of coverage is restricted to a higher systematic units of the Ixodida order [2]. number of „islands” and „islets”. An example is Worldwide tick fauna comprises about 900 dispersion of I. ricinus ticks, which are usually not recognized species, of which 77 belong to the evenly distributed within the habitat and their European fauna. Currently, the Polish fauna number may change even at intervals of a few includes 19 species of ticks (Ixodida) identified as meters – the so called „mosaic distribution”. permanent residents in our country, and the species Ticks of Poland 127

Fauna of ticks in Poland and their ability to cases of attacking other bird species by A. reflexus transmit pathogens have been reported. It often attacks people, especially in cases where there is no access to Family Argasidae pigeons. Behaviour and activities (annual rhythm, Argas (Argas ) polonicus Siuda, Hoogstraal, circadian rhythm) of A. reflexus are similar to those Clifford et Wassef, 1979 . In Poland the localities of of A. polonicus . Parasitizing ticks cause in infested this species have been found in Cracow (in the humans stress, allergic reactions and toxicoses Śródmieście and Podgórze ). The attic of St. (oedema and erythema, itching, pain, fever, Mary’s Church is locus typicus of this species [5]. weakness, nausea, diarrhoea, dizziness, headaches, Several foci have been registered in the Czech anxiety, increased heart and breathing rate, fainting Republic and [6]. A. polonicus is a nests- with varying degrees of severity), which may pose and burrows-dwelling parasite. It exists mainly in threat to health and even lives of victims [69–71] synanthropic habitats in towers and attics of (Table 1). Large populations of A. reflexus threaten buildings, where its main hosts are rock pigeons farms of pigeons which die when attacked en masse. (Columba livia ) [5,6], but incidents of attacks on Pigeons abandoning nests with nestlings have also humans have also been recorded [7,8]. In Cracow, been observed [72]. the one peak annual activity cycle of A. polonicus Carios vespertilionis Latreille, 1802. In Poland begins in early April and lasts until the end of localities of this species are recorded across the October. Maximum abundance falls in July and country [1,73]. C. vespertilionis belongs to a nests- August and during warmer summers to early and burrows-dwelling type of species, parasitizing September. Throughout the entire period of activity bats in natural, synanthropic and semi-synanthropic all developmental stages are observed in various habitats where it hides in the cracks of walls of states of repletion. The larvae are more numerous in buildings and caves, also under piles of guano. late summer (predominantly unfed specimens) and Moreover, it is found in tree hollows inhabited by spring (most replete specimens). A. polonicus is a bats. The annual rhythm of activity in the parasite of nocturnal activity. It feeds in a manner acquisition of hosts in Central Europe is not fully typical of ticks, i.e. the larvae slowly for about 6 understood; in the circadian rhythm ticks are active days, nymphs and adults quickly, from several during the day. The argasids can attack humans minutes to about 2 hours. They spend the day hiding [17,74] (Table 1), but in Poland no such case has in cracks in beams and walls; usually in one crevice been reported. a few specimens in different developmental stages and different repletion states are gathered. Family Ixodidae Predominantly nocturnal activities of these ticks and Ixodes (Exopalpiger ) trianguliceps Birula, their absence at the ground level of St. Mary’s 1895. In Poland I. trianguliceps occurs across the Church do not pose the risk of attacking people who country (from the subalpine zone of the Tatra visit the church during the day. However, tick mountains to the coast of the Baltic Sea) and is one attacks on trumpeters performing night shifts on the of the most common parasites of small mammals church tower have been reported [1,8]. Studies to [1,75,76]. Most of localities of I. trianguliceps in date on the role of A. polonicus as a vector of Poland are found in the foothills and mountain transmission of disease pathogens have been areas. It lives in moderately humid habitats, mostly negative. Direct adverse effects of attacks by soft in shady mixed and deciduous forests. There is no ticks of the genus Argas are shown in the table evidence of existence of these ticks in the swamp (Table 1). forests with heavily watered ground and in dry Argas (Argas ) reflexus (Fabricius, 1794). On woods, on sandy soil with a thin layer of litter and the Polish territory most localities of A. reflexus are bare grassland sites. It is out of nest dwelling found to the west of the Vistula River, it is probably parasite and polyphagous species of a three-host a common tick in the western part of Poland. A. development cycle. It feeds mainly on small reflexus is a nests- and burrows-dwelling parasite. mammals (about 50 species); among its hosts All the known Polish localities are found in several species of birds and a viviparous lizard synanthropic habitats (attics, church attics, houses (Lacerta vivipara ) have been reported [1]. Adult and lofts), in all places where pigeons nest, the main ticks are active from April to October, nymphs from hosts of these ticks [1,68]. Outside Poland sporadic April to September, and the larvae for the whole 128 M. Nowak-Chmura, K. Siuda year [77]. It is believed that I. trianguliceps is the epidemiology of transmissible diseases in Europe main vector and the reservoir of tick-borne (Table 1). encephalitis virus (Togaviridae: Flavivirus ) among Ixodes lividus Koch, 1844 . I. lividus occurs populations of small mammals (Table 1). across the whole of Poland. It is a nidicolous Ixodes (Pholeoixodes ) arboricola Schulze et parasite, specifically ornithophillic, closely related Schlottke . I. arboricola probably occurs across the to the Riparia riparia . It nests in burrows carved in whole of Poland, but most of the localities of the the ground by these birds. In Poland it is most ticks have been recorded in the western part of the frequently recorded in the central and northern country. I. arboricola is a nests- and burrows- parts. I. lividus has a one-year life cycle involving dwelling parasite, strictly ornithophilic, associated three hosts and is time-dependent on the nesting and with birds nesting in tree hollows and bird booths, development rhythm of R. riparia . It may be rarely in burrows carved in the ground. In Central important in transmission of pathogens (Table 1). and Western Europe I. arboricola attacks hosts Ixodes (Pholeoixodes ) rugicollis Schulze et throughout the year, its abundance falls in the Schlottke, 1929 . Geographical borders of winter, the maximum activity of females is in the I. rugicollis are not fully known. In Poland its spring, in other seasons there is preponderance of prevalence has been found near Wroclaw [83] and larvae and nymphs, adult males do not feed [78]. Przemyśl [84]. I. rugicollis is a nests- and burrows- There is little data about the medical, veterinary and dwelling parasite of a three-host development cycle. economic importance of I. arboricola (Table 1). It lives in burrows and shelters, mostly of predatory Ixodes (Pholeoixodes ) crenulatus Koch, 1844 . mammals of the family Mustelidae. In Poland cases In Poland over a dozen localities have been recorded of I. rugicollis parasitism have been detected on across the country. This is a nests- and burrows- dogs and cats. No data on the epidemiological dwelling parasite, dwelling in burrows of rodents importance of I. rugicollis is available. and predatory mammals, also found in caves. The Ixodes (Scaphixodes ) caledonicus Nuttall, hosts of immature stages and females are 1910 . Localities of I. caledonicus are rarely insectivorous mammals, rodents, predatory recorded, in Poland found in Pomerania, a parasite mammals and birds in contact with mammal of Apus spp. [85]. I. caledonicus is a nests- and burrows. Adult males do not attack a host. These burrows-dwelling parasite, absolutely ticks may attack humans, domestic and ornithophillic. It attacks birds nesting and living in livestock: dogs, cats, horses, sheep. In annual the rocky hideouts. Biology of this species and its rhythm the highest intensity of invasion of females medical and veterinary importance are poorly and immature stages of I. crenulatus is recorded in known. spring (April), followed by reduction in the intensity Ixodes (Trichotoixodes ) frontalis (Panzer, of invasion in summer, and its increase again in 1798 ). In Poland the occurrence of I. frontal is has autumn. Medical and veterinary importance of this been identified on the Vistula Spit [86] and on birds species is little known (Table 1). during their spring migration (own unpublished Ixodes (Pholeoixodes ) hexagonus Leach, 1815 . studies). I. frontalis is an absolutely ornithophillic, In Poland it is likely to occur across the whole out of nest dwelling parasite with a three-host country, but most of the known foci are situated in development cycle. It attacks ground feeding birds the southern Poland. The largest concentration of that nest in trees. The importance of this species in these ticks has been observed at a beaver farm in the epidemiology has been demonstrated (Table 1). Popielno in Masuria [1,79,80]. This nests- and Ixodes (Pomerantzevella ) simplex Neumann, burrows-dwelling parasite inhabits different types 1906 . In Poland one location in Bukowiec near of hollows, also in buildings, in caves, rock shelters Nowy Sącz is known [87] Subsequent studies on and dog kennels [1,81]. There is no precise data on ticks parasitizing bats have not shown the increase the course of the seasonal rhythm of activity of I. in the number of localities of I. simplex in Poland hexagonus on the Polish territory. In the United [73]. It is a nests- and burrows-dwelling tick, a Kingdom these ticks are active throughout the year parasite of bats, living in caves and grottos, and its with increased activity of the attacks on hosts in main host is considered to be the bat Miniopterus April and May, and from August to October [78]. I. schreibersi . In Poland it has been collected from hexagonus is counted among the species causing Myotis myotis [87]. There is no data of medical and tick paralysis [82], and is important in the veterinary importance. Ticks of Poland 129

Ixodes (Eschatocephalus ) vespertilionis Koch, mammals, birds and reptiles. It prefers warm- 1844. In Poland 22 sites have been registered, one in blooded hosts, all active stages attack Samogoszcz in Mazovia, others in caves in the humans, mostly nymphs and females. I. ricinus is Polish Jura Krakowsko-Częstochowska and in the counted among the arthropods of the greatest Carpathians [73]. I. vespertilionis is a nests- and significance in the epidemiology of transmissible burrows-dwelling oligoxenous parasite of bats with diseases (Table 1). three-host development cycle. The course of the Family Amblyommidae seasonal cycle of activity is closely associated with Haemaphysalis (Aboimisalis ) punctata the rhythm of activity and hibernation of bats. Canestrini et Fanzago, 1877. In Poland two Females and immature forms attack hosts from localities have been registered in West Pomerania November to May, adult males do not feed. There is [93,94]. H. punctata is a polixenic, out of no data on their medical and veterinary importance. nest dwelling parasite of a three-host development Ixodes (Ixodes ) apronophorus Schulze, 1924 . cycle. Larvae and nymphs attack mainly small-sized The distribution of this species in Poland is little animals (mammals, birds, domestic fowls among known, several localities have been registered in others), hosts of the adult forms are mainly domestic Pomerania, Masuria, in the Białowieża Forest and in and wild ungulates, in Poland it has been collected the Lublin region [80,85,88–90]. I. apronophorus is from cows [93]. H. punctata attacks also humans a three-host, nests- and burrows-dwelling, and can cause tick paralysis in the host [82] (Table hygrophilous parasite occurring in wetlands, 1). overgrown banks of water reservoirs, muddy rivers Haemaphysalis (Haemaphysalis ) concin na and streams, islands and islets, marshes and swamps Koch, 1844. In Poland one locality of H. concinna with sedge clumps in which it lives in the nests and has been recorded in Troszyn in West Pomerania burrows of small mammals and birds [1]. Adult [93]. H. concinna lives in well-lit, thin, moist males probably do not feed. The ability of this deciduous and mixed forests with rich bushy species to transmit pathogens has been undergrowth, forest steppes and wet steppe habitats, demonstrated (Table 1). overgrown lake districts and river valleys. It is also Ixodes (Ixodes ) persulcatus Schulce, 1930 . found in thickets of reeds on the banks of lakes [95]. Poland is outside the compact range of H. concinna is a polixenic, exophilic parasite of I. persulcatus , a few records of the tick have been three-host development cycle. Its hosts are reported from the Białowieża Forest [85,91]. I. numerous species of reptiles, birds, mammals and, persulcatus is out of nest dwelling parasite of a among others, domestic cattle, goats and sheep. three-host development cycle. It is a species with a Humans are attacked by nymphs and adult ticks. In broad food specificity and can attack all species of Slovakia adult H. concinna are active from mid- terrestrial vertebrates, including humans. The April to mid-August with maximum activity in species is of great medical and veterinary June, nymphs from mid-April to mid-October, importance (Table 1). larvae from late May to mid-October [95]. All Ixodes (Ixodes ) ricinus (Linnaeus, 1758). In active development stages are active day and night. Poland it exists throughout the country, hundreds of High epidemiological importance of these ticks has locations have been recorded [92]. It occurs in damp been demonstrated (Table 1). habitats (about 80-100% relative humidity), mainly Dermacentor (Dermacentor ) reticulatus in deciduous and mixed forests, or bushy thickets. (Fabricius, 1794). In Poland most of the known These ticks are not usually found in dry pine forests locations are found in the north-eastern and eastern on sandy soils and coniferous forests without parts of the country [1,44,96], but also in the undergrowth. It does not occur in swamps and bogs. western Poland natural occurrence of D. reticulatus I. ricinus ticks are unevenly distributed in habitats, has been recorded [3,4,97]. In Poland D. reticulatus and their number may change every few meters. exists mainly in wooded or bushy valleys of rivers, They tend to gather along narrow roads and forest streams and drainage channels, in mixed swamp paths overgrown with grass vegetation along animal forests, mid-forest glades and meadows, clearings trails where they have a greater chance of contact and bushy pastures on small hills among marshes with the host. I. ricinus is out of nest dwelling covered with gray willow [98]. D. reticulatus is a parasite of three-host development cycle with broad polygenic, nests- and burrows-dwelling parasite of food specificity. It attacks terrestrial animals, three-host development cycle. Immatures live in 130 M. Nowak-Chmura, K. Siuda burrows and corridors of burrows of small Migration of ticks beyond their natural mammals. The hosts of adult D. reticulatus are range medium-sized and large mammals. It rarely attacks humans, but is important in the epidemiology of In Poland sporadic cases of natural and unnatural transmissible diseases (Table 1). transfer of alien tick species whose natural range of

Table 1. Medical significance of ticks occurring in the Polish fauna

Species Medical significance References localized allergic skin reactions, systemic allergic reactions manifesting as generalized urticaria and asthma; transmission: tick-borne encephalitis Argas reflexus virus, Grand Arbaud virus and Ponteves virus, Crimean-Congo [9–12] hemorrhagic fever, Coxiella burnetii , Salmonella enteritidis ; it can cause tick paralysis in the host local allergic skin reactions similar to the effects of A. reflexus attack, Argas polonicus [10] no data on transmission of pathogens in humans local mild itching lasting several weeks, transmission: Carios vespertilionis tick-borne encephalitis virus, Sokuluk virus, Issyk-Kul virus, [13-18] Borrelia burgdorferi s. l., Coxiella burnetii , Wolbachia sp. Argas spp. transmission: Borrelia anserina, Anaplasma (Aegyptianella ) pullorum [19] transmission: tick-borne encephalitis virus, Borrelia burgdorferi s. l., Ixodes trianguliceps B. afzelii, B. garinii, Coxiella burnetii , Anaplasma phagocytophilum, [10, 19-23] Babesia microti transmission: Borrelia burgdorferi s. l., Rickettsia spp., involved in the Ixodes arboricola [24,25] spread of ornithosis in birds transmission: Coxiella burnetii, Yersinia pestis; it can cause tick paralysis Ixodes crenulatus [26] in the host transmission: tick-borne encephalitis virus, Borrelia burgdorferi s.l ., Ixod es hexagonus Anaplasma phagocytophilum , Rickettsia helvetica , R. conorii , Babesia [10,19,27] canis, B. divergens, B. microti; it can cause tick paralysis in the host transmission: the virus of Russian spring-summer encephalitis, Kama Ixodes lividus [26,28,29] virus , Coxiella burnetii , Rickettsia sibirica , Rickettsia spp. Ixodes rugicollis no data Ixodes caledonicus no data transmission: tick-borne encephalitis virus, Chiz virus, Bahig virus, Ixodes frontalis è [19,26,30] Kemerovo virus, Coxiella burnetii Ixodes simplex no data Ixodes vespertilionis no data transmission: Omsk hemorrhagic fever virus, Rickettsia sibirica , Coxiella Ixodes apronophorus [1,26] burnetii, Francisella tularensis transmission : spring- summer tick-borne encephalitis virus , Powassan virus, Omsk hemorrhagic fever virus, West Nile virus , Langat virus , Uukuniemi virus , Kemerovo virus , Sichote-Alin virus, Borrelia burgdorferi , B. garinii, B. afzelii , B. valaisiana , B. miyamotoi, Rickettsia Ixodes persulcatus tarasevichiae , R. sibirica , R. helvetica, Anaplasma phagocytophilum, [10,19,31-40] A. marginale, A. centrale , Coxiella burnetii, Francisella tularensis, Erysipelothrix rhusiopathiae, Yersinia pseudotuberculosis, Salmonella sp ., Theileria sergenti, Babesia divergens, B. ovis , Babesia sp. , Bartonella henselae , Bartonella spp. Ticks of Poland 131

transmission : tick-borne encephalitis virus , Shetland encephalitis virus, Crimean- Congo haemorrhagic fever virus , Uukuniemi virus, Kemerovo virus (Koliba, Lipovnik, Tribec), Louping ill virus, Borrelia burgdorferi s.l ., B. garinii , B. afzelii , B. valaisiana, B. lusitaniae, B. bissettii, B. spielmani , Rickettsia slovaca , R. helvetica , R. monacensis , R. conorii, R. aeschilmannii, Anaplasma phagocytophilum, A. marginale, Ixodes ricinus A. centrale, Coxiella burnetii , Ehrlichia chaffeensis , Salmonella [10,19,31,41-59] enteritidis , Francisella tularensis, Listeria monocytogenes, Pasteurella, Erysipelothrix rhusiopathiae, Brucella melitensis, Theileria mutans, T. sergenti, Bartonella vinsonii, B. henselae , Babesia divergens, B. microti, B. caballi, B. bigemina, B. ovis, B. bovis, B. major, B. canis, B. capreoli, B. motasi, B. venatorum, Toxoplasma gondii ; can cause tick paralysis in the host transmission : tick-borne encephalitis virus (Western subtype), Crimean- Congo haemorrhagic fever virus, Bhanja virus, Tribec virus, Rickettsia Haemaphysalis sibirica , R. aeschlimannii , Coxiella burnetii , Anaplasma phagocytophilum, [1,19,60,61] punctata Francisella tularensis , Salmonella pullorum , S. enteritidis , Brucella sp., Theileria mutans , T. buffeli/orientalia, Babesia motasi , B. bovis , B. bigeminia , B. major ; it can cause tick paralysis in the host

transmission: tick-borne encephalitis virus (Western and Eastern Haemaphysalis subtypes), Borrelia burgdorferi s.l., Rickettsia hulinii, R. sibirica , Coxiella [1,19,62-64] concinna burnetii , Francisella tularensis , Salmonella pullorum , Brucella sp.

transmission: tick-borne encephalitis virus , Omsk hemorrhagic fever virus , Rickettsia conori , R. slovaca , R. sibirica, R. honei, R. raoulti, Rickettsia spp., Coxiella burnetii , Francisella tularensis , Salmonella sp ., Brucella Dermacentor abortus, B. melitensis , Erysipelothrix rhusiopathiae , Listeria [10,19,44,65-67] reticulatus monocytogenes , Theileria rossica, T.equi , Nicollia equi, N. ninense, Clostridium sp ., Brucella sp. , Babesia canis, B. microti, B. caballi, B. divergens, Hepatozoon canis occurrence is remote from the Polish territory have our country, but their transfer may cause increased been recorded. Geographical transference of ticks risk of tick-borne diseases. The general tendency of on migrating hosts, referred to as natural transfer, climate warming in Poland, well-conducted occurs in nature and is independent of breeding of terrarium animals, potential hosts for activity. Cases of unnatural tick transfer are ticks, and formation of new parasite-host systems, associated with deliberate or accidental human create greater opportunities for acclimatization of activity (Table 2). Each described case of ticks tick species brought from warmer areas of the Earth, transfer into new territory is valuable information and therefore open up new vectors of disease for faunists and epidemiologists, because expansion transmission. Reported cases of tick feeding on host of ticks is epizootiologically and epidemiologically indicate numerous direct consequences of important. parasitism. These are local, systemic changes Migratory birds are the most common group of causing disturbances in normal development of the hosts which can easily introduce alien species of host. ticks into the Polish fauna. Probably every year, In the course of studies conducted on reptiles during bird migrations to the southern part of [100], isolated cases of lizards and pythons infested Central Europe and further north, alien species of with exceptionally large number of ticks were found ticks are imported to Poland. During the study of (from 1 to 68 specimens of ticks on 1 host). birds in the Hel Peninsula (the Baltic coast in Apathetic and slow behaviour of the reptiles and Poland), four specimens of Ixodes eldaricus were observable weakened life activity showed the direct recorded for the first time in Poland [99]. consequences of high number of ticks parasitizing It is assumed that species brought for climatic them. It was noted that ticks parasitizing in clusters reasons cannot acclimatize in natural conditions of obstructed nasal and ear openings of Varanus 132 M. Nowak-Chmura, K. Siuda

Table 2. Registered cases of ticks transfer to Poland

Country from Cite of collection from host in which animals Species Host Poland were imported * refers to reptiles Amblyomma exornatum Świętochłowice Varanus exanthematicus Ghana (Koch, 1844) (Silesia province) Świętochłowice Iguana iguana El Salvador Amblyomma flavomaculatum (Silesia province ) (Lucas,1846) Świętochłowice Varanus exanthematicus Ghana (Silesia province ) Świętochłowice Varanus exanthematicus Ghana Amblyomma latum (Silesia province ) (Koch, 1844) Świętochłowice Python regius Ghana (Silesia province ) Amblyomma nuttalli Świętochłowice Varanus exanthematicus Ghana Dőnitz, 1909 (Silesia province) Amblyomma quadricavum Świętochłowice Iguana iguana El Salvador Schulze, 1941 (Silesia province) Amblyomma sphenodonti Sphenodon punctatus Cracow New Zealand Dumbleton, 1943 Amblyomma transversale Świętochłowice Python regius Ghana (Lucas, 1845) (Silesia province) Amblyomma varanensis Świętochłowice Varanus salvator Indonesia (Supino,1897) (Silesia province) Świętochłowice Varanus exanthematicus Ghana Amblyomma spp . (Silesia province ) Koch, 1844 Świętochłowice Python regius Ghana (Silesia province ) Dermacentor marginatus Sus scrofta The Kłodzko Valley (Sulzer, 1776) Testudo sp. Wieliczka, Chorzów Hyalomma aegyptium Testudo graeca Świętochłowice Greece (Linnaeus,1758) Testudo marginata (Silesia province ) Popielno Motacilla flava Hyalomma marginatum (Warmia-Masuria province ) Koch, 1844 Umianowice, Pińczów region, Acrocephalus schoenobaenus (Świętokrzyskie province) Ixodes eldaricus Prunella modularis, The Hel Peninsula Djaparidze, 1950 Erithacus rubecula Ixodes festai Turdus merula The Hel Peninsula Rondelli, 1926 Rhipicephalus rossicus Jakimov et Kohl-Jakimova, ? Machnów (Lublin province) 1911 Rhipicephalus sanguineus Canis familiaris Warsaw (Latreille, 1806) Ticks of Poland 133

Table 3. Tick-host specificity of Ixodida species recorded in Poland

Hosts Species Amphibia Reptilia Aves Mammalia Homo Argas reflexus + + + + + Argas polonicus + + + + + Argas vespertilionis + + + + + Ixodes trianguliceps + + + + + Ixodes arboricola + + + + Ixodes crenulatus + + + + + Ixodes hexagonus + + + + + Ixodes lividus + + + + Ixodes rugicollis + + + + Ixodes caledonicus + + + + Ixodes frontalis + + + + Ixodes simplex + + + + Ixodes vespertilionis + + + + Ixodes apronophorus + + + + Ixodes persulcatus NS NS NS NS NS Ixodes ricinus NS NS NS NS NS Haemaphysalis punctata + + + + + + Haemaphysalis concinna + + + + + + + + + + + +

Explanations: + + + + strictly specific host group + + + moderately specific host group + + relatively specific host group + accidental host group NS non-specific host group attacking all available hosts exanthematicus . In the eye and its close vicinity a Polish research on infection caused by few replete tick specimens restricted the field of pathogenic micro-organisms in humans and animals view. The overall prevalence of ticks infestation conducted on ticks imported on reptiles confirmed was 77.6%, 81.2% thereof for the host group of in two Amblyomma flavomaculatum specimens the snakes (pythons) and 78.7% for lizards (monitor presence of Anaplasma phagocytophilum , and lizards). Therefore, breeders of exotic animals are hence indicated a new epidemiological problem in warned to purchase animals from licensed brokers our country – the problem of transmissible diseases and not from casual sellers, and an animal examined pathogens in ticks brought on imported reptiles. The by a veterinarian and an experienced breeder findings also suggest that A. flavomaculatum ticks reduces the risk of introducing a host with parasites may participate in the natural circulation of A. into the terrarium. Moreover, ticks transfer into phagocytophilum in . No bacteria of home herpetoculture may detach unnoticed from the Rickettsia spp. causing spotted fevers were found in body of the host and move around the terrarium or the examined ticks [102]. the room in which they are held. In consequence, it might result in a tick transmission to an accidental Selected aspects of the biology of ticks host. Such an incident occurred in a breeding room, where the African tick Amblyomma flavomaculatum Host specificity. The relationship between a tick was collected from Iguana iguana imported from species and a vertebrate species – the host, which is Central America [101]. essential for the development and survival of 134 M. Nowak-Chmura, K. Siuda populations of a given species of ticks, is known as Argasidae sexual dimorphism is poorly marked, the host specificity. Out of approximately 900 species differences are visible in the construction of genital of ticks in the world only a few have very strict host aperture positioned at the rear edge of the coxae of specificity, feeding solely on one host species. In the the first pair of legs. Polish fauna it is I. lividus – the parasite of Sand In Ixodidae and Amblyommidae larva, nymph Martin ( R. riparia ). Ticks characterized by strict and female have a very similar structure. Their host specificity seek their hosts within a group of gnathosoma is mounted on the anterior edge of closely related species of vertebrates. For instance, idiosoma, dorsal scutum is adjacent to the base of in the Polish fauna these are such parasites of bats as the gnathosoma, in unfed specimens it covers the C. vespertilionis , I. vespertilionis , I. simplex , or anterior dorsal part of the idiosoma. Their idiosoma species ecologically associated with habitat, e.g. greatly increases their body size in the course of ticks dwelling and feeding in tree hollows of birds. feeding. Differentiating characteristics of these Moderate host specificity is exhibited mainly by developmental stages are as follows: larva has three ticks from ecological group of nidicolous species pairs of legs, there are no developed spiracular and that choose for hosts related host groups, but also genital orifices; nymph has four pairs of legs, feed on vertebrates which accidently occur at the spiracles and beginnings of future genital aperture; site and are not related, for example, representatives the female has four pairs of legs, spiracles, of the genus Argas , or subgenus Pholeoixodes . It developed genital aperture and on the dorsal surface has been shown that about 100 species of ticks of of the base of gnathosoma the so called porose the world fauna are host nonspecific. These are areas, i.e. two clusters of glands outlets. Sexual mainly exophilic species, such as in the Polish fauna dimorphism is evident. In males the entire dorsal I. ricinus which feeds on all terrestrial vertebrates. surface of idiosoma is covered with dorsal scutum. Until now no species of ticks (Ixodida) has been Besides, in males of the Ixodidae family practically recognized as specific for humans. Among the ticks the entire ventral surface of idiosoma is covered found in Poland we can distinguish several groups with abdominal scuta; in males of the as regards the types of host specificity or lack Amblyommidae they cover the rear of the ventral thereof (Table 3). Most of these species of ticks feed surface of idiosoma, or there are no abdominal scuta on atypical and accidental hosts, such as A. reflexus and then coxae of legs are more strongly developed. and A. polonicus regarded as specific parasites of Development cycles of ticks. Life cycle pigeons willing to attack distantly related humans. includes egg, larva, nymph and adult stage. A Feeding on species atypical for the parasite may in common feature of all development cycles of ticks host-specialized ticks cause disturbances in is that females of nearly all the species lay their eggs development or incomplete engorgement. In the outside the body of the host, on the ground, in the Polish fauna no ticks specific for amphibians litter, walls, cracks in buildings, etc., and the fact of (Amphibia) and reptiles (Reptilia) have been a single long-term, from a few to several days, recognized. larvae feeding. Notable exceptions are the larvae of Host specificity of ticks is in natural conditions Ornithodoros s.s (Argasidae) which transform into one of biological factors limiting the geographic stage I nymphs without feeding. distribution and population density of ticks. Modern Hosts of ticks may belong to the same or man-made changes in the environment, as well as different species of vertebrates. Active deve lop- transport of animals over longer distances, facilitate mental stages are present on the body of the host the spread of ticks to new areas and questing for usually only during feeding. Oviposition, new hosts. embryonic development and moulting of each life Morphological characteristics of active stages stage take place outside the body of the host. There of development of ticks. In the life cycle of ticks are four main types of development cycles of ticks there are three active developmental stages: larva, (multi-host, three-host, two-host, one-host), the nymph and adult (male or female). In the division of which is based on differences in the development of argasids (Argasina) there are two to relationships between developing ticks and the host. eight nymphal instars, their number may be Multi-host development cycle of Argasidae . different in individuals of the same species. In the Argasidae can attack practically all vertebrates development of ixodid ticks (Ixodina) there is only nesting or staying temporarily in their hideout. Life one nymphal instar. Ticks are dioecious, but in cycle: egg – larva – nymph (usually 2–4 stages, but Ticks of Poland 135 may be up to eight nymphal instars) – an adult form regards the habitat of host acquisition: (male or female). Larva after hatching from eggs Nests- and burrows-dwelling ticks . Natural and growing attaches to the first host and feeds from conditions of existence of Argasidae are burrows, a few to several days. Nymphs and adults feed for a pits, caves, bird nests, hollows, crevices in the rock short time, from several minutes to two hours. in warm and hot countries. In the biotopes altered by Adults can feed several times and after each feeding human activity, especially in the temperate climate, the females lay new batches of eggs. This is an Argasidae find their hiding places in synanthropic example of gonotrophic harmony, which is an environment. Some Ixodina have also specialized as expression of compatibility between the processes nidicolous parasites. In the Polish fauna, species of of digestion of food and the development of the the subgenus Pholeoixodes (Ixodidae) which, like ovaries – the adoption of one blood meal from the nidicolous Argasidae, spend their whole lives in host secures maturation of one portion of eggs in the burrows, caves, hollows and other hiding places female tick. After engorgement the nymphs and where they can feed on the host that lives there, adults detach from the host and hide in the host’s sleeps, reproduces and overwinters, or finds nest. temporary shelter. These tick species usually exhibit Development cycles of ticks from the families varying degrees of host specificity (e.g. Ixodidae and Amblyommidae. Life cycle: egg – monophagous I. lividus tick or oligophagous I. larva – nymph – adult (male or female). Each active arboricola tick parasitizing titmice). Additional stage of development feeds once from a few to factors favouring survival of ticks adapted to life in several days, and feeding time is usually longer in such hidden habitats are usually little fluctuations of each further life stage. In the development there is a climatic conditions such as temperature, humidity or close harmony between feeding and subsequent light. moulting in immature stages as well as between Out of nest dwelling ticks . Most ixodid ticks feeding, development and oviposition by females (Ixodidae and Amblyommidae) living today are out (gonotrophic cycle). Taking into account the of nest dwelling parasites that have adapted to living number of hosts, the following development cycles in exposed habitats and feeding on motile hosts that are distinguished in Ixodidae and Amblyommidae: migrate and are not strictly associated with definite Development cycle of three-host ticks. In this places of residence and reproduction. These ticks type of life cycle each growing tick has three hosts, are usually moderately host-specific or host- one for each active stage of development. Three- nonspecific (e.g. poliphagous I. ricinus in the Polish host development is the oldest and most common fauna). In this ecological group of ticks host form of the development of ixodid ticks, including acquisition is associated with high risk of failure to all the species of Ixodidae and Amblyom - get the host in time and, consequently, with death midae in the Polish fauna. from exhaustion after using energy reserves Development cycle of two-host ticks. Each tick accumulated in the previous stage of development, has two hosts in its development. Larvae and or on account of the occurrence of environmental nymphs feed on one host, and adults feed on conditions preventing the tick survival. Survival of another. An example of this type of development is a hungry tick is highly dependent, especially in such the life cycle of H. marginatum which is brought conditions, on its tolerance to temperature and light into Poland by migratory birds. changes, and relative humidity. In the case of open Life cycle of one-host ticks. The entire life cycle habitats many ticks die before they manage to find of the tick is associated with one individual their host and feed. Especially high mortality rate, vertebrate host. The subgenus Boophilus ticks of the depending on environmental conditions, occurs genus Rhipicephalus parasitizing large grass-eating among the larvae. Most species of nonnidicolous mammals in tropical countries reproduce in this ticks cling to plants passively waiting for a host. way. When ticks locate approaching host, they extend the Ecological groups of ticks acquiring hosts. first pair of legs with Haller’s sensory organ Ticks attack their hosts in conditions of natural positioned on feet and, if contact is made, catch the occurrence in a variety of habitats. These are often host with legs and pass on to his body. These ticks diversified environmental conditions, e.g. altered by have little mobility and do not move further than a human activity, or dictated by the current climate. few meters away. A chance to find a host is created There are several ecological groups of tick as by narrow forest tracks and paths that are often 136 M. Nowak-Chmura, K. Siuda movement trails of animals and humans. There is a summer and fall (autumn peak). During the spring group of species, e.g. of the genus Hyalomma , peak the abundance of hungry ticks is definitely the inhabiting steppe and desert environments that can highest, the autumn peak may occur in the years in actively seek their host. They are more mobile and which there are very hot and dry summer months. can move within several hundred meters. Very characteristic is the pattern of activity of Out of nest- and burrows-dwelling ticks. Adult hungry D. reticulatus ticks, adults have two clearly forms of certain species of ixodid ticks are exophilic separated periods of activity during the year. Spring parasites and immature forms adapted to nidicolous activity falls in the second half of March (in some parasitism. In such cases, only adult forms and years from February) to the first decade of June, larvae are exposed to severe climatic changes and with the peak of activity in the third decade of April. the difficulties associated with obtaining a suitable Autumn activity occurs from mid-August to mid- host. In the Polish fauna such species is D. November, with the peak of activity at the end of the reticulatus . first and second decade of October. In spring the Out of nest dwelling-stationary ticks. There are a number of active ticks is much greater. Immature small number of tick species which develop a close forms of D. reticulatus are active in the summer, and more durable relationship with the host. These from June to September. The daily rhythms of ticks tend to move from nonnidicolous type of hungry ticks’ activity in host acquisition are parasitism to a permanent existence on the body of associated with circadian rhythms of activity of the host. Larvae hatched on the ground after their hosts and microclimatic changes in the habitat obtaining host spend entire life cycle on it until at certain times of the day. engorged and fertilized females detach from the host Argasidae, nidicolous parasites of birds, are to lay eggs on the ground. In such form of usually characterized by strictly nocturnal pattern of parasitism only the hungry larva is exposed to locomotor activity, e.g. A. polonicus . However, dangers associated with finding a host. Ticks of this Argasidae, nidicolous parasites of mammals active type of parasitism are not found in the Polish fauna. at night, are generally parasites of diurnal locomotor A typical example is the species of subgenus activity of unfed specimens, e.g. C. vespertilionis . Boophilus of the genus Rhipicephalus . Their rhythm of activity is adapted to the circadian Seasonal and circadian rhythms of host rhythm of activities of their hosts. acquisition by hungry ticks. There are two groups In case of ixodid ticks (Ixodidae and of ecological rhythms of ticks: seasonal rhythms Amblyommidae) circadian rhythm of activity is related to annual changes in the external endogenously generated and the main exogenous environment and the circadian (daily) rhythms factors are diel microclimatic changes in the habitat associated with the rhythms of daily changes in the of ticks: the degree of solar radiation and lighting, external environment. humidity and temperature. An example is the In Ixodida seasonal rhythms are manifested by pattern of circadian activity of I. ricinus. They are interweaving of periods of active life: host active all day and night but are most active in the acquisition, feeding, growth, metamorphosis, morning (about 8–9) and at night (about 23–24). reproduction, with periods of „biological rest”: Increased tick activity is also observed in the diapause synchronized with specific seasons of the evening (about 18–19), especially during autumn annual climate rhythm of the external environment. activity of these parasites. The lowest activity of all The model of seasonal rhythms of life activity of developmental stages is recorded during midday ticks may be different depending on the hours [103]. geographical location of population within the range of a given species. Ticks attacking humans in Poland Argasidae found in Poland residing in synanthropic and semi-synanthropic habitats, It has not been found that any tick species medium wet or dry, about 50–70% of relative inhabiting the Polish and world fauna is a specific humidity, have the peak of activity in the middle of human parasite. On the Polish territory people can summer. be attacked by ticks of the family Argasidae: In Poland I. ricinus is active from early spring to A. reflexus and A. polonicus . From the family late autumn, but has two seasons of peak activity of Ixodidae, to which most ticks occurring in Poland hungry specimens – spring (spring peak) and in late belong, humans are mainly attacked by I. ricinus , a Ticks of Poland 137 non-host-specific species. Therefore, it is the most individuals, which is validated by studies carried out important tick in the epidemiology of transmissible in various research centres in Poland. Only some of diseases in our country (Table 1). In Poland there is them are presented below. a risk of attacking humans by a taiga tick The presence of antibodies against the antigens I. persulcatus which, like I. ricinus , is of utmost of Borrelia burgdorferi was detected in 23.8% of importance in the epidemiology of transmissible foresters from areas of the north-eastern Poland, in diseases (Table 1). The tick species with high 40.7% from the south-eastern Poland, in 66.67% of epidemiological significance which can also feed on the workers from forestry of Lower Silesia, in man in Poland is I. hexagonus (Table 1). It can 35–61.9% of foresters from the area of the West inhabit dog kennels and even human quarters where Pomerania province [104]. The forestry staff of there are permanent beddings for dogs and cats. Roztocze National Park in south-eastern Poland is Incidents of infesting people in Poland by D. reti cu- often exposed to attacks of I. ricinus infected with latus from the family Amblyommidae have also B. burgdorferi and A. phagocytophilum . In 40.7% of been recorded. forestry workers the presence of specific IgG and / Outside Polish borders isolated cases of people or IgM antibodies against B. burgdorferi s.1. was attacked by ticks C. vespertilionis , I. crenulatus , detected. The prevalence of IgG antibodies against H. con cinna and H. punctata have been reported. A. phagocytophilum was 17.7% [105]. In the woods near Bialystok the presence of Ticks as the cause of occupational disease A. phagocytophilum infections in I. ricinus ticks (14.5%) was found, and the prevalence of IgG While intruding into tick habitat, man can antibodies against A. phagocytophilum (3.9%) in the become an accidental host of any specimen, and forest guards from the same region was determined, hence a genuine risk of being infected with tick- as well as IgM anti- B. burgdorferi antibodies borne diseases. Particularly vulnerable are social (26.4%) and IgG (18.6%) [106]. groups whose work or interests require constant or The presence of antibodies against A. phago - seasonal stay outdoors. Foresters, farmers, cytophilum and B. burgdorferi was also tested gardeners, orchard men, enthusiasts of hunting, among forestry workers from the Lublin region hunters, border guards, seasonal collectors of forest [107]. fruits, tourists, naturalists, people resting in parks Detection and diagnostics of borreliosis is still and forests are particularly exposed to attacks by associated with interpretation difficulties frequently ticks, and noteworthy is the fact that in Poland there complicated by coinfections with other pathogens, are no safe areas in this respect. as well as high costs and longevity of treatment. According to the National Institute of Hygiene, Understanding the principles of personal protection tick-borne diseases in Poland constitute an against ticks is the cheapest and most certain way increasingly growing problem, and each year the recommended for all professional groups residing in incidence of infection in humans, especially with habitats and feeding grounds of ticks. borreliosis, is consistently high. For instance, 8 225 Rules of hygiene and safety at work should be persons contracted borreliosis in 2008, 10 333 applied especially in cases where the material with people in 2009, 9 011 persons in 2010 and 6 775 which people work is blood and tissues of animals – individuals in 2011 (until November 15th). 351 a potentially infectious material. This may be humans were infected with tick-borne encephalitis important for those involved in meat processing virus in 2009, 292 persons in 2010 and 172 people (hunters, butchers, game meat harvesters). in 2011 (up to November 15th). For some occupational groups (forestry, Risk of tick-borne diseases in recreational agriculture, hunting) borreliosis is regarded as a areas of large cities in Poland work-related disease, but the diagnosis is difficult owing to cumbersome procedures, lack of full The expansion of ticks into cities, especially documentation of the disease and relevant legal urban green areas, is considered to be a natural regulations. Forest workers need to be screened with phenomenon of the spread of parasites in search of serological tests, which are the only reliable method hosts. The presence of urban vacancies, illegal to detect infection, and the results from different waste dumps, small crops in home gardens and areas of Poland confirm high proportion of infected urban allotments leads to enhancement and 138 M. Nowak-Chmura, K. Siuda maintenance of the population of small rodents continents in the tropical and warm countries. In within the small and large cities. Small rodents, southern Europe there are 7 species [72,115]. large population of domestic animals and urban In the wild these ticks live in the burrows and birds are the intermediate hosts of ticks and natural nests of mammals, birds and reptiles, in caves, nutritional base for these parasites in each city. crevices and cavities in rocks, in cracks in the soil, Noticeable is a close relationship between the in clusters of stones. Most of the species exist on the development of gardening, horticulture, agro steppes and semi-deserts, some live high in the tourism, urbanization and the occurrence of ticks. mountains (e.g. Ornithodoros tholozani (Laboul b èn e Studies carried out in the Polish urban areas have and Megnin, 1882) (syn. O. papillipes ) at an altitude shown that ticks are present in cities, and that they of 2000–2800 meters above the sea level [72]). In are infected with morbific pathogens [41,48,67,68, the areas exploited by humans Ornithodoros ticks 108–114]. use as habitat huts of the natives, especially the old It is necessary to pay special attention to clay ones, less often brick apartment buildings, in familiarize the urban population, especially children which they live in the crevices of walls, under floors and adolescents, with areas of occurrence of ticks and in the cracks of furniture, as well as in and the principles of individual protection against synanthropic burrows of rodents. They use similar their attacks. Notice-boards informing about the shelters in farm buildings and animal pens, ruins of presence of ticks in parks and city squares would be old buildings as well as cracks, crevices and holes in advisable. High-risk territories are places with tall clay and stone walls surrounding human domiciles grass and undergrowth (up to 120 cm in height), but [116,117]. also paths and lawns in parks. Private gardens O. tholozani is a reservoir and a vector of covered with autumn leaves and withered forest Borrelia sogdianum in the countries of western and litter also create habitat for I. ricinus . Urban green central Asia. It is a polyxenic parasite whose hosts zone and its permanent residents protect the are various species of mammals, birds and reptiles, population of ticks in cities from extinction. The and it often attacks people. It is widespread from risk is also in close contact of humans with pets, Kazakhstan, the Middle East, through the central which may serve as periodical hosts of ticks and western Asian countries to Libya in the subsequently dropping off in the home environment. Mediterranean. This species causes outbreaks of Ticks can get to all parts of the body crawling on the tick-borne relapsing fever within human settlements skin under clothing, and the bite can occur [72]. anywhere. Most Ornithodoros are parasites of night activity in host acquisition, but they are classified as Examples of risks to human health caused anthropophilic species attacking people during by ticks outside Polish borders daytime in glowing sunlight. One such species is Ornithodoros asperus Warburton, 1918 (syn. Selected examples of ticks endangering people O. verru cosus ) occurring from Iraq via in different parts of the world have been presented. Transcaucasia, the Caucasus to the south of Most of the species live in warm and tropical and . A case has been described [72] of a countries, those that threaten human health are group, probably of tourists who during a very sunny represented on all continents. day sheltered from strong sunlight in the shadow of People travelling to work, especially where there the rocks where they were massively attacked by is contact with soil, e.g. working in quarries or ticks transmitting Borrelia caucasica . mineshafts, digging canals or ditches, building The countries of the western Mediterranean mounds of earth or stone, performing agricultural region are inhabited by Ornithodoros erraticus and archaeological jobs, etc., as well as tourists and (Lucas, 1849), a tick attacking mainly small rodents holidaymakers in hot and warm areas, are exposed and carrying Borrelia hispanica, the pathogen of to attack by ticks of the genus Ornithodoros Koch, Hispano-African relapsing fever in , Portugal, 1844 from family Argasidae, which are reservoirs Morocco, Algeria, Tunisia [118]. and vectors of spirochetes of different species of the In the south of the Sahara in Africa there exists a genus Borrelia – pathogens of tick-borne relapsing dangerous species Ornithodoros moubata (Murray, fever. Ticks of the genus Ornithodoros exist on all 1877). It frequently inhabits homes of the natives Ticks of Poland 139 and is a reservoir and a vector of Borrelia duttoni . the first signs of tick paralysis usually occur five People can be exposed to these ticks during safari days after tick invasion, increase the likelihood of trips to Africa. the disease in localities where nobody expects it. From the Ornithodoros species inhabiting North Incubation period of tick paralysis usually lasts America, most of the concerns raise in humans the 5–7 days. The paralysis symptoms begin in the attacks of Ornithodoros coriaceus Koch, 1844 lower limbs, initially slight to increasing problems occurring frequently in the mountainous coastal with coordination, ataxia, and muscle weakness. area of California (USA) and Mexico. [119] In Within hours the symptoms of paralysis become California it is known as „Pajaroello”, and the tick’s more severe and gradually affect the trunk, upper attack is believed to be more dangerous than a limbs, neck, throat and face. The attacked person rattlesnake bite. cannot move arms, legs, stand upright or sit. In Eastern Europe and Asia (Russia, Mongolia, Descending, symmetrical, flaccid paralysis of the China, Japan) there is I. persulcatus [120]. Outside limbs follows with the weakening of tendon its compact range of distribution, its presence has reflexes, and Romberg sign. There is also been found in the Bialowieża Primeval Forest in nystagmus, difficulty in speaking, breathing, Poland [85]. It exists in a variety of woods along the chewing and swallowing, and reduced sensitivity. middle and southern taiga, and in forest steppes. It is The body temperature is normal and the blood very aggressive, more frequently than any other picture does not deviate from the norm. In the final Ixodidae attacks man. In sparsely populated taiga I. phase of the disease (usually the second, third day) persulcatus is most numerous in clearings, forest coma and death follow. The most vulnerable to the edges, on the outskirts of animal trails, resting and disease are young children (up to 2 years). The grazing areas of animals, and watering places of primary therapeutic procedure is to remove the tick large mammals. It is one of the species of the genus in time prior to the patient’s critical condition. The Ixodes of major importance in the epidemiology of venom causing paralysis is likely to be quickly transmissible diseases (Table 1). Amongst its eliminated or metabolized in a short time and then victims were probably exiles working in the taiga in the patient recovers quickly. the nineteenth and twentieth centuries. In the world fauna the most important role in Travelling to North America humans can come causing tick paralysis in humans is played in North in contact with two species of ticks from the group America by Dermacentor andersoni Stiles, 1908 of I. ricinus , i.e. Ixodes scapularis Say, 1821 and and Dermacentor variabilis (Say, 1812), in Ixodes pacyficus Cooley et Kohls, 1943, considered Australia by Ixodes holocyclus Neumann, 1899 as some of the most important vectors of tick-borne [118]. There is a known case of a group of Polish diseases in North America. mountaineers from Cracow, who in Banff (Canada) Ticks can endanger people not only in the Rocky Mountains collected D. andersoni epidemiologically. The consequence of infestation from the clothing of one of the members of the with certain ticks can be poisoning of the host expedition. It is known that just one feeding D. organism and generalized allergic and stress andersoni female may induce full paralysis and reactions, but the most dangerous direct cause human death. consequence of tick parasitism to humans is the disease defined as tick paralysis. Approximately 43 An overview of the latest Polish research on species of ticks of the world fauna have been ticks considered capable of inducing tick-borne paralysis with toxins contained in the saliva of ticks. Six of In the latest Polish literature on tick issues much those tick species exist or are transferred into the space is devoted to research into the epidemiology Polish territory (Table 1), but in Poland there have and significance of ticks in the transmission of tick- not been officially recorded cases of tick paralysis. borne diseases. Publications referring to the classic However, its incidence cannot be ruled out in people faunistics are relatively few, most of them contain returning from areas of natural occurrence of the information about I. ricinus – commonly occurring most important species of ticks in this respect. The tick species in Poland. The research base on the ease and speed with which people move around the biology and ecology of ticks is also increasing. The world, the fact that an attached tick cannot be seen first report on Polish ticks data was presented by (especially the American Dermacentor) , and that Lachmajer [85], an update and complete 140 M. Nowak-Chmura, K. Siuda descriptions were made by Siuda [1]. Research Studies on the morphology and biology of pursued in this field by the national centres at the ticks turn of the century is presented in this study (Table 4). The database of world literature in the field of biology is enriched by the Polish insightful research on the anatomy and morphology of ticks [187,188], Epidemiological research with particular emphasis on sense organs, Studies on the role of ticks in the epidemiology pheromones and teratological changes [189–192], of transmissible diseases are broadly represented by as well as research on the development of ticks the Polish researchers [56,121–132], and the [193,194], tick behaviour in natural and laboratory published works are often pioneering not only in conditions associated with host acquisition and Poland, but also in Europe and in the world feeding [195]. [49,51,65,102,133–135]. Circadian and seasonal activity of Polish ticks is Because the most important role in the biology still not sufficiently understood. Many species are and epidemiology of developing infectious and difficult to observe in the wild. Consequently, most invasive diseases in Poland is played by I. ricinus , researchers examine tick life cycles for the species its role in epidemiology is most frequently studied easiest to obtain for study: I. ricinus , D. reticulatus and the prevalence of pathogens in the system [44,103]. vector–zoonotic reservoir is determined. The second Research on the relationship between parasite most frequently studied epidemiologically tick is D. species and vertebrate host species, a necessary reticulatus [42–45,48,52,58,67,127, 136– 145], and relationship for the development and survival of the on this occasion its foci are being discovered parasite population, is a common topic of studies of throughout Poland. Polish parasitologists. It is also reflected in the study Monitoring public health risk of tick-borne of tick-host specificity [44,100,196–198]. diseases and recording the frequency of occurrence of tick attacks, especially on humans occupationally Faunistic studies exposed to ticks, as well as determination of endemic sites are becoming increasingly important Faunistic studies are conducted only by a few owing to high incidence rate and diagnostic research centres and are focused on the occurrence, difficulties [11,105,107,146–160]. distribution and abundance of ticks in habitats in Essential research trends in the twenty-first various Polish regions, both in urban areas and in century parasitology are studies using methods of natural biotopes [4,97,110,113,114,199– 204]. molecular genetics, whose aim is application of Studies on biodiversity of ticks feeding on hosts, molecular methods for the detection of DNA of large and small vertebrates, have their long tradition pathogens transmitted to humans by ticks dating back to the early twentieth century [47,50,121,161–163]. [89,205,206]. They are successful insofar as they in An important issue in research is co-occurrence progress and bring a lot of new findings on, among of micro-organisms not only within the populations others, infestation of different hosts by ticks, of ticks from various regions in Poland, but mainly location of ticks on the body of the host and within the body of a single tick [59,164–167], and in consequences of their feeding [73,76,84,196,207– patients bitten by ticks treated for meningitis [168] 216]. and with a diagnosis of borreliosis [169]. There are research centres regularly monitoring Several centres in Poland conduct research on distribution of ticks in Poland, expansion of their the role of vertebrates as a reservoir of tick-borne ranges and discovery of new localities of species. pathogens: game [170–173] bison [174], dogs The following areas in Poland are best known in [175,176], rodents [126,177,178], birds [179], and terms of the presence of ticks: West-Pomeranian testing animal products such as milk for the and Pomeranian provinces [68,76,97, 217], north- presence of tick-borne pathogens [151]. eastern Poland and Masovia [3,88,111,218–221], Extremely important studies are performed on Lower Silesia province [222,223], areas of the epidemiological, clinical and molecular aspects of south-eastern Poland, especially the Lublin region tick-borne diseases in humans [180–186]. [224–226], and the provinces of southern Poland: Silesia, Świętokrzyskie, Lesser Poland, Sub car- Ticks of Poland 141

Table 4. List of scientific centres in Poland conducting research on ticks and their medical significance

Research centre in Poland* Current research interests

- studies on haematophagous arthropods and their role in the transmission of zoonoses in Poland, - research on the role of Ixodidae in the epidemiology of transmissible diseases: tularemia, tick-borne encephalitis, and since the 90s of the last century, mainly the so-called „emerging infectious diseases” - newly diagnosed infectious and invasive zoonoses in the world: Lyme disease, human Department of Tropical granulocyte anaplasmosis, spotted fever group (SFG) rickettsiosis, babesiosis Parasitology, Chair of Tropical and their natural foci, Medicine and Parasitology, - research on prevalence of infections in ticks with pathogens and their spread National Centre of Tropical in the areas under study, Medicine, - research on co-infections with several tick-borne pathogens, Medical University of Gdańsk - studies on prevalence level of pathogens in tick populations and host density of these parasites, - molecular detection and genotyping of pathogens in ticks and their natural hosts, - identifying areas of occurrence of natural tick-borne disease foci in Poland with special reference to northern and north-eastern part of the country, - research on the prevalence of infection in people exposed to tick attacks - study of ticks feeding on deer and bison, analysis of causes of location on the host body, - analysis of feeding traces and histopathological changes caused by ticks in bison, Department of Invertebrate - research on variability of Ixodes ricinus in ungulates, Zoology, University of Gdańsk - studies of ticks feeding on wild boar, determination of dynamics and seasonal occurrence, parameters of infection and location, - study of ticks feeding on small mammals, - research on the occurrence of ticks in Poland, especially in the northern part of the country - research on morphology of ticks with a special focus on sense organs and teratological changes, - study on the development of embryonic and extra-embryonic stages, and factors affecting the development of ticks Argas reflexus, Ixodes ricinus, Dermacentor reticulatus, Dermacentor marginatus, - research on tick-host system, Chair and Department of Biology - study on the behaviour of ticks associated with the search for the host and and Parasitology, feeding in natural and laboratory conditions, Medical University of Lublin - research on tick distribution and ecology, especially in the south-eastern part of the country, - studies on the role of ticks in epidemiology of transmissible diseases, transfer of tick-borne pathogens in south-eastern Poland, - monitoring public health risks of tick-borne diseases through serological testing and recording the frequency of tick attacks, - study of chemical and biological surveillance of tick abundance

- research towards identifying the prevalence of pathogens ( Borrelia burgdorferi s.l., Anaplasma phagocytophilum , Bartonella sp., Babesia sp.) in the vector - zoonotic reservoir system taking into account variability amongst Department of Parasitology, and within species of pathogens and their phylogenetics, Faculty of Biology, - studies on the effects of various environmental factors on the prevalence of University of Warsaw, Warsaw pathogens in Ixodes ricinus tick populations in different biotopes (urban biotopes with strong anthropopression and natural biotopes of mixed forests with little anthropopression) 142 M. Nowak-Chmura, K. Siuda

Research centre in Poland* Current research interests

- monitoring the occurrence of ticks in selected districts of Lower Silesia in forest Department of Microbial and urban areas Wrocław, Ecology and Environmental - structures of tick populations, seasonal activity, ecological relationships of tick Protection, activity, Institute of Genetics and - mapping the results of environmental and laboratory studies using geographic Microbiology, information systems (Arc View), University of Wrocław - determination of the degree of tick infection with Borrelia burgdorferi s.l. (DFM method and nested PCR) - research on fauna and taxonomy of ticks (Ixodida) in Poland and Central Europe, - studies on the occurrence, distribution and abundance of ticks in urban Department of Invertebrate recreational areas and natural biotopes (landscape and national parks), especially Zoology and Parasitology, in the southern Poland, Institute of Biology, - research on daily and annual cycles of ticks, Pedagogical University of - studies on ecology, host specificity and epidemiological significance of ticks, Cracow - research on migration of alien species of ticks ( Ixodes , Amblyomma , Hyalomma ) to Poland on different hosts and spread of ticks beyond their natural ranges of occurrence - studies on the occurrence of ticks, especially in the Silesia province, Department of Parasitology, - epidemiological studies on human and animal exposure to tick-borne pathogens Medical University of Silesia such as, among others, spirochetes of Borrelia burgdorferi s. l., Anaplasma in Katowice, Sosnowiec phagocytophilum , Babesia sp., tick-borne encephalitis virus, Toxoplasma gondii , rickettsiae - studies using molecular genetics methods, the aim of which is application of molecular methods for the detection of DNA of human disease pathogens transmitted by ticks ( Borrelia , Babesia , Ehrlichia /Anaplasma, Rickettsia , Bartonella ), - research on delimitation of areas endemic for Ixodes ricinus and borreliosis, babesiosis, anaplasmosis in forested areas of Szczecin and West Pomeranian Department of Genetics, province, Faculty of Biology, - research on coexistence of DNA of various pathogens in Ixodes ricinus , University of Szczecin, - study on participation of forest birds and rodents in Greater Poland in the spread Szczecin of borreliosis, babesiosis, anaplasmosis, ehrlichiosis, Bartonella genus, - studies on the role of wild game and forest vertebrates as reservoir of tick-borne pathogens, - study of bacteria of the genus Bartonella in the tissues of game animals (roe deer, red deer) and Ixodes ricinus infesting these animals in areas of West Pomeranian province Division of Parasitology and - epidemiology of canine diseases transmitted by ticks, especially babesiosis in Parasitic Diseases, Department of dogs Preclinical Sciences, Faculty of Veterinary Medicine, Warsaw University of Life Sciences – SGGW, Warsaw Department of Applied - research on anatomy and role of Ixodes scapularis synganglion, Entomology, Faculty of - popularization of knowledge about ticks, methods of protection against ticks Horticulture and Landscape Architecture, Warsaw University of Life Sciences - SGGW, Warsaw Department of Biology and - the role of Ixodes ricinus in the epidemiology of transmissible diseases, Medical Parasitology, including Lyme disease and piroplasmosis in the areas of north-western Poland, Pomeranian Medical University, especially Szczecin and vicinity Szczecin Ticks of Poland 143

Research centre in Poland* Current research interests

- studies on the occurrence, distribution, activity, annual cycle and range of tick hosts in Poland and their role as a reservoir and vector of tick-borne diseases, - research on the role of ticks and mammals in the spread of micro-organisms (Borrelia burgdorferi s.l., Babesia microti , Babesia canis , Babesia divergens, W. Stefański Institute of Bartonella sp., Rickettsia sp., Hepatozoon canis, Anaplasma phagocytophilum ) in Parasitology of Polish Academy selected Polish regions, of Sciences, Warsaw - research on prevalence of tick-borne infection of small mammals in Poland, - studies on the occurrence and distribution of ticks in urban recreational areas and natural biotopes, - occurrence, biology and epidemiological significance of Dermacentor reticulatus in Poland

- the role of ticks in the epidemiology of disease transmission (Lyme disease, anaplasmosis, babesiosis, bartonellosis, tick-borne encephalitis), - frequency of occurrence of specific pathogens in ticks Ixodes ricinus and Dermacentor reticulatus , Unit of Zoonoses, - tick activity in the foci of specific tick-borne diseases, Institute of Rural Health, Lublin - occurrence of tick-borne encephalitis virus in milk, - prevalence of antibodies against specific pathogens in occupationally exposed populations, foresters and farmers, - tick-borne disease prevention

Laboratory of Rickettsiae, - research on microorganisms that are etiological agents of zoonoses transmitted by Chlamydiae and Enzootic ticks, Spirochetes National Institute of -performance of full range of diagnostic testing (in humans, animal reservoirs, Public Health, vectors) allowing detection of infections with bacteria Borrelia burgdorferi s.l., National Institute of Hygiene, Coxiella burnetii , and the genera of Rickettsia , Bartonella , Anaplasma (serological, Warsaw molecular, bacteriological testing, culture of etiological agent) - expansion of Dermacentor reticulatus and Ixodes ricinus in urban environments High School of Civil Sciences, of southeastern Poland, especially the Lublin region, Lublin - assessment of the risks of tick attacks in environments with varying degrees of anthropopression - the study of ticks as vectors of human and animal diseases (bison, northern vole), - selected epidemiological, clinical and molecular aspects of Anaplasma Department of Infectious phagocytophilum Diseases and Hepatology, - the agent of human granulocyte anaplasmosis, Medical University of Białystok - diagnostic and therapeutic testing of tick-borne diseases: tick-borne encephalitis and Lyme disease, - vaccination against tick-borne encephalitis

Department of Infectious - diagnosis, epidemiology and treatment of tick-borne diseases Diseases and Neuroinfections, Medical University of Bialystok

Department of Biochemistry - molecular testing for the role of Ixodes ricinus in the transmission of human and and Molecular Biology, animal pathogens ( Babesia sp., Anaplasma phagocytophilum , Borrelia burgdorferi University of Natural Sciences s.l.) in the area of central and eastern Poland and Humanities in Siedlce * The review presents achievements of research institutions from which full information about their studies has been obtained pathia [81,92,227–229]. to Poland on different hosts and aspects of Research is also in progress on migration of alien expansion of ticks outside their natural ranges of species of ticks (Ixodes, Amblyomma, Hyalomma) occurrence, hence the knowledge of importing alien 144 M. Nowak-Chmura, K. Siuda tick species to the territory of Poland is motion using fine tweezers, or with a tissue or systematically increasing [99–101,230,231]. instruments available in pharmacies to remove ticks. Extremely important are comprehensive Strict hygiene measures should be observed while publications popularizing knowledge of ticks and pulling a tick. Ticks must not be removed with bare tick-borne diseases which should be available fingers, nor should any grease or lubricant fluid be primarily for family doctors, naturalists, forests and applied. After removal of the parasite the site should national parks employees, teachers, tourists, be disinfected. The removed tick may be sent for schoolchildren and students. Especially in the examination to an appropriate laboratory. In case of spring, when ticks activity in host acquisition is less accessible places assistance in removing the increasing, there is a need for publications on tick should be sought from an experienced nurse or methods of protection against ticks and widely a doctor at the health clinic. The place after tick understood prophylaxis [185,232–239]. removal should be monitored and, if feeling unwell in the next few weeks, going to a doctor and Prevention of tick attacks in Poland informing him about tick infestation is recommended. People residing in forests or for Ixodid ticks from families: Ixodidae: other reasons staying in the areas of constant I. ricinus , Amblyommidae: D. reticulatus. exposure to ticks may, after consulting a doctor, Broadly defined recreational places in Poland are undergo vaccination against viral encephalitis areas of high risk of exposure to ticks and tick-borne transmitted by ticks. One possibility of infection diseases. There are no safe places in Poland in this with tick-borne encephalitis virus is also eating raw respect. People spending their free time in the city in goat’s milk and dairy products from goats infected recreational settings (private gardens, allotments, with the virus by parasitizing ticks. parks, walking paths for animals), and outside the The simplest procedures performed in the city (places of summer recreation for children and immediate environment of humans aiming at adults, forest and parts of the forest immediately reduction of tick population are removing shrubby adjacent to areas inhabited by humans, pastures, thickets, regular mowing, restricting access of small meadows, hiking trails, river banks and others) rodents and other wild animals to human buildings, should be aware of prophylaxis against tick attacks. and inspection of the skin and fur of farm animals. The easiest protection is appropriate clothing, preferably in bright colours, preventing parasites Argasids of genus Argas (Argasidae) in from moving to bare skin, e.g. long pants tucked Poland and Europe into socks, boots, a long-sleeved sweatshirt tightly inserted into trousers, a hat or cap on the head, neck Effective protection against argasids is getting protected with a scarf. Additional and recommended rid of pigeons, hosts of these ticks, which nest near protective measures are repellents which should be human dwellings and windows in attics, lofts, in sprayed on the skin and clothing. The aim is to wild nests built on balconies and other prevent tick transfer to bare skin, but effectiveness constructions, in order to prevent ticks from of such measures is limited to a few hours, therefore entering the human living quarters. Argasids of the it is recommended to repeat repellent application subgenus Argas spend the day hidden in the frames several times a day. In order to limit contact with of window cracks, crevices and fissures in walls, ticks, walking trails overgrown with tall grass, behind paintings, folds of curtains, and during the shrubs and wildlife trails should be avoided as well night they quest for host, who can often be as lying down on the grass without spreading a accidental sleeping man. Therefore, the blanket. After spending time outdoors, especially neighbourhood of pigeon lofts with resting place for during the spring and autumn periods of ticks the night should be avoided. Flats once converted activity, the entire body, hair and clothes should be from lofts or attics where pigeons had lived, or flats searched for ticks; light coloured clothing will help on the top floors bordering bird nests should detect moving parasites. The smallest undergo disinfection with specialist chemicals to developmental forms of ticks (larvae and nymphs), eradicate ticks. Incompetently chosen methods to owing to very small size (about 1–2 mm), may be control the ticks, or unprofessionally secured cracks difficult to notice. Each tick embedded in the skin in the walls and adjacent windows can allow ticks to must be removed immediately with a firm, fast survive even a few years without access to the host. Ticks of Poland 145

One way to detect the presence of ticks in the room fungi, viruses, bacteria), which have also been used is observation of walls and cracks in walls where in fight against ticks. Combating ticks by chemical ticks can leave their droppings in the form of off- means is prohibited in order to protect the whitish lumps, or sticking double-sided adhesive environment, and the European Union restricts the tape in places adjacent to openings, on the use of pesticides that were once exploited to fight windowsills, and wherever their movement is ticks [240]. There are several techniques to control expected. While attempting to move, ticks will stick ticks in their natural environment, i.e. influencing to the tape. [11] In the absence of possibility of changes in microclimatic habitat conditions which isolating lofts from human domiciles, walls should impede their development cycle, land drainage, to be adequately protected in order to eliminate melioration, removal of shrubs and grasses from cracks, holes and hideouts, which will prevent tick habitats, chemical and biological procedures [71]. migration between two adjacent compartments. In Poland no techniques to combat ticks in their Parasitizing ticks can cause serious human health natural environment are used. problems [11], therefore noticing on the human Polish scientists conducting research on ticks body blisters, itching and rashes and recurrent greatly contribute to ever-increasing recognition of dyspnoea should be consulted with a physician. parasitism of this group, identification of species, Bat argasids C. vespertilionis are active during diagnosis and treatment of diseases, i.e. utilizing all the day, therefore people intruding into hiding possible means offered by the twenty-first century places of bats, such as caves, must be protected from to save human health and life. argasids attacks with suitable tight clothing. Appropriate repellents can be applied, which should References be sprayed on the skin and clothes. [1] Siu da K. 1993. Klesz cze (Aca ri: Ixo di da) Pol ski. II. Argasidae (Ornitodorinae): a possibility of Sys te ma ty ka i roz miesz cze nie. Mo no gra fie Pa ra zy to- lo gicz ne vol. 12. Po lish Pa ra si to lo gi cal So cie ty, contact during trips to warm and tropical Warsaw. countries [2] Gu gliel mo ne A.A., Rob bins R.G., Apa na ske vich D.A., Pet ney T.N., Es tra da -Pe ńa A., Ho rak I.G., Shao Tourists travelling to warm and tropical R., Bar ker S.C. 2010. The Ar ga si dae, Ixo di dae and countries may be attacked by ticks of the subfamily Nut tal liel li dae (Aca ri: Ixo di da) of the world: a list of Ornithodorinae. It is difficult to determine the va lid spe cies na mes. Zo ota xa 2528: 1-28. presence of ticks in the room. The easiest way is to [3] Kar bo wiak G., Kiew ra D. 2010. New lo ca tions of collect the dry content from cracks, or the ground Der ma cen tor re ti cu la tus ticks in We stern Po land: the level parts of walls and floors, and leave in the sun. first evi den ce of the mer ge in D. re ti cu la tus oc cur ren - Under the influence of heat, ticks will demonstrate ce are as? Wia do mo ści Pa ra zy to lo gicz ne 56: 333-340. activity and will be easier to observe. Staying [4] No wak M. 2011. Di sco ve ry of Der ma cen tor re ti cu la- tus (Fa bri cius, 1794) (Aca ri: Am blyom mi dae) stan- overnight or hiding from the sun in mud huts, ruins dings in the Lu bu skie Pro vin ce (We stern Po land). of buildings, caves, rocks, etc. should be avoided, as Expe ri men tal and Ap plied Aca ro lo gy 54: 191-197. well as setting up tents or sleeping outdoors in a [5] Siu da K., Ho og stra al H., Clif ford C.M., Was sef H.Y. place where there are many rodent burrows. In cases 1979. Ob se rva tions on the sub ge nus Ar gas (Ixo do- when the aforementioned places cannot be avoided, idea: Ar ga si dae: Ar gas ). 17. Ar gas (A. ) po lo ni cus sp. protective insect repellents should be sprayed on the n. pa ra si ti zing do me stic pi ge ons in Kra ków, Po land. skin, clothes and a sleeping bag. Impenetrable Jo ur nal of Pa ra si to lo gy 65: 170-181. mosquito nets, sleeping bags and clothing are [6] Dusbábek F. 1985. Iden ti fy of Ar gas (Agras ) po lo ni- recommended. While staying overnight in such cus po pu la tions in Cze cho slo va kia and Po land. Fo lia room the bed should be moved away from walls. Pa ra si to lo gi ca 32: 163-171. [7] Bie le nin I. 1980. Dal sze przy pad ki za ata ko wa nia lu- Inserting bed legs in water and paraffin oil can also dzi przez Ar gas po lo ni cus Siu da, Ho og stra al, Clif ford act as a deterrent. et Was sef, 1979, po za lo cus ty pi cus . In: Ma te ria ły IV From the twenties of the 20th century attempts Sym po zjum Aka ro en to mo lo gii Me dycz nej i We te ry- have been made at biological control of ticks, but na ryj nej, 4-6 IX 1980 Gdańsk: 2. without much success. Ticks have many natural [8] Siu da K., Ja rosz Z., No rek L. 1982. Przy pa dek za ata- enemies (such as arthropods, amphibians, birds, ko wa nia stra ża ków- hej na li stów Ko ścio ła Ma riac kie- mammals, nematodes, protozoa, entomopathogenic go w Kra ko wie przez obrze żki pol skie Ar gas (Ar gas ) 146 M. Nowak-Chmura, K. Siuda

po lo ni cus Siu da, Ho og stra al, Clif ford et Was sef, gu li ceps as vec tors for Ana pla sma pha go cy to phi lum 1979 (Aca ri na, Ixo di des, Ar ga si dae). Wia do mo ści and Ba be sia mi cro ti in field vo le ( Mi cro tus agre stis ) Pa ra zy to lo gicz ne 27: 57-62. po pu la tions. Ap plied and Envi ron men tal Mi cro bio lo- [9] Bar to sik K. 2011. Bio lo gi cal cha rac te ri stics and me- gy 74: 7118-7125. di cal im por tan ce of ticks from the fa mi ly Ar ga si dae [21] Gri gor’eva L.A., Tret’kia kov K.A. 1998. Fe atu res of pa ra si ti zing hu mans. In: Sta wo no gi. Pa so ży ty czło- the pa ra si tic sys tem of ixo did ticks – Bor re lia in wie ka i zwie rząt . (Eds. A. Bu czek, C. Bła szak). Aka- small mam mals in the Rus sian Nor th west. Pa ra zi to- pit, Lu blin: 53-62. lo giia 32: 422-430. [10] Siu da K. 2006. Cha rak te ry sty ka klesz czy (Ixo di da) [22] Kar bo wiak G. 2004. Zo ono tic re se rvo ir of Ba be sia o zna cze niu me dycz nym w Pol sce. In: Bio lo gia mo le- mi cro ti in Po land. Po lish Jo ur nal of Mi cro bio lo gy 53: ku lar na pa to ge nów prze no szo nych przez klesz cze . 61-65. (Ed. B. Sko tar czak). Wy daw nic two Le kar skie PZWL, [23] Ne fe do va V.V., Ko ren berg E.I., Fa de eva I.A., Go re - War sza wa: 33-41. lo va N.B. 2005. Ge ne tic cha rac te ri stics of hu man pa- [11] Śpie wak R., Lund berg M., Gun na ro S., Jo hans son tho ge nic Bor re lia iso la ted from Ixo des trian gu li - S.G.O., Bu czek A. 2006. Al ler gy to pi ge on tick ( Ar- ceps Bir. and Ixo des pa vlo vskyi Pom. Me dit sin ska ia gas re fle xus ) in Up per Si le sia, Po land. An nals of Pa ra zi to lo giia 2: 9-12. Agri cul tu ral and Envi ron men tal Me di ci ne 13: 107- [24] Lach ma jer J. 1965. Po ten cjal na szko dli wość klesz- 112. czy nad ro dzi ny Ixo do idea na te re nie Pol ski. Wia do- [12] Tah ma se bi F., Ghia si S.M., Mo sta fa vi E., Mo ra di mo ści Pa ra zy to lo gicz ne 1-2: 171-177. M., Pia zak N., Mo za fa ri A., Ha eri A., Fo oks [25] Spi talská E., Li ter ák I., Ko cia nová E., Ta ra gel’ová A.R., Chi ni kar S. 2010. Mo le cu lar epi de mio lo gy of V. 2011. The im por tan ce of Ixo des ar bo ri co la in Cri me an- Con go he mor r ha gic fe ver vi rus ge no me iso- trans mis sion of Ric ket t sia spp., Ana pla sma pha go cy- la ted from ticks of Ha ma dan pro vin ce of Iran. Jo ur - to phi lum , and Bor re lia burg dor fe ri sen su la to in the nal of Vec tor Bor ne Di se ases 47: 211-216. Czech Re pu blic, Cen tral Eu ro pe. Vec tor Bor ne [13] Bie la sho va V.S. 1966. Ar gas ve sper ti lio nis ticks in and Zo ono tic Di se ases 11: 1235-1241. Ka za kh stan. In: Per voe Aka ro lo gi che skoe So ve sh cha- [26] Fi lip po va N.A. 1977. Ik so do wy je kle shch pod siem. nie (Ed. B.E. By chow skij). Te zi sy Do kla dov, Iz da- Ixo di nae. Fau na SSSR. Pau ko obra znye. Vol. 4. Iz da - tel’stvo Na uka, Mo skov- Le nin grad: 25-26. tel stvo Na uka, Le nin grad. [14] Dusbábek F., Ro sický B. 1976. Ar ga sid ticks (Ar ga- [27] Nij hof A.M., Bo da an C., Post igo M., Nie uwen hu ijs si dae: Ixo do idea) of Cze cho slo va kia. Ac ta Scien tia- H., Opste egh M., Frans sen L., Jeb bink F., Jon ge jan F. rum Na tu ra lium 10: 1-43. 2007. Ticks and as so cia ted pa tho gens col lec ted from [15] Ga vri lo vskaya I.N. 2001. Is syk- Kul vi rus di se ase. do me stic ani mals in the Ne ther lands. Vec tor Bor- In: The En cyc lo pe dia of Ar th ro pod- trans mit ted In fec- ne and Zo ono tic Di se ases 7: 585-595. tions. (Ed. M.W. Se rvi ce), CA BI Pu bli shing, UK [28] Gra ham R.I., Ma in wa ring M.C., Du Feu R. 2010. Lon don: 321-234. De tec tion of spot ted fe ver gro up Ric ket t sia spp. from [16] Ho og stra al H. 1956. Afri can Ixo do idea. I. Ticks of bird ticks in the U.K. Me di cal and Ve te ri na ry En to- the Su dan (with spe cial re fe ren ce to Equ ato ria Pro- mo lo gy 24: 340-343. vin ce and with pre li mi na ry re views of the ge ne ra Bo - [29] L’vov D.K., Ari sto va V.A., Gro ma she vskii ophi lus , Mar ga ro pus and Hy alom ma ). Dep. Na vy, V.L., Skvort so va T.M., Bo iko V.A., Mel’ni ko va Bur. Med. Surg., Wa shing ton D.C. E.E., Gu sh chi na E.A., Ia ru lo va R.A., Mo ro zo va [17] Ho og stra al H. 1985. Ar ga sid and Nut tal liel lid ticks T.N., Pe tro va E.S. 1998. Ka ma, a new vi rus (Fla vi vi- as pa ra si tes and vec tors. Ad van ces in Pa ra si to lo gy 24: ri dae, Fla vi vi rus, Tiu le nii an ti ge nic gro up), iso la ted 135-238. from Ixo des li vi dus ticks. Vo pro sy Vi ru so lo gii 43: [18] Hub bard M.J., Ba ker A.S., Cann K.J. 1998. Di stri- 71-74. bu tion of Bor re lia burg dor fe ri s.l. spi ro cha ete DNA [30] Cha stel C., Chan dler L., Le Goff F., Cha stel in Bri tish ticks (Ar ga si dae and Ixo di dae) sin ce the O., Tesh R., Sho pe R. 1999. Chizé vi rus, a new phle - 19th cen tu ry, as ses sed by PCR. Me di cal and Ve te ri- bo vi rus iso la ted in Fran ce from Ixo des (Tri cho to ixo- na ry En to mo lo gy 12: 89-97. des ) fron ta lis .Ac ta Vi ro lo gi ca 43: 279-283. [19] EFSA Pa nel on Ani mal He alth and We lfa re [31] Adam ska M. 2006. Wek tor i re zer wu ar Bar to nel la (AHAW). Scien ti fic Opi nion on Geo gra phic Di stri- spp. In: Bio lo gia mo le ku lar na pa to ge nów prze no szo- bu tion of Tick- bor ne In fec tions and the ir Vec tors in nych przez klesz cze . (Ed. B. Sko tar czak). Wy daw nic- Eu ro pe and the other Re gions of the Me di ter ra ne an two Le kar skie PZWL, War sza wa: 203-211. Ba sin. 2010. 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ne and Zo ono tic Di se ases 11: 877-882. ska- Ba do ra J., Zwo liń ski J., Bu czek A., Dut kie wicz J. [33] Fo men ko N.V., Bor go ia kov VIu., Pa nov V.V. 2011. 2006. Pre va len ce of Bor re lia burg dor fe ri ge no spe cies Ge ne tic fe atu res of Bor re lia miy amo toi trans mit ted in Ixo des ri ci nus ticks from Lu blin re gion (eastern by Ixo des per sul ca tus . Mo le ku liar na ia Ge ne ti ka, Mi- Po land). An nals of Agri cul tu ral and Envi ron men tal kro bio lo gia i Vi ru so lo gia . 2: 12-17. Me di ci ne 13: 301-306. [34] Ka tar gi na O., Gel ler J., Va si len ko V., Ku znet so va [43] Grzesz czuk A., Stań czak J. 2006. Hi gh ly va ria ble T., Järvekülg L., Ve ne S., Lund kvist Ĺ., Go lo vl jo va I. year to year pre va len ce of Ana pla sma pha go cy to phi- 2011. De tec tion and cha rac te ri za tion of Ba be sia spe- lum in Ixo des ri ci nus ticks in nor the astern Po land. Fo- cies in Ixo des ticks in Es to nia. Vec tor Bor ne and Zo - ur years fol low- up. An nals of New York Aca de my of ono tic Di se ases 11: 923-928. Scien ce 1078: 309-311. [35] Kol la ritsch H., Chmelík V., Dont sen ko I., Grzesz- [44] Kar bo wiak G. 2009. Kleszcz łą ko wy Der ma cen tor czuk A., Kon dru sik M., Uso nis V., La kos A. 2011. re ti cu la tus – wy stę po wa nie, bio lo gia i ro la ja ko wek- The cur rent per spec ti ve on tick -bor ne en ce pha li tis to ra cho rób od klesz czo wych. Roz pra wa ha bi li ta cyj- awa re ness and pre ven tion in six Cen tral and Eastern na. Agen cja Re kla mo wo- Wy daw ni cza A. Grze gor - Eu ro pe an co un tries: re port from a me eting of experts czyk, War sza wa. co nve ned to di scuss TBE in the ir re gion. Vac ci ne 20: [45] Kuź na- Gry giel W., Bu kow ska K., Ci choc ka A., Ko - 4556-4564. sik- Bo gac ka D., Sko tar czak B. 2002. The pre va len ce [36] Mo ro zo va O.V., Ca bel lo F.C., Do bro tvor sky A.K. of pi ro pla sms in a po pu la tion of Ixo des ri ci nus (Aca - 2004. Se mi- ne sted PCR de tec tion of Bar to nel la hen- ri: Ixo di dea) form north- we stern Po land. An nals of se lae in Ixo des per sul ca tus ticks from We stern Si be- Agri cul tu ral and Evi ron men tal Me di ci ne 9: 175-178. ria, Rus sia. Vec tor Bor ne and Zo ono tic Di se ases 4: [46] Pod sia dly E., Chmie lew ski T., So chon E., Ty lew- 306-309. ska- Wierz ba now ska S. 2007. Bar to nel la hen se lae in [37] Mo skvi ti na N.S., Ro ma nen ko V.N., Ter no vo - Ixo des ri ci nus ticks re mo ved from dogs. Vec tor- Bor- V.A., Iva no va N.V., Pro to po po va E.V., Kra vchen ko ne and Zo ono tic Di se ases 7:189-192. L.B., Ko no no va Iu.V., Ku ra no va V.N., Chau sov [47] Ry ma szew ska A. 2008. Wy kry wa nie i ana li za DNA E.V., Mo skvi tin S.S., Per shi ko va N.L., Ga sh kov Ric ket t sia he lve ti ca izo lo wa ne go z po pu la cji klesz cza S.I., Ko no va lo va S.N., Bol’sha ko va N.P., Lok tev po spo li te go Ixo des ri ci nus na Po mo rzu Za chod nim V.B. 2008. 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A risk of in fec tion with ticks of Ixo des ri ci nus le of ar th ro pods in envi ron ments at va rio us sta ges of (Lin na eus, 1758) spe cies (Aca ri: Ixo di dae) in so uth- an th ro po ge ni za tion. Sta te of in ve sti ga tions in Ixo di- -eastern Po land de pen ding on the da ily and se aso nal des, pa ra si tes of ro dents and on Ne ma to ce ra. Wia do- rhy thm. In Sta wo no gi. In wa zje i ich kon tro la. (Eds. A. mo ści Pa ra zy to lo gicz ne 22: 9-19. Bu czek, C. Bła szak). Aka pit, Lu blin: 31-43. [92] Siu da K., No wak M., Grycz K., So larz K. 2004. Stan [104] Ni ści gor ska J. 2006. Bo re lio za ja ko cho ro ba za wo- wia do mo ści nad roz prze strze nie niem Ixo des ri ci nus do wa le sni ków. In: Bio lo gia mo le ku lar na pa to ge nów (Lin na eus, 1758) (Aca ri: Ixo di da: Ixo di dae) na te re- prze no szo nych przez klesz cze. (Ed. B. Sko tar czak). nie wo je wódz twa ma ło pol skie go. In: Zró żni co wa nie i Wy daw nic two Le kar skie, PZWL War sza wa: prze mia ny śro do wi ska przy rod ni czo - kul tu ro we go 156-158. Wy ży ny Kra kow sko- Czę sto chow skiej. Vol. I. (Ed. J. [105] Ci sak E., Chmie lew ska- Ba do ra J., Zwo liń ski J., Par ty ka) Wy daw nic two Oj cow ski Park Na ro do wy, Wój cik- Fa tla A., Po lak J., Dut kie wicz J. 2005. Risk Oj ców: 295-301. of tick- bor ne bac te rial di se ases among wor kers of [93] Lach ma jer J., Skier ska B., We gner Z. 1956. Klesz- Roz to cze Na tio nal Park (so uth- eastern Po land). An - 150 M. Nowak-Chmura, K. Siuda

nals of Agri cul tu ral and Envi ron men tal Me di ci ne 12: na se ko mykh i kle sh chej. Iz da tel stvo Mo sko vsko go 127-132. Uni ver si te ta, Mo skva. [106] Grzesz czuk A. 2006. Ana pla sma pha go cy to phi lum [118] So nen shi ne D.E. 1993. Bio lo gy of ticks. Vol. 2. in Ixo des ri ci nus ticks and hu man gra nu lo cy tic ana- Oxford Uni ver si ty Press, Oxford, New York. pla smo sis se ro pre va len ce among fo re stry ran gers in [119] Fur man D.P., Lo omis E.C. 1984. The ticks of Ca - Bia ły stok re gion . Ad van ces in Me di cal Scien ces : 51: li for nia (Aca ri: Ixo di da). Bul le tin of the Ca li for nia In- 283-286. sect Su rvey 25: 1-239. [107] Zwo liń ski J., Chmie lew ska- Ba do ra J., Ci sak E., [120] Ko lo nin G.V. 2009. Fau na of ixo did ticks of the Bu czek A., Dut kie wicz J. 2004. Wy stę po wa nie prze- world (Aca ri, Ixo di dae). Mo scov. ciw ciał prze ciw Ana pla sma pha go cy to phi lum i Bor- [121] Chmie lew ska- Ba do ra J., Zwo liń ski J., Ci sak E., re lia burg dor fe ri u le śni ków w re gio nie lu bel skim. Wój cik -Fa tla A., Bu czek A., Dut kie wicz J. 2007. Pre - Wia do mo ści Pa ra zy to lo gicz ne 50: 221-227. va len ce of Ana pla sma pha go cy to phi lum in Ixo des ri- [108] Bar to sik K., Drącz kow ski P., Jung M., Ol szew ski ci nus ticks de ter mi ned by po ly me ra se cha in re ac tion K., Bu czek A. 2008. Ar ga sids and bed bugs in fe sta- with two pa irs of pri mers de tec ting 16S rRNA and an- tions in an urban are as. In: Sta wo no gi. Od dzia ły wa nie kA ge nes. An nals of Agri cul tu ral and Envi ron men tal na ży wi cie la . (Ed. A. Bu czek, C. Bła szak). Aka pit, Me di ci ne 14: 281-285. Lu blin: 29-45. [122] Chmie lew ski T., Pod sia dly E., Kar bo wiak G., Ty- [109] Bia duń W., Chy bow ski J. 2008. Roz miesz cze nie i lew ska -Wierz ba now ska S. 2009. Ric ket t siae spp. in względ na li czeb ność klesz cza po spo li te go Ixo des ri- ticks, Po land. Emer ging In fec tio us Di se ases 15: ci nus L. w gra ni cach ad mi ni stra cyj nych Lu bli na. In: 486-488. Fau na miast – Ochro nić ró żno rod ność bio tycz ną w [123] Ci sak E., Chmie lew ska- Ba do ra J., Raj tar B., Zwo- mia stach (Eds. P. In dy kie wicz, L. Je rzak, T. Bar- liń ski J., Ja błoń ski L., Dut kie wicz J. 2002. Stu dy on czak). SAR „Po mo rze” Byd goszcz: 303-308. the oc cur ren ce of Bor re lia burg dor fe ri sen su la to and [110] Kar bo wiak G., Siu da K. 2001. Wy stę po wa nie tick -bor ne en ce pha li tis vi rus (TBEV) in ticks col lec- klesz cza po spo li te go Ixo des ri ci nus (Aca ri: Ixo di da) ted in Lu blin re gion (eastern Po land). An nals of Agri- na te re nach re kre acyj nych du żych aglo me ra cji miej- cul tu ral and Envi ron men tal Me di ci ne 9: 105-110. skich w Pol sce i je go zna cze nie epi de mio lo gicz ne. 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In ten syw ność za ka że nia po pu la cji Ixo des ri ci- kręt ka mi Bor re lia burg dor fe ri s.l. na te re nie Wro cła- nus kręt ka mi Bor re lia burg dor fe ri sen su la to w la sach wia i Ślę żań skie go Par ku Kra jo bra zo we go. In: Sta wo - pół noc no -za chod niej Pol ski. Wia do mo ści Pa ra zy to lo- no gi. Śro do wi sko, pa to gen ny i ży wi cie le (Eds. A. Bu - gicz ne 49: 255-271. czek, C. Bła szak). Ko li ber, Lu blin: 113-118. [126] Kar bo wiak G., Siń ski E. 1994. Ro la klesz czy i [113] Siu da K., Pet’ko B., Stan ko M., Kar bo wiak G. drob nych ssa ków w sze rze niu się za ka żeń Bor re lia 2002. The di stri bu tion of the tick Ixo des ri ci nus (Lin- burg dor fe ri i Ba be sia mi cro ti . Prze gląd Epi de mio lo- na eus, 1758) (Aca ri: Ixo di da: Ixo di dae) on the area of gicz ny 48: 219-224. Kra ków. In: Po stę py pol skiej aka ro lo gii (Ed. S. Igna - [127] Kiew ra D., Ry dza nicz K., Lonc E. 2006. Pre va len- to wicz). Wy daw nic two SGGW, War sza wa: 119-130. ce of Bor re lia burg dor fe ri s.l. in Ixo des ri ci nus col- [114] Su per gan M., Gryt ner- Zię ci na B., Kar bo wiak G., lec ted from fi ve wo oded are as in Lo wer Si le sia (Po - Ha pu nik J. 2008. Roz miesz cze nie klesz czy w la sach i land). In: Sta wo no gi. Zna cze nie epi de mio lo gicz ne. par kach aglo me ra cji war szaw skiej. In: Sta wo no gi. (Eds. A. Bu czek, C. Bła szak). Ko li ber, Lu blin: Od dzia ły wa nie na ży wi cie la . (Eds. A. Bu czek, C. Bła- 183-187. szak). Aka pit, Lu blin: 63-71. [128] Ko sik- Bo gac ka D., Kuź na -Gry giel W., Bu kow ska [115] Ma nil la G. 1998. Fau na d’Ita lia. Aca ri. Ixo di da . K., Ja bo row ska M. 2006. Ro le of mo squ ito es and Edi zio ni Cal de ro ni Bo lo gna, Bo lo gna, Ita ly. ticks in trans mis sion of so me of the epi zo otic di se- [116] Pe tri sh che va P.A., Zem skaya A.A. 1962. Ar ga so - ases. 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Ogrze wal ska M., Behn ke J.M. 2006. Ba be sia mi cro- A. Bu czek. C. Bła szak). Aka pit, Lu blin: 105-113. ti : pre va len ce in wild ro dents and Ixo des ri ci nus ticks [140] Kon dru sik M., Pan ce wicz S.A., Gry gor czuk S., from the Ma zu ry La ke Di strict of North- Eastern Po- Czu pry na P., Mo niusz ko A., Zaj kow ska J.M. 2011. land. In ter na tio nal Jo ur nal of Me di cal Mi cro bio lo gy Pre wa len cja Ana pla sma pha go cy to phi lum w klesz- 296 S1: 137-143. czach Ixo des ri ci nus na te re nie wo je wódz twa pod la- [131] Sko tar czak B., Ci choc ka A. 2001. The oc cur ren ce skie go – oce na zró żni co wa nia se zo no we go i po mię - DNA of Ba be sia mi cro ti in ticks Ixo des ri ci nus in the dzy sta no wi ska mi. In: Sta wo no gi. Pa so ży ty czło wie ka fo rest are as of Szcze cin. Fo lia Bio lo gi ca 49: 247-250. i zwie rząt. (Eds. A. Bu czek, C. Bła szak). Aka pit, Lu- [132] Stań czak J., Ku bi ca -Bier nat B., Ra ce wicz M., Kru- blin: 95-104. mi nis- Ło zow ska W., Kur J. 2000. De tec tion of three [141] Pa weł czyk A., Siń ski E. 2004. Pre wa len cja za ka że - ge no spe cies of Bor re lia burg dor fe ri sen su la to in Ixo- nia klesz czy I. ri ci nus kręt ka mi Bor re lia burg dor fe ri des ri ci nus ticks col lec ted in dif fe rent re gions of Po- s.l.: se zo no we i rocz ne zmia ny. Wia do mo ści Pa ra zy- land. In ter na tio nal Jo ur nal of Me di cal Mi cro bio lo gy to lo gicz ne 50: 253-258. 290: 559-566. [142] Sy ty kie wicz H., Pu cyk A. 2007. De tec tion of Ba - [133] Sko tar czak B., Ry ma szew ska A., Wo dec ka B., be sia sp. DNA in com mon tick po pu la tion oc cu ring at Saw czuk M. 2003. Mo le cu lar evi den ce of co in fec tion Kam pi nos Na tio nal Park. W: Sta wo no gi. Śro do wi sko, of Bor re lia burg dor fe ri sen su la to, hu man gra nu lo cy- pa to ge ny i ży wi cie le. (Eds. A. Bu czek, C. Bła szak). tic ehr li chio sis agent, and Ba be sia mi cro ti Wy daw nic two Ko li ber, Lu blin: 147 -152. in ticks from north- we stern Po land. Jo ur nal of Pa ra- [143] Wój cik- Fa tla A., Ci sak E., Chmie lew ska- Ba do ra si to lo gy 89: 194-196. J., Zwo liń ski J., Bu czek A., Dut kie wicz J. 2006. Pre - [134] Stań czak J., Ra ce wicz M., Ku bi ca -Bier nat B., Kru- va len ce of Ba be sia mi cro ti in Ixo des ri ci nus ticks mi nis- Ło zow ska W., Dą brow ski J., Adam czyk A., from Lu blin re gion (eastern Po land). An nals of Agri- Mar kow ska M. 1999. Pre va len ce of Bor re lia burg- cul tu ral and Envi ron men tal Me di ci ne 13: 319-322. dor fe ri sen su la to in Ixo des ri ci nus ticks (Aca ri, Ixo- [144] Wój cik- Fa tla A., Ci sak E., Za jąc V., Zwo liń ski J., di dae) in dif fe rent Po lish wo odlands. An nals of Agri- Dut kie wicz J. 2011. Pre va len ce of tick- bor ne en ce - cul tu ral and Envi ron men tal Me di ci ne 6: 127-132. pha li tis vi rus in Ixo des ri ci nus and Der ma cen tor re ti- [135] We gner Z., Stań czak J., Ra ce wicz M., Kru mi nis- cu la tus ticks col lec ted from the Lu blin re gion (eastern -Ło zow ska W., Ku bi ca -Bier nat B. 1993/1994. Oc cur - Po land). Ticks and Tick -bor ne Di se ases 2: 16-19. ren ce of Bor re lia spi ro cha etes in ticks (Aca ri, Ixo di- [145] Zy gner W., Bą ska P., Wi śniew ski M., Wę dry cho- dae) col lec ted in the fo rest are as in Olsz tyn Pro ven ce wicz H. 2010. The mo le cu lar evi den ce of Ba be sia mi- (north- cen tral Po land). Bul le tin of the In sti tu te of Ma- cro ti in hard ticks re mo ved from dogs in War saw ri ti me and Tro pi cal Me di ci ne in Gdy nia 44/45: 51-59. (cen tral Po land). Po lish Jo ur nal of Mi cro bio lo gy 59: [136] Bia duń W., Rzy mow ska J., Stę pień- Ru kasz H., 95-97. Niem czyk M., Chy bow ski J. 2007. The oc cu ren ce of [146] Bar to sik K., Ku brak T., Ol szew ski T., Jung M., Bu- Bor re lia burg dor fe ri sen su la to in Ixo des ri ci nus and czek A. 2008. Pre ven tion of tick bi tes and pro tec tion Der ma cen tor re ti cu la tus ticks col lec ted from roe de- aga inst tick- bor ne di se ases in So uth- Eastern Po land. er and de er shot in the so uth- eastern Po land. Bul le tin An nals of Agri cul tu ral and Envi ron men tal Me di ci ne of the Ve te ri na ry In sti tu te in Pu ła wy 51: 213-217. 15: 181-185. [137] Cie pie la A.P., Ko moń T., Sy ty kie wicz H. 2006. [147] Bar to sik K., La chow ska- Ko tow ska P., Szy mań ska Pre li mi na ry stu dies on the pre va len ce of Bor re lia J., Wój cik- Fa tla A., Pa bis A., Bu czek A. 2011. Envi - burg dor fe ri sen su la to in Ixo des ri ci nus (L.) wi thin ron men tal con di tio ning of in ci den ce of tick- bor ne en - Nad bu żan ski Land sca pe Park. In: Sta wo no gi. Zna cze- ce pha li tis in the so uth- eastern Po land in 1996–2006. nie epi de mio lo gicz ne. (Eds. A. Bu czek, C. Bła szak). An nals of Agri cul tu ral and Envi ron men tal Me di ci ne Wy daw nic two Ko li ber, Lu blin: 213-219. 18: 119-126. [138] Cu ber P., Asman M., So larz K., Szil man E., Szil - [148] Bar to sik K., Si tarz M., Szy mań ska J., Bu czek A. man P. 2010. Pierw sze stwier dze nia obec no ści wy- 2011. Tick bi tes on hu mans in the agri cul tu ral and re- bra nych pa to ge nów cho rób trans mi syj nych w klesz- cre atio nal are as in so uth- eastern Po land. An nals of czach Ixo des ri ci nus (Aca ri: Ixi di dae) ze bra nych w Agri cul tu ral and Envi ron men tal Me di ci ne 18: oko li cach zbior ni ków wod nych w Ro goź ni ku (wo je- 151-157. wódz two ślą skie). In: Sta wo no gi. Eko lo gicz ne i pa to- [149] Bu czek A., Bar to sik K., Ru dek A., Ru dek M., Wój- lo gicz ne aspek ty ukła du pa so żyt- ży wi ciel. (Eds. A. cik- Fa tla A., Szy mań ska J., Iskrzyń ska- Po pio łek Ż. Bu czek, C. Bła szak.). Aka pit, Lu blin: 155-164. 2010. Envi ron men tal con di tio ning of bor re lio sis in [139] Cu ber P., Asman M., So larz K., Szil man E., Szil - fo re stry wor kers of va rio us fo rest in spec to ra tes in the man.P. 2011. The pre va len ce of Ana pla sma pha go cy- cen tral part of Po land. In: Sta wo no gi. Eko lo gicz ne i to phi lum and Ba be sia sp. in ticks (Aca ri: Ixo di da) pa to lo gicz ne aspek ty ukła du pa so żyt- ży wi ciel. (Eds. col lec ted from re cre atio nal are as of Si le sian Pro vin ce. A. Bu czek, C. Bła szak). Wy daw nic two Aka pit, Lu - In: Sta wo no gi. Pa so ży ty czło wie ka i zwie rząt . (Eds. blin: 207-219. 152 M. Nowak-Chmura, K. Siuda

[150] Ci sak E., Chmie lew ska- Ba do ra J., Zwo liń ski J., la tion ship be twe en Ana pla sma pha go cy to phi lum in- Dut kie wicz J., Pa tor ska- Mach E. 2003. Oce na czę sto- fec tion in Ixo des ri ci nus ticks and expo sed fo re stry ści za ka żeń wi ru sem klesz czo we go za pa le nia mó zgu wor kers on the ter ri to ry of Lu blin Re gion. Zdro wie i kręt ka mi Bor re lia burg dor fe ri wśród rol ni ków in- Pu blicz ne 117: 134-137. dy wi du al nych na te re nie Lu belsz czy zny. Me dy cy na [161] Ry ma szew ska A. 2007. Sym bio tic bac te ria in Pra cy 54: 139-144. oocy te and ova rian cell mi to chon dria of the tick Ixo - [151] Ci sak E., Wój cik- Fa tla A., Za jąc V., Sro ka J., Bu - des ri ci nus : bio lo gy and phy lo ge ne tic po si tion. Pa ra- czek A., Dut kie wicz J. 2010. Pre va len ce of tick- bor - si to lo gy Re se arch 100: 917-920. ne en ce pha li tis vi rus (TBEV) in sam ples of raw milk [162] Wo dec ka B. 2011. FlaB ge ne as a mo le cu lar mar - ta ken ran dom ly from cows, go ats and she ep in eastern ker for di stinct iden ti fi ca tion of Bor re lia spe cies in Po land. An nals of Agri cul tu ral and Envi ron men tal envi ron men tal sam ples by the PCR- re stric tion frag- Me di ci ne 17: 283- 286. ment length po ly mor phism me thod. Ap plied and [152] Ci sak E., Zwo liń ski J., Chmie lew ska- Ba do ra J., Envi ron men tal Mi cro bio lo gy 77: 7088-7092. Dut kie wicz J., Wój cik- Fa tla A., Za jąc V. 2011. Ana - [163] Wo dec ka B., Le on ska A., Sko tar czak B. 2010. A ly sis of the sta te of know led ge and awa re ness in the com pa ra ti ve ana ly sis of mo le cu lar mar kers for the de- area of tick- bor ne di se ases pro phy la xis in the po pu la- tec tion and iden ti fi ca tion of Bor re lia spi ro cha etes in tion at oc cu pa tio nal risk. Zdro wie Pu blicz ne 121: 47- Ixo des ri ci nus . Jo ur nal of Me di cal Mi cro bio lo- 51. gy 59: 309-314. [153] Fli siak R., Pro ko po wicz D., Fli siak I., Bo brow ska [164] Siń ski E. 2009. Wpływ ko in fek cji u klesz czy (Ixo- E., Mię goć H., Grzesz czuk A., Su lik E., Oko łów C. di dae) na trans mi sję mi kro pa so ży tów krwi. Wia do- 1994. Za gro że nie en de micz ne Bo re lio zą z Ly me w mo ści Pa ra zy to lo gicz ne 55: 341-347. re gio nie Pusz czy Bia ło wie skiej. Prze gląd Epi de mio- [165] Sko tar czak B., Wo dec ka B., Ci choc ka A. 2002. lo gicz ny 3: 211-217. Co exi sten ce DNA of Bor re lia burg dor fe ri sen su la to [154] Haj dul M., Za rem ba M., Kar bo wiak G., Siń ski E. and Ba be sia mi cro ti in Ixo des ri ci nus ticks from 2006. Ry zy ko za ka że nia kręt ka mi Bor re lia burg dor- north -we stern Po lan d An nals of Agri cul tu ral and fe ri s. l. w bio to pach le śnych oko lic War sza wy. In: Envi ron men tal Me di ci ne 9: 25-28. Sta wo no gi. Zna cze nie epi de mio lo gicz ne. (Eds. A. Bu- [166] Sko tar czak B ., Adam ska M ., Saw czuk M ., Ma cie - czek, C. Bła szak), Wy daw nic two Ko li ber, Lu blin: jew ska A., Wo dec ka B., Ry ma szew ska. A. 2008. Co- 195-203. exi sten ce of tick- bor ne pa tho gens in ga me ani mals [155] Kiew ra D., Do brac ki W., Lonc E, Do brac ka B. and ticks in we stern Po land. Ve te ri nar ni Me di ci- 2004. Eks po zy cja na ukłu cia przez klesz cze a wy stę- na 53: 668-675. po wa nie ru mie nia wę dru ją ce go u pa cjen tów z bo re- [167] Stań czak J., Ra ce wicz M., Kru mi nis- Ło zow ska lio zą z Ly me na te re nie Dol ne go Ślą ska. Prze gląd W., Ku bi ca -Bier nat B. 2002. Co in fec tion of Ixo des ri- Epi de mio lo gicz ny 58: 281-288. ci nus (Aca ri: Ixo di dae) in north Po land with the [156] Kon dru sik M., Mie dziń ska T., Pan ce wicz S.A., agents of Ly me bor re lio sis (LB) and hu man gra nu lo- Zaj kow ska J.M., Gry gor czuk S.S., Świerz biń ska R., cy tic ehr li chio sis (HGE). In ter na tio nal Jo ur nal of Sa niu tycz- Ku ro czyc ki S., Her ma now ska -Szpa ko wicz Me di cal Mi cro bio lo gy 33: 198-201. T 2004. Za cho ro wa nia na klesz czo we za pa le nie mó - [168] Pan ce wicz S., Du naj J., Zaj kow ska J., Kon dru sik zgu (KZM) w woj. bia ło stoc kim- pod la skim w la tach M., Gry gor czuk S., Mo niusz ko A., Czu pry na P., 1993-2002. Prze gląd Epi de mio lo gicz ny 58: 273-280. Wierz biń ska R. 2011. Wy stę po wa nie ko in fek cji wi ru- [157] Lej brandt E., Szlen dak E. 2004. Bo re lio za z Ly me sem klesz czo we go za pa le nia mó zgu, B. burg dor fe ri , w wo je wódz twie ma zo wiec kim w 2003 ro ku. In: Sta - A. pha go cy to phi lum i Ba be sia sp. u cho rych le czo- wo no gi. In te rak cje pa so żyt- ży wi ciel . (Eds. A. Bu czek, nych z po wo du za pa leń opon mó zgo wo -rdze nio wych C. Bła szak) Wy daw nic two Li ber, Lu blin: 193-200. po eks po zy cji na po kłu cie przez klesz cze – do nie sie- [158] Pan ce wicz S.A., Zaj kow ska J., Kon dru sik M., nie wstęp ne. In: Sta wo no gi. Pa so ży ty czło wie ka i Snar ska -Fur ła I., Świer biń ska R., Her ma now ska - zwie rząt (Eds. A. Bu czek, C. Bła szak). Aka pit, Lu- -Szpa ko wicz T. 1998. Wy kry wal ność prze ciw ciał blin: 115-123. prze ciw ko Bor re lia burg dor fe ri wśród pra cow ni ków [169] Chmie lew ska- Ba do ra J., Ci sak E., Za jąc V., Zwo- le śnic twa w pół noc no- wschod nim re gio nie Pol ski. liń ski J., Dut kie wicz J. 2010. Wy stę po wa nie współ za- Me dy cy na Pra cy 3: 253- 260. ka żeń Bor re lia burg dor fe ri , Ana pla sma pha go cy to- [159] Pod sia dły E., Chmie lew ski T., Kar bo wiak G., Kę- phi lum , Bar to nel la spp. i Ba be sia mi cro ti u pa cjen tów dra E., Ty lew ska- Wierz ba now ska S. 2011. The oc - z roz po zna niem bo re lio zy. Me dy cy na Ogól na 16: cur ren ce of spot ted fe ver ric ket t sio ses and other tick- 217-225. -bor ne in fec tions in fo rest wor kers in Po land. Vec tor- [170] Adam ska M. 2006. DNA Ana pla sma pha go cy to- -Bor ne and Zo ono tic Di se ases 11: 985-989. phi lum we krwi sa ren oraz w po zy ska nych z nich [160] Zwo liń ski J., Wój cik- Fa tla A., Chmie lew ska- Ba - klesz czach. Me dy cy na We te ry na ryj na 62: 201-203. do ra J., Ci sak E., Bu czek A., Dut kie wicz J. 2007. Re- [171] Adam ska M. 2008. Wild ru mi nants in the area of Ticks of Poland 153

the north- we stern Po land as po ten tial re se rvo ir ho sts J.S. 2007. Ana pla smo sis in hu mans. In: Ric ket t sial di- of Bar to nel la scho en bu chen sis and Bar to nel la bo vis . se ases old and new. (Eds. P. Pa ro la, D. Ra oult). Tay- Ac ta Pa ra si to lo gi ca 53: 407-410. lor and Fran cis Gro up, In fo ram He al th ca re, USA, Inc. [172] Saw czuk M., Ma cie jew ska A., Sko tar czak B. 2008. New York, Lon don: 223-236. Iden ti fi ca tion and mo le cu lar cha rac te ri za tion of The - [184] Kon dru sik M., Gry gor czuk S., Sko tar czak B., Wo- ile ria sp in fec ting red de er ( Ce rvus ela phus ) in nor th- dec ka B., Ry ma szew ska A., Pan ce wicz S., Zaj kow ska we stern Po land. Eu ro pe an Jo ur nal of Wil dli fe Re se- J., Świerz biń ska R., Her ma now ska- Szpa ko wicz T. arch 54: 225-230. 2007. Mo le cu lar and se ro lo gi cal dia gno sis of Bor re- [173] Sko tar czak B., Adam ska M. 2005. De tec tion of lia burg dor fe ri in fec tion among pa tients with dia gno- Bar to nel la DNA in roe de er ( Ca pre olus ca pre olus ) sed Ery the ma mi grant. An nals of Agri cul tu ral and and in ticks re mo ved from de er. Eu ro pe an Jo ur nal of Envi ron men tal Me di ci ne 14: 159-163. Wil dli fe Re se arch 51: 287-290. [185] Pro ko po wicz D. 1995. Cho ro by prze no szo ne przez [174] Grzesz czuk A., Ziar ko S., Pro ko po wicz D., Ra dzi- klesz cze. Wy daw nic two Fun da cji PB Bűchne ra, War- won P.M. 2004. Za ka że nie żu brów z Pusz czy Bia ło - sza wa. wie skiej bak te ria mi Ana pla sma pha go cy to phi lum . [186] Ty lew ska -Wierz ba now ska S., Chmie lew ski T., Me dy cy na We te ry na ryj na 60: 600-601. Kon dru sik M., Her ma now ska- Szpa ko wicz T., Sa wic - [175] Sko tar czak B., Koś W., Wo dec ka B., Ry ma szew- ki W., Su łek K. 2001. First ca ses of acu te hu man gra- ska A., Saw czuk M., Zaj kow ska J., Pan ce wicz S., nu lo cy tic ehr li chio sis in Po land. Eu ro pe an Jo ur nal of Świerz biń ska P. 2003. Pies do mo wy ja ko re zer wu ar Cli ni cal Mi cro bio lo gy and In fec tio us Di se- kręt ków Bor re lia burg dor fe r i sen su la to z te re nów ases 20:196-198. en de micz nych dla cho ro by z Ly me w Pół noc no -Za - [187] Iz deb ska J.N. 2006. Po rów na nie sa mic klesz czy chod niej Pol sce. In: Sta wo no gi i ży wi cie le (Eds. A. Ixo des ri ci nus z żu brów i in nych ży wi cie li z ró żnych Bu czek, C. Bła szak). Aka pit, Lu blin: 231-240. re jo nów Pol ski. In: Per spek ty wy roz wo ju po pu la cji [176] Zy gner W., Gór ski P., Wę dry cho wicz H. 2009. De - żu brów . (Ed. W. Olech).Wy daw nic two Ar ti sco: tec tion of the DNA of Bor re lia afze lii , Ana pla sma 85-89. pha go cy to phi lum and Ba be sia ca nis in blo od sam ples [188] Szlen dak E. 2008. Ana to mia syn gan glio nu Ixo des from dogs in War saw. Ve te ri na ry Re cord 164: sca pu la ris Say (Aca ri: Ixo di dae) z uwzględ nie niem 465-467. roz miesz cze nia wy bra nych grup ko mó rek neu ro se- [177] Pa weł czyk A., Siń ski E. 2000. Pre va len ce of IgG kre cyj nych oraz przy pusz czal na ro la syn gan glio nu w an ti bo dies re spon se to Bor re lia burg dor fe ri s.l. in po- re gu la cji wi te lo ge ne zy i syn te zy ek dy ste ro idów. Wy- pu la tions of wild ro dents from Ma zu ry La kes Di strict daw nic two SGGW, Warszawa. re gion of Po land. An nals of Agri cul tu ral and Envi- [189] Bar to sik K., Drącz kow ski P., Kwe starz E., Wo ło- ron men tal Me di ci ne 7: 79-83. szyn- Ho rak E., Bu czek A. 2010. Mor pho me tric fe atu- [178] Pa weł czyk A., Siń ski E. 2001. Współ wy stę po wa- res of Hal ler’s or gan in Ixo des ri ci nus (L.) ticks (Aca- nie Bor re lia ga ri nii i B. afze lii wśród po pu la cji gry zo- ri: Ixo di da: Ixo di dae) of Po lish po pu la tion. In: Sta wo- ni le śnych. Wia do mo ści Pa ra zy to lo gicz ne 47: no gi. Eko lo gicz ne i pa to lo gicz ne aspek ty ukła du pa- 741-746. so żyt- ży wi ciel. (Eds. A. Bu czek, C. Bła szak). Wy- [179] Mi cha lik J., Wo dec ka B., Sko rac ki M., Si ko ra B., daw nic two Aka pit, Lu blin: 75-82. Stań czak J. 2008. Pre va len ce of avian- as so cia ted Bor- [190] Bo czek J., Szlen dak E. 2005. Fe ro mo ny klesz czy i re lia burg dor fe ri s.l. ge no spe cies in Ixo des ri ci nus in nych roz to czy. In: Sta wo no gi. Ró żno rod ność form i ticks col lec ted from black birds ( Tur dus me ru la ) and od dzia ły wań. (Eds. A. Bu czek, C. Bła szak). Wy daw - song thru shes ( T. phi lo me los ). In ter na tio nal Jo ur nal nic two Ko li ber, Lu blin: 69-76. of Me di cal Mi cro bio lo gy 298S1: 129-138. [191] Bu czek A. 2000. Expe ri men tal te ra to ge ny in the [180] Chmie lew ska- Ba do ra J., Ci sak E., Dut kie wicz J. tick Hy alom ma mar gi na tum mar gi na tum (Aca ri: Ixo- 2000. Ly me bor re lio sis and mul ti ple scle ro sis: any di da: Ixo di dae): Ef fect of high hu mi di ty on em bry- con nec tion? A se ro epi de mic stu dy. An nals of Agri cul- onic de ve lop ment. Jo ur nal of Me di cal En to mo lo gy tu ral and Envi ron men tal Me di ci ne 7: 141-143. 37: 807-814. [181] Grzesz czuk A. 2004. Hu man ana pla smo sis – emer- [192] Siu da K., No wak M., Ko wal czyk M., Górz A., Pik - ging tick- bor ne di se ase. In: Sta wo no gi . In te rak cje pa- sa K., Szyl man P., Kar bo wiak G. 2006. Ca ses of ano- so żyt- ży wi ciel. (Eds. A. Bu czek, C. Bła szak). Wy - ma lies of ticks col lec ted from na tu ral envi ron ment daw nic two Li ber, Lu blin: 103-108. (Aca ri: Ixo di da: Ixo di dae). In: Ad van ces in Po lish [182] Grzesz czuk A., Stań czak J. 2006. High pre va len ce Aca ro lo gy . (Eds. G. Ga bryś, S. Igna to wicz). SGGW, of Ana pla sma pha go cy to phi lum in fec tion in ticks re- War sza wa: 304-311. mo ved from hu man skin in north- eastern Po land. An - [193] Ja sik K., Bu czek A. 2004. De ve lop ment of the sa- nals of Agri cul tu ral and Envi ron men tal Me di ci ne 13: li va ry glands in em bry os of Ixo des ri ci nus (Aca ri: 1-4. Ixo di dae). Expe ri men tal and Ap plied Aca ro lo gy 32: [183] Grzesz czuk A., Bar N.C., Bak ken S.J., Dum ler 219-229. 154 M. Nowak-Chmura, K. Siuda

[194] Ja sik K., Bu czek A. 2005. Ori gin of ali men ta ry wa nia Ixo des ri ci nus (L.) na pta kach wę drow nych. tract in em bry oge ne sis of Ixo des ri ci nus (Aca ri: Ixo- Wia do mo ści Pa ra zy to lo gicz ne 17: 417-426. di dae). Jo ur nal of Me di cal En to mo lo gy 42: 541-547. [206] Paw lik B., Dy mon M., Ko chan W., Siu da K. 1973. [195] Bu czek A., Ku śmierz A., Ol szew ski K., Bu czek L., Sto pień za klesz cze nia drob nych ssa ków w Oj cow- Czer ny K., Łań cut M. 2002. Com pa ri son of rab bit skim Par ku Na ro do wym. Wia do mo ści Pa ra zy to lo- skin chan ges after fe eding of Ixo des ri ci nus (L.) and gicz ne 19: 735-745. Der ma cen tor re ti cu la tus (Fabr.). In: Aca rid phy lo ge- [207] Fry de ryk S. 2000. Pa so żyt ni cze Aca ri dzi ka ( Sus ny and evo lu tion: ada pta tion in mi tes and ticks. (Eds. scro fa L.) z Po je zie rza Po mor skie go. Wia do mo ści F. Ber ni ni, R. Nan nel li, G. Nuz za ci, E. de Lil lo). Pro- Pa ra zy to lo gicz ne 46: 163-168. ce edings of the IV Sym po sium of the Eu ro pe an As so- [208] Iz deb ska J.N. 1998. Wy stę po wa nie Der ma cen tor cia tion of Aca ro lo gi sts, Klu wer Acad. Publ., Do- re ti cu la tus (Aca ri, Ixo di dae) u żu bra ( Bi son bo na sus ) rdrecht: 419-424. z Pusz czy Bia ło wie skiej. Prze gląd Zo olo gicz ny 42: [196] Kar bo wiak G. 2000. The ro le of Apo de mus fla vi- 219-221. col lis and Cle th rio no mys gla re olus as ho sts of Ixo des [209] Iz deb ska J.N. 2001. Eu ro pe an bi son ar th ro pod ri ci nus and Der ma cen tor re ti cu la tus in nor thern Po - from clo sed Po lish bre eding fa ci li ties. Ac ta Pa ra si to- land. In: Pro ce edings of the 3rd In ter na tio nal Con fe- lo gi ca 46: 135-137. ren ce Ticks and Tick - bor ne pa tho gens in to the 21st [210] Iz deb ska J.N. 2004. Ob ser wa cje lo ka li za cji klesz- cen tu ry. (Eds. M. Ka zimírová, M. La bu da, P.A. Nut- czy (Aca ri, Ixo di dae) u żu brów ( Bi son bo na sus ) w tall). High Ta tra Mo un ta ins, Slo va kia 30 Au gust - 3 Pol sce. In: Sta wo no gi. In te rak cje pa so żyt- ży wi ciel . Sep tem ber 1999. In sti tu te of Zo olo gy SAS, Bra ti sla- (Eds. A. Bu czek, C. Bła szak). Wy daw nic two Li ber, va: 181-183. Lu blin: 45-51. [197] Kar bo wiak G., Iz deb ska J.N., Cza pliń ska U., Wi ta [211] Iz deb ska, J.N., Cy dzik K. 2010. Ana ly sis of the re- I. 2003. Przy pad ki zi mo wa nia klesz czy z ro dzi ny Ixo - asons for dif fe ren ces in to pi cal spe ci fi ci ty among va- di dae na ży wi cie lach w Pusz czy Bia ło wie skiej. In: rio us spe cies of tick (Aca ri, Ixo di dae) in fe sting Eu ro- Sta wo no gi i ży wi cie le . (Eds. A. Bu czek, C. Bła szak). pe an bi son (Aca ri, Ixo di dae) in fe sting Eu ro pe an bi- Li ber, Lu blin: 77-82. son. Eu ro pe an Bi son Con se rva tion New slet ter 3: [198] Siu da K., Maj szak A., No wak M. 2006. Ticks 75-84. (Aca ri: Ixo di da) pa ra si ti zing birds (Aves) in Po land. [212] Iz deb ska J.N., Rol biec ki L. 2004. An ana ly sis of Bio lo gi cal Let ters 43: 147-151. symp toms of pa ra si tic ar th ro pod in fe sta tion on bi son [199] Bia duń W., Kra sno dęb ski S. 2007. Wy stę po wa nie skin. (Eds. M. Ka ra siń ska, K. Da lesz czyk). In: Proc- klesz cza po spo li te go Ixo des ri ci nus L. w śro do wi- ce dings of Con fe ren ce of Eu ro pe an Bi son Con se rva- skach o ró żnym stop niu i cha rak te rze an tro po pre sji. tion, Mam mals Re se arch In sti tu te PAS, Bia ło wie ża: Wia do mo ści Pa ra zy to lo gicz ne 53: 133-137. 58-61. [200] Kiew ra D., Lonc E., Żysz kow ska W., Ry dza nicz K. [213] Ję dry sik D. 2006. Sta wo no gi pa so żyt ni cze sar ny 2008. Roz prze strze nie nie klesz czy Ixo des ri ci nus w Ca pre olus ca pre olus (L.) z te re nów Po je zie rzy Po łu - Ma sy wie Ślę ży (Dol ny Śląsk) – ma po wa nie i wi zu ali- dnio wo bał tyc kich. Ph.D. The sis, Uni ver si ty of za cja da nych śro do wi sko wych z za sto so wa niem GIS. Gdańsk. In: Sta wo no gi. Od dzia ły wa nie na ży wi cie la (Eds. [214] Ka dul ski S. 1996. Dal sze ba da nia nad sta wo no ga - A. Bu czek, C. Bła szak). Aka pit, Lu blin: 81-86. mi pa so żyt ni czy mi ło sia Al ces al ces w Pol sce. Wia do- [201] Kiew ra D., Lonc E., Ry dza nicz K. 2009. Kar to wa- mo ści Pa ra zy to lo gicz ne 42: 349-355. nie śro do wi sko wych ba dań pa ra zy to lo gicz nych na [215] Ka dul ski S., Szczu rek B. 2004. Ec to pa ra si tes on przy kła dzie klesz czy po spo li tych Ixo des ri ci nus . Wia- fal low de er, Da ma da ma (L.) in Po me ra nia, Po land. do mo ści Pa ra zy to lo gicz ne 9: 399-404. Ac ta Pa ra si to lo gi ca 49: 80-86. [202] No wak M., Siu da K. 2009. Klesz cze. In: Ma gur ski [216] Zy gner W., Wę dry cho wicz H. 2006. Oc cur ren ce of Park Na ro do wy – Mo no gra fia Przy rod ni cza. (Eds. A. hard ticks in dogs from War saw area. An nals of Agri- Gó rec ki, B. Ze ma nek). Kremp na, Kra ków: 177-180. cul tu ral and Envi ron men tal Me di ci ne 13: 355-359 [203] Siu da K., Ślu sar czyk J., No wak M. 2001. Roz prze- [217] Fry de ryk S. 1998. No we in te re su ją ce stwier dze nie strze nie nie klesz cza Ixo des ri ci nus (Lin na eus, 1758) Der ma cen tor re ti cu la tus (Fabr.) (Aca ri, Ixo di dae) na (Aca ri: Ixo di da: Ixo di dae) na te re nie Gar bu Ten czyń- dzi ku ( Sus scro fa L.). Wia do mo ści Pa ra zy to lo gicz ne skie go. In: Ba da nia na uko we w po łu dnio wej czę ści 44: 737-739. Wy ży ny Kra kow sko- Czę sto chow skiej (Ed. J. Par ty ka). [218] Bog da szew ska Z. 2004. Wy stę po wa nie i eko lo gia Wy daw ca Oj cow ski Park Na ro do wy: 295-298. klesz cza łą ko we go Der ma cen tor re ti cu la tus (Fa bri- [204] Sko tar czak B., So ro ka M., Wo dec ka B. 1999. Wy- cius, 1794) w ogni sku ma zur skim. I. Okre śle nie obec- stę po wa nie Ixo des ri ci nus na wy bra nych te re nach re - ne go za się gu wy stę po wa nia. Wia do mo ści Pa ra zy to lo- kre acyj nych wo je wódz twa szcze ciń skie go. Wia do- gicz ne 50: 727-730. mo ści Pa ra zy to lo gicz ne 45: 507-517. [219] Bog da szew ska Z., Kar bo wiak G., Siu da K. 2006. [205] Kahl K. 1971. Przy czy nek do zna jo mo ści wy stę po- Wy stę po wa nie i bio lo gia klesz cza łą ko we go Der ma - Ticks of Poland 155

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