Ticks and Tick-borne Diseases 5 (2014) 41–47

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Mini Review

Tick pests and vectors (Acari: Ixodoidea) in European towns: Introduction, persistence and management夽 Igor Uspensky ∗ A. Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem 91904, Israel

a r t i c l e

i n f o

Article history: Received 18 February 2013 Received in revised form 13 June 2013 Accepted 3 July 2013 Available online 14 October 2013 Keywords: Ticks Urban areas Tick introduction Tick persistence Tick management Tick-borne diseases

a b s t r a c t Ticks have always been a part of fauna in and around human settlements, and their significance changed concurrently with the enlargement of settlements and their transformation into towns. The increased rate of urbanization during the last decades has created a new reality for tick existence. Two groups of ticks are of major concern for modern towns: those living under natural conditions of urban surroundings and those well-adapted to urban conditions. During the process of urbanization, encroachment into forested and uncultivated areas as well as protection of existing green spaces create opportunities for ticks living in nature to also exist under urban and suburban conditions. Conditions of modern urban and especially suburban environment in developed European countries adequately meet tick requirements. Tick species having an advantage in urban areas are those that can use one and the same host at all parasitic stages, can starve for a prolonged time, can use either urban pests or domesticated animals as hosts, and can live in man-made buildings. The ticks of the Argas reflexus group (Argasidae) and the brown dog tick Rhipicephalus sanguineus (Ixodidae) comply with practically all conditions necessary for successful survival in urban areas. The ability of ticks to transmit numerous human and animal pathogens and the presence of many reservoir hosts in urban and suburban areas create persistent danger for human populations and domestic animals. Impact on urban ticks should be directed against the two major requirements of tick existence: reducing populations of potential tick hosts (feral pigeons, stray dogs and cats, and urban rodents), and changing other environmental conditions to make them less suitable for ticks. It is especially important that urban inhabitants be properly informed about the danger posed by ticks, the sites of possible tick attacks, and basic self-protection techniques. © 2013 Elsevier GmbH. All rights reserved.

Introduction In recent decades, the rate of urbanization has been accelerating worldwide. Development of urban areas has been followed by dramatic changes in floral and faunal biodiversity, affecting vectors of human and animal diseases and making a strong impact on wildlife-pathogen interactions (Bradley and Altizer, 2007; Decker et al., 2010). The fast urbanization is followed by increased mobility of the human population, intensive long-distance trade, and new contacts of humans and their pets with nature, all of which may contribute to changing of epidemiological and epizootiological conditions in and around towns. Ticks have always been a

夽 A short version of this paper was presented at the XI International Jena Symposium on Tick-Borne Diseases, Weimar, Germany, March 2011. ∗ Present address: 16, Yustman Moshe Street, Apt. 65, Jerusalem 93842, Israel. Tel.: +972 2 6450056. E-mail addresses: [email protected], [email protected] 1877-959X/$ – see front matter © 2013 Elsevier GmbH. All rights reserved. http://dx.doi.org/10.1016/j.ttbdis.2013.07.011

part of urban fauna, especially in suburban areas. The urbanization and human activities connected with it may often positively influence the occurrence and abundance of ticks both in short-term and in long-term perspectives, in developed as well as in developing countries. The increased rate of urbanization has attracted attention to the problem of vectors and vector-borne diseases in urban areas (Gratz, 1999; Comer et al., 2001; Robinson, 2005), and of ticks and ´ 1978; Korenberg et al., tick-borne diseases in particular (Rosicky, 1984; Steere, 1994; Dautel and Kahl, 1999; Wilamowski et al., 1999; Uspensky, 2008a). As new data accumulate on the occurrence of ticks and recognition of zoonoses in urban areas, there is an urgent need to create an effective, efficient, and environmentally safe system of protection for urban dwellers from tick attacks and bites and the attendant human and animal infections with tick-transmitted pathogens. To successfully accomplish this task, it is necessary to systematize our knowledge of the different aspects of tick occurrence in cities and towns and to understand the factors influencing their presence. The present review is an attempt to make a step in that direction.

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European cities and towns – trends of development and conditions for tick existence Europe is a multinational conglomerate of developed countries with mostly urban population formed more than a century ago. The level of urbanization in western Europe is currently about 75% with an expected annual growth of 0.3% per year from 2000 through 2015. Apparently, the urbanization level in Europe will stabilize at about 82% (GEO-3, 2002). The stabilization of the urbanization process has been a result of the tendency to increase the quality of urban life. Two main factors are of a vital importance for tick persistence: suitable environmental conditions and the availability of appropriate hosts. There are several trends in urban development of European towns influencing both of the above factors. A tendency to preserve green spaces inside cities is a positive aspect for both human life and tick existence. In many European towns, numerous green areas have been preserved for decades, such as urban forests, parks, wide boulevards, and old cemeteries, as well as large private properties in suburban areas. Urban forests are especially typical for northern Europe (Malmivaara et al., 2002; Straupe et al., 2012). In some capitals, historic green parks pass right through the central parts of the cities (e.g., in Stockholm, Berlin, Tallinn). The focus on environmental protection, ecologically-based standards of urban growth, and creation of residential districts at the border with natural localities create rather favorable conditions for the existence of tick populations. The process of urbanization has been followed by a sharp increase in urban pet populations (dogs, cats, some rodents, etc.), which is often followed by an increase in the numbers of stray (free-roaming) pets, mainly dogs and cats (Slater, 2001), which are excellent hosts of adult ticks. The massive immigration to Europe from Africa during the last decades created a new tendency, which may have a negative impact on the environment: Growth of densely populated and impoverished areas with numerous pests and private animals, which often penetrate close to the city center, has become typical of some large cities. This tendency appears to be rather disruptive for many European positive traditions including improvement of the urban environment (Asiegbu, 2010). Poverty and joblessness, together with enormous numbers of homeless people in some areas of large European cities [for example, in Paris in 2005, this number was close to 200,000 (UN-Habitat, 2006)] dramatically diminish the quality of life. Ironically, however, this tendency improves the conditions for tick persistence. The success of tick life in an urban area primarily depends on the size of a municipality and on its level of development. About 50% of the western European population live in small towns (up to 50,000 inhabitants) (GEO-3, 2002), where there are numerous and diverse green spaces. These green spaces support appropriate temperature and humidity conditions that are favorable for tick persistence, as well as for thriving host populations for all parasitic stages of ticks. Suburban areas in such towns do not dramatically differ from their central parts. Squirrels and hedgehogs, which are usually protected, are adequate hosts for adult ticks. A number of birds serve as hosts for immature tick stages. Various pets and rodents also support tick populations. Special attention should be paid to residential areas near large cities where people settle in natural environment. In these areas, animals are under protection, including numerous hosts of all parasitic stages of ticks, some of them being reservoirs of ticktransmitted pathogens. Some residential areas are really parts of suburban areas of large cities. Those located farther away often conglomerate into small towns that become satellites of large cities. An especially important trend is the increasing number of hosts of adult ticks, such as deer, lagomorphs, foxes, and raccoons, which

easily penetrate into urban areas and can dramatically amplify the tick populations. Thus, the urban environment creates a new reality for animal existence. Though the urbanization process is followed by impoverishment of biodiversity, suitable environmental conditions for ticks inside their geographic range mostly remain in suburban areas and may be found even in central parts of large cities. Let us consider different scenarios of tick occurrence in urban areas.

Ticks unusual for the proper area Ticks whose range is far from a given area can be occasionally brought into towns by tourists with their luggage or pets, with goods, in airplanes, etc. We described a Dermacentor variabilis female that attached to a woman in Jerusalem after she brought the tick in her luggage with clothes used in the USA (Uspensky et al., 1997; Wilamowski et al., 1999). Numerous other cases of importing exotic ticks to European cities and towns far away from their natural range were described (Jaenson et al., 1994; McGarry et al., 2001; Jameson and Medlock, 2009; Wilamowski et al., 1999). It is worth noting that an adult Amblyomma variegatum was found roaming a London bus coming from Heathrow airport (Y. Rechav, personal communication). A significant increase in pet tourism supports tick introduction into European countries from remote areas. In Germany in 1990, 31.1% of dogs were taken abroad, while in 1994 this number increased to 40.8% (Glaser and Gothe, 1998b). Apparently, this figure has continued to increase. The same phenomenon occurred in other European countries (Menn et al., 2010). The discontinuation of quarantine restrictions among some countries of the European Union resulted in at least a 10-fold increase in animal movement within Europe (Bellamy and Salmon, 1999). Some tick species brought home by pets may be rather exotic for the new sites. Thus, dogs returning to the U.K. were found to harbor the following species: Amblyomma americanum, D. variabilis, D. albipictus, and Ixodes pacificus from the U.S.A., and Haemaphysalis leachi from several African countries (Jameson et al., 2010). This scenario concerns introduction of individual exotic ticks, which might be of danger only to the person(s) directly involved, and cannot be followed by long-term survival and reproduction of the introduced ticks. The only exception is the brown dog tick Rhipicephalus sanguineus, which is considered below. Can migrating birds be a source of urban invasion by exotic ticks? In fact, a number of tick species regularly travel between countries and continents on migrating birds (Hoogstraal et al., 1961, 1963; Gusev, 1962). The migratory routes of birds are determined by various geomorphological formations, including the valleys of large rivers (Berthold, 1993). Many towns are located on the banks of such rivers and if the birds’ resting or breeding sites are located nearby, the penetration of ticks inside urban areas might take place through local migrations of birds. This scenario is not very common, since the season of tick activity in Europe coincides with the nesting period in birds’ life when their local migrations are minimal. However, local migrations can still assist ticks naturally inhabiting the area with penetrating into towns. Various types of human activities may influence long-distance tick transfer. This process began long ago when man first domesticated some mammals and birds. People moved over great distances with their animals, which mediated introduction of ticks parasitizing these animals into new areas. These movements determined the present ranges of many tick species (Hoogstraal, 1972). In some case, such transfer may be the starting point of tick dispersal over a large new territory including urban areas. Hyalomma marginatum was found on horses imported from Portugal to the U.K. (Jameson and Medlock, 2009). Horses imported from the U.S.A. to

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Norway and Germany were reported to be infested by D. albipictus (Lillehaug et al., 2002; Liebisch et al., 2006). International trade in exotic reptiles expanded steadily over the last decades increasing the chances of introduction of non-endemic ticks and the attendant pathogens. Ticks of the genera Amblyomma and Aponomma were found on imported reptiles in the U.K. and Poland (Pietzsch et al., 2006; Nowak, 2010). However, the most efficient way of tick dispersion is with cattle. The recent appearance of R. sanguineus in Hungary has been explained by the import of infested calves from Croatia, and infestation of farm dogs quickly followed this event (Hornok and Farkas, 2005). Thus, this scenario under some circumstances might be followed by the introduction of non-endemic ticks or tick-borne pathogens into new regions, including urban areas.

The urban areas as a new habitat for ticks inside their range The species of ticks that have naturally inhabited the locality of a town, and which continue to live in adjacent areas deserves much greater attention than the exotic ticks. The urban area is a complex system, which developed as a result of urban intervention into natural areas and agricultural lands to provide dwellings, services, and employment for growing numbers of urban inhabitants (Miller and Hobbs, 2002; Robinson, 2005). Forest clearing for agricultural purposes as well as major human encroachment into forested and uncultivated areas create opportunities for populations of local ixodid ticks to continue to flourish under urban and especially suburban conditions. It was recently suggested (using the model of Ixodes scapularis and Borrelia burgdorferi) that suburban sprawl leading to forest fragmentation might increase the proportion of ticks infected with human pathogens (LoGiudice et al., 2003). Contacts between wild and urban fauna are well established, especially in expanding cities. Some residential units in suburban areas are located immediately adjacent to woodlands. Rodents that migrate back and forth between human dwellings and nature bring immature ticks into houses. Stray dogs and cats are also good vehicles for transporting ticks from nature to towns. Transfer of immature ticks by birds from adjacent areas during post-nesting migrations is also widespread. Ticks inhabiting areas immediately outside the city may penetrate as far as the city center. Numerous and regular findings of I. ricinus were recorded in capitals and large cities of Germany, Czech Republic, Poland, and some other countries, and various human pathogens or their DNA were identified in these ticks (Kahl and Radda, 1988; Kahl et al., 1989; Daniel ˇ ´ and Cerny, 1990; Hubálek et al., 1993; Sinski and Rijpkema, 1997; ´ Dautel and Kahl, 1999; Stanczak et al., 2004; Maetzel et al., 2005). Antibodies to several human pathogens were detected in Florence residents exposed to tick bites (Ciceroni et al., 2003). Cases of Lyme borreliosis among urban park workers after bites by I. ricinus were documented in London (Rees and Axford, 1994). Unfortunately, reliable information on urban epidemiology of tick-borne infections remains rather scarce. It is also important to note such ticks as D. reticulatus, D. marginatus, and Haem. concinna in Europe, and I. persulcatus in Eurasia, which have been regularly found in urban and suburban areas over their entire ranges. All of these ticks may attack people and transmit a number of pathogens of medical importance. The expansion of the D. reticulatus range in central and western Europe (Sréter et al., 2005; Dautel et al., 2006; Bullová et al., 2009) during the last decades has increased the potential of this tick as an urban pest ´ 2011). (Biadun, The variety of tick species which can be detected in a given town increases if ticks are collected by different techniques. In central European cities and towns either I. ricinus alone or together with another exophilic species are discovered when ticks are only collected from vegetation. When this technique is supplemented

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by collecting ticks from mammals of various sizes and from birds, the number of tick species significantly increases (Table 1). Ticks found by such techniques, even if they do not attack people or do it rarely, may be of high epizootiological significance. Thus, the hedgehog tick, I. hexagonus, has been regularly encountered in European towns. This tick was proved to be a reservoir host for the tick-borne encephalitis virus (Radda, 1973). Since the European hedgehog Erinaceus europaeus was shown to be a reservoir host for Borrelia burgdorferi s.l. (Gray et al., 1994; Gern et al., 1997; Skuballa et al., 2012), this tick is involved in enzootic transmission cycle in urban areas. Besides, it was suggested that the hedgehog may be a reservoir host for Anaplasma phagocytophilum (Silaghi et al., 2012); it means that I. hexagonus may participate in the circulation of this pathogen, too. In addition to hedgehogs, I. hexagonus can also feed on badgers, martens, and foxes which are regular visitors to suburban areas, as well as on dogs and cats (Gern et al., 1997; Nijhof et al., 2007). The introduction or invasion of alien tick hosts into a new area can influence the abundance of ticks and lead to emergence of tickborne pathogens previously unknown in the area. In the 1960s, Siberian chipmunks (Tamias sibiricus) appeared in pet shops of several European countries, mainly in northern France and Belgium, and it became fashionable to keep these exotic animals as pets. It would have been worth knowing in advance of the introduction that the Siberian chipmunk is one of the main hosts of immature I. persulcatus (Labzin, 1985) and that a number of human pathogens were isolated from this rodent (Shekhanov, 1979). Some pet fanciers soon started getting rid of their chipmunks, while some rodents simply escaped from captivity. These animals found themselves not far from human dwelling, in urban parks and in urban and suburban forests. Today, a number of chipmunk populations are established in France, Belgium, Holland, Germany, Italy, Switzerland (Long, 2003; Chapuis, 2006). The rodents were recorded in urban parks of Rome (Bertolino et al., 2000; Benassi and Bertolino, 2011), Geneva (Long, 2003), Brussels (Allen, 2009), and in and around many other towns. The number of chipmunks in France is estimated at about 100,000 individuals, and their populations have being identified in 11 suburban forests and urban parks (Chapuis, 2005). These rodents recently appeared in Denmark and the U.K. (Chapuis, 2006). As could be expected, introduced chipmunks turned out to be good hosts for preadult I. ricinus (Vourc’h et al., 2007). Pisanu et al. (2010) showed that the introduced rodents are more heavily infested by I. ricinus than the native rodents, such as the wood mouse Apodemus sylvaticus and the bank vole Myodes glareolus. It was also found that the introduced rodent is a reservoir host for B. burgdorferi s.l. Importantly, the native rodents infested with I. ricinus are associated with only one genospecies of B. burgdorferi s.l., whereas the chipmunk is associated with 3 genospecies (Marsot et al., 2011).

Ticks that ‘enjoy’ living in towns Ticks living in nature are mostly three-host ticks needing different hosts of a different size at each parasitic stage. As a rule, they cannot starve for more than several months, nor can they live in man-made structures. This creates specific limitations to their existence in urban areas. Tick species especially adapted to life in urban areas are those that: (a) can use either urban pests (rodents, birds, stray animals) or domesticated animals (pets, poultry) as hosts; (b) can use one and the same host at all parasitic stages; (c) can survive starvation for a prolonged period of time; (d) can live in man-made buildings. Those that also have a high reproductive rate possess an additional advantage. There are representatives of both tick families

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Table 1 Results of tick collection by various techniques in European cities and towns. City/town

Techniques used

Tick species found (number of specimens)

Length of study, years

References

Prague Munich (and 4 other Bavarian towns) Kiev Budapest

Collection from vegetation Collection from vegetation

Ixodes ricinus (779) I. ricinus (13,403)

4 1–2

Baˇsta et al. (1999) Schorn et al. (2011)

Collection from dogs Collection from hedgehogs

2 2

Hamel et al. (2013) Földvári et al. (2011)

Kiev

Collection from vegetationa

Dermacentor reticulatus (33), I. ricinus (19) I. ricinus (4746), I. hexagonus (57), I. acuminatus (1), Hyalomma marginatum (1) I. ricinus (69%), D. reticulatus (28.5%), Haemaphysalis concinna (2.5%) I. ricinus (62%), I. apronophorus, I. trianguliceps, I. crenulatus, I. laguri, Haem. punctata, Haem. concinna, D. reticulatus, Rhipicephalus rossicus I. ricinus (36), I. lividus (6), Haem. concinna (2), I. arboricola (1) I. ricinus (77), D. reticulatus (76) I. ricinus (122), D. reticulatus (39), I. kaiseri (12)

12

Akimov and Nebogatkin (2002)

b

Collection from small mammals

Collection from birds Collection from cattle and goats Collection from dogs and cats a

12

2 1(?) 1(?)

There are no data in the paper on the number of tick specimens collected during the study. b There are data only on the proportion of I. ricinus among all tick species collected during the study.

(Argasidae and Ixodidae) that satisfy the above conditions necessary for thriving in urban areas. The European pigeon tick, Argas reflexus, is the most common inhabitant of urban areas in central and western Europe (Dautel et al., 1991; Dautel and Kahl, 1999), being closely tied to the main urban pest bird, the rock pigeon Columba livia also known as the ‘flying rat’. The capability of pigeons to perfectly cope with urban conditions allows them to dominate the urban environment, and their abundance in Europe alone is estimated at between 20 and 30 million birds (IUCN, 2012). In the sites where pigeons have lived for years, A. reflexus can develop large populations. The capacity of these ticks to fast for up to several years allows them to survive even when pigeons become unavailable. A. reflexus also feeds on other synanthropic nesting birds. Comprehensive taxonomic studies (Hoogstraal and Kohls, 1960a, 1960b; Theodor and Costa, 1960; Filippova, 1966) have shown that there are several species closely related to A. reflexus s.str. Argas polonicus collected from the church in the central square of Krakow (Siuda et al., 1979) was also found in churches of several towns of the former Czechoslovakia (Dusbábek, 1985). Argas vulgaris has been distributed in south-eastern Europe (Russia, Ukraine, Armenia) and in central Asia parasitizing synanthropic birds, including C. livia (Filippova, 1966). In Israel, another representative of the group, A. latus, was found in Jerusalem and several other towns (Filippova et al., 1999; Wilamowski et al., 1999). All the above species attack and bite humans inside their dwellings even in multi-story buildings, often provoking severe allergic responses. Among ixodid ticks, the brown dog tick (or kennel tick) R. sanguineus is, beyond doubt, the main urban tick pest. R. sanguineus meets practically all of the above-mentioned requirements for thriving in an urban environment. Having a very close affinity to dogs, this tick may inhabit kennels, yards, and the adjacent sites, including human dwellings (Uspensky and Ioffe-Uspensky, 2002; Dantas-Torres, 2010). Although many species of ticks may be brought into human dwellings, only R. sanguineus can initiate a local population there. This tick is a three-host species, but all parasitic stages can feed on one and the same dog. Moreover, adult ticks can change dog hosts during feeding (Little et al., 2007), and this behavioral trait can explain the findings of these ticks on dogs that never traveled to R. sanguineus endemic countries (Glaser and Gothe, 1998a). Under certain conditions adult and immature R. sanguineus can be very aggressive toward people, contrary to the widely held opinion that its affinity to humans is weak (Parola et al., 2008; Uspensky, 2009). A case of multiple tick attacks on a homeless man in Marseille followed by his infection with Mediterranean spotted fever (MSF) and subsequent death was described by Hemmersbach-Miller et al. (2004). Findings of R. sanguineus

inside houses and prolonged persistence of tick populations in human dwellings have been regularly reported (Garben et al., 1980; Hoffmann, 1981; Uspensky and Ioffe-Uspensky, 2002). This tick is of a great medical and veterinary significance being the vector and reservoir of many human and animal pathogens (Table 2). Analysis of over 100 cases of MSF in Jerusalem showed that 72% of the patients got infected in a home environment (Jacobson, 1982). The number of Rickettsia conorii-infected adult R. sanguineus detected in Marseille was found to positively correlate with the number of people hospitalized with MSF (Raoult et al., 1993). Human infections following bites by ticks from indoor colonies are well documented (Péter et al., 1984; De Sousa et al., 2007; Renvoisé et al., 2012). Introduction of the brown dog tick into new areas, especially of females of the species, has been followed in many cases by quick infestation of naïve dogs and establishment of local colonies of ticks (Sibomana et al., 1986; Loth, 2005). This explains frequent findings of this tick in human dwellings in the northern and southern countries, far beyond its natural geographic range (Garben et al., 1980; Hoffmann, 1981; Ruiz et al., 2003). Human protection from tick attacks under urban conditions The two main factors which influence the success of tick populations under urban conditions, defined above, determine the two main lines of attack against urban ticks. The first one is aimed at diminishing the populations of potential tick hosts in urban areas. Often this task may be accomplished without resorting to extreme measures against the animals. For example, in Basel (Switzerland), the population of pigeons was reduced in half simply by prohibiting people to feed the birds (Haag-Wackernagel, 1995). Thorough management of urban rodents and stray dogs and cats is of a great importance for controlling ixodid ticks, and there are effective technologies for such management (Singleton et al., 2003; Tasker, 2007; Rylnikov, 2011). Obstruction of favorite ways of migration of large wild animals into towns, e.g., by fences (Uspensky, 1999), might also have a positive effect. As the second line of attack, a reduction of tick populations may be accomplished by proper cultivation of urban parks and forests including regular removal of garbage and mowing of grass, especially near human paths (Romanenko, 2011). In addition to controlling urban tick populations, it is of utmost importance that urban inhabitants be adequately informed about the dangers of tick bites, the sites of possible tick attacks, and the basic self-protection techniques. It is necessary to emphasize that people on leisure, such as urban inhabitants spending time in parks and forests, pay little attention to notices on tick dangers (Uspensky, 1999); therefore

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Table 2 Some most important pathogens transmitted by Rhipicephalus sanguineus and diseases they provoke in Europe and adjacent areas (after Walker et al., 2000; Uspensky, 2008b). Pathogen

Target of infection

Disease

Known areas of infection in Europe

Rickettsia conorii conorii R. c. israelensis R. c. caspia R. massiliae Ehrlichia canis Anaplasma (Ehrlichia) platys Babesia vogeli Babesia gibsoni Hepatozoon canis

Humans

Mediterranean spotted fever Israeli spotted fever (tick typhus) Astrakhan spotted fever Spotted fever rickettsiosis Canine monocytic ehrlichiosis Canine anaplasmosis Canine babesiosis

Mediterranean area, Black Sea area Israel, Portugal, Sicily Caspian Sea northern area, Kosovo Mediterranean area Worldwide Southern Europe, Israel Worldwide Southern Europe (sporadically) Southern Europe

Dogs

such information should be repeatedly presented by various means, especially during the tick activity season. To effectively solve this problem, it is necessary to integrate and coordinate the efforts of specialists from different disciplines (from acarologists and veterinarians to mass media representatives) (Medlock and Jameson, 2010; Braks et al., 2011; Dantas-Torres et al., 2012). In this regard, one should welcome the recommendation by W.H.O. to include consideration of tick-borne diseases (and, thus, the conditions affecting tick populations) as an integral part of planning process when designing and developing new residential areas (Ginsberg and Faulde, 2008).

Additional comments concerning the problem While the possibility of tick occurrence in urban areas and the resulting threats to public health are recognized by specialists in the field, our understanding of the real scope and nature of the problem is far from sufficient. The relevant data are spread over a wide variety of sources, many of which present only a minimal amount of information pertaining to the specific issue of ticks or tick-borne pathogens in cities and towns. In some sources, it is unclear whether a tick attack on an urban dweller occurred inside or outside of the town, while others provide only indirect reference to tick occurrence. Often, ticks spotted in a town are mentioned in passing, usually without species identification, in a study directed at a different objective, such as detection of DNA of tick-transmitted pathogens in samples from human patients, animals, or ticks. At present, the main problem in studying urban ticks (as well as in acarological studies in general) is that of correct species identification. The number of practicing tick taxonomists has been going down in recent years, while the technology of molecular tick identification is not yet sufficiently mature. Not all molecular specialists dealing with tick identification are adequately informed about the rules of zoological nomenclature or the systematic positions of the taxa they work with. For example, there was an anecdotal case of a paper published in one of the much respected peer-reviewed parasitological journals where a gamasid mite was presented as an argasid tick. Many scientists and the journal editors fail to appreciate the significance of reporting the instances of tick detection and bites in urban areas. There is more concern with the hypothetical threat of ticks and tick-borne diseases in the future [e.g., an improbable suggestion of D. andersoni as the main candidate for invasion into Europe (Van der Weijden et al., 2007)], than with their real impact on public health today. A poignant example of the dichotomy between the available data and the reality concerns the brown dog tick in Finland. To my knowledge, there is only a single report on R. sanguineus findings in the country, when several ticks were found indoors in Tampere (Hackman, 1977). Meanwhile, from a brief note in the Helsinki Information Bulletin (Anonymous, 2007), it is apparent that the brown dog tick “has become more widespread in recent years”. The Bulletin further reports that “dozens of outbreaks of

Canine hepatozoonosis

brown dog tick have emerged in Finland this decade”. This means that even in developed European countries we are still far from knowing the true scale and complexity of the problem of urban ticks. Conclusion The attempt was made to outline different aspects of the problem of ticks in urban areas. It is clear that two groups of ticks are of major concern for modern towns: those living under natural conditions of urban surroundings and those well adapted to urban conditions. In Europe, I. ricinus is the main representative of the first group and R. sanguineus of the second group. There is a number of techniques for minimizing contacts of urban inhabitants with ticks. However, there is a gap between our recognition of the problem and the development of effective system of human protection. The establishment of database concerning all aspects of tick presence in a given municipality (sites of regular findings, ways of penetration, main hosts, etc.) is the first necessary step in narrowing this gap. Only a multidisciplinary approach to the problem can bring success in making European cities and towns reasonably safe from ticks and tick-borne diseases. Acknowledgements I am greatly indebted to Ilia Ouspenski for his excellent editorial assistance. I thank Fokko F.D. Ponsen for translation of a paper from Dutch. References Akimov, I.A., Nebogatkin, I.V., 2002. Ticks of Kiev – urbozoological and epizootiological aspects. Vest. Zoolog. 36, 91–95 (in Russian). Allen, P., 2009. Thousands of French chipmunks carrying potentially fatal diseases ready to invade Britain. Mail Online, July 23 (Available at: www.dailymail.co.uk/news/article-1201456). Anonymous, 2007. Brown dog tick spreading around Finland. Helsingin Sanomat, Intern. Edition, September. Asiegbu, M.F., 2010. African migrants in spite of ‘fortress’ Europe: an essay in philosophy of popular culture. African Journal Online, Available at: www.ajol.info/index.php/og/article/newfile/52332/40957 Baˇsta, J., Plch, J., Hulínská, D., Daniel, M., 1999. Incidence of Borrelia garinii and Borrelia afzelii in Ixodes ricinus ticks in an urban environment, Prague, Czech Republic, between 1995 and 1998. Eur. J. Clin. Microbiol. Infect. Dis. 18, 515–517. Bellamy, R., Salmon, R., 1999. Risk of importation of diseases exotic to Great Britain following the relaxation of quarantine regulations. Q. J. Med. 92, 683–687. Benassi, G., Bertolino, S., 2011. Distribution and activity of the introduced Tamias sibiricus (Laxmann, 1769) in an urban park in Rome, Italy. Mammalia 75, 87–90. Berthold, P., 1993. Bird Migration: A General Survey. Oxford University Press, New York. Bertolino, S., Currado, I., Mazzoglio, P.J., Amori, G., 2000. Native and alien squirrels in Italy. Hystrix (n.s.) 11, 65–74. ´ W., 2011. New habitats of Dermacentor reticulatus (Fabricius, 1794) in the Biadun, Lublin region. Polish J. Environ. Stud. 20, 263–266. Bradley, C.A., Altizer, S., 2007. Urbanization and the ecology of wildlife diseases. Trends Ecol. Evol. 22, 95–102. Braks, M., van der Giessen, J., Kretzschmar, M., van Pelt, W., Scholte, E.-J., Reusken, C., Zeller, H., van Bortel, W., Sprong, H., 2011. Towards an integrated approach

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