The occurrence of the Dermacentor reticulatus tick –expansion to new areas and their possible reasons
Grzegorz Karbowiak
W.Stefanski Institute of Parasitology, PolishAcademy of Sciences
Twarda 51/55, 00-818 Warsaw, Poland
Abstract
Dermacentor reticulatus tick can be foundin temperatezones of Eurasia. Their area of occurrence is dividedinto two parts: west and east. Presently, D. reticulatus spread their area through the older free zone. The possible reasons for dividing the previous area into two parts is the climatic structure of Europe, for example the specific mean winter and summer temperatures. The region where D. reticulatus is absent is characterisedby mean winter temperatures between 0C and 5C and thin snow cover. The alternative hypothesis is the effect of human influence - liquidation of habitats of this tick and eradication of their hosts.
The present expansion can be the effect of climate changes. The mean temperatures in Europe increased, following the elongation of the vegetation season and positive trends of wet daysare observed. Consequently, northern Europe has become warmer and wetter over the last century.
Human activity can also influence the spreading of the ornate dog tick. The possible factors are the changes in agricultural land-use, environmental protection and spreading with international tourism and trade.In summary, the expansion of Dermacentor reticulatus tick into new areas could be the synergistic effect of many favourable factors.
Key words: Dermacentor reticulatus;
Introduction
In middle Europe,Dermacentor reticulatus is the second most important hard tick species after the common tick Ixodes ricinus, in respect to their number and impact on the economy.The most important hosts for adult ticks are wild and domestic ruminants, horses and dogs, whereas for larvae and nymphs, this is rodents and insectivores. Humansare very seldom attacked by this tick. First-hand consequences of feeding are damage to skin and stress; in addition, the D. reticulatus tick is the main vector of Babesia canis and other piroplasms species, and is also able to transmit tularaemia, rickettsioses and other pathogens. Due to, this tick has the great epidemiological importance in Europe.
1. The preferred habitats of D.reticulatus tick
D.reticulatusoccurs in mild, damp open areas that are weakly covered by trees and bushes. It favours natural deciduous forests placed near water bodies or large stagnant waters. Therefore, it is most common in the wet forest associated with river valleys and ravine systems, lake shores and meadows near the forests borders. Typical biotopes are swampy mixed woods, meadows and shrub pasture communities. The most important factor for their occurrence is the high level of ground water, along with the drying up of soil [1, 2, 3]. Inthe area of the former Soviet Union, it also occurs in typical marshes [4, 5].
Data about the vertical distribution of this tick are pure. It seems to be strongly associated with lowland regions. Široký et al. [6] reported the biggest population of ticks in localities situated at altitudesat177 m above sea level and only single locations above 200 m a.s.l.
The characteristic feature of D. reticulatus is the ability of adaptation to different habitats, whilst under continuous human influence and fairly anthropogenic environments [7, 8, 9]. Széll et al. [10] consider this tick to be anthropophilic. As a result, their occurrence is not limited to natural plant communities, but with Ixodes ricinus and Haemaphysalis concinna, it is spread in urban areas. In towns and urban agglomerations, it inhabits recreational areas, featuring afforestation and/or conglomerates of bushy vegetation. In the parks, these are areas that have been created from natural meadows and forests, with parts of primeval herbage. Due to the small number of regular observations, it is difficultto determine a general principle of the occurrence and activity of ticks under urban conditions. The gathering of ticks is mainly conducted for epidemiological purposes, and authors seldom note the ecological data, such as the type of plant communities, the time of the study and the meteorological conditions. Littleindirect information is available in veterinary clinics where dogs infected with babesiosis have been cured.
2. The occurrence area of D.reticulatusin the last decade of 20th Century
The D.reticulatus tick is found in the western Palaearctic region, in a temperate forest climate zone of Eurasia, from England and Francein the west to the basin of Yenisei River in Siberiain the East. The northern border of their range runs along the 56-57° N geographical latitude, while the commonly sustained southern border is 50° N geographical latitude [3, 11]; however, there are documented populations from Portugal, located in 39 and 50° N [12]and in Romania and Hungary between 50 and 46° N [13, 14, 15]. According toImmler [2], the D. reticulatus tick occurrence area is limited to regions with 400 to 1000 mm of spring precipitation and a summer isotherm of 20-22C. However, a wider occurrence area in the past is possible. Within the geographic range, D. reticulatus is distributed in a highly focal pattern, whichis associated with their habitat needs [16].Their occurrence area is characterisedby phenomena that are not observed in other tick species and are generally rare in nature. Namely, it is divided into two separate parts –Western Europe and Eastern Europe[2,11, 17]. The western region covers the populations occurringfrom France to eastern Germany. InFrance D. reticulatus ticks were recorded in the highland of southern Jura, in the RhoneValley, NorthernFrench Alps [18] and Ardenes [19, 20]. In Germany,D.reticulatus tick populations were found in Taurus Mountains, Schwarzwald and Bayern [1], to Leipzig on the East[21]. The single, isolated foci of D. reticulatus ticksis recorded in Holland[22], south-western England [2] and Portugal[23].
There are some populations in Austria, the CzechRepublicand western Slovakia; however, they can be regarded as single foci. Hubalek et al. [24] described the populations occurring in northern Austria, which are associated with the population in the CzechRepublicand western Slovakia. These ticks are present in southern Moravia and Danuba rivers-basin and regions along the southern Slovakian border between Bratislava and Komarno[25, 26, 27].
In the area of the Eastern range of the occurrence, the D. reticulatus tick is common from eastern parts of Poland, across Belarus and the European part of Russia to the Central Siberian Plateau. In Russia,large populationswere noted in the Smolensk and Moscowdistricts[28,29]. In the St. Petersburgdistrict(59º N),where the northern border of the occurrence exists, this tick is relatively rare [30].
The northern border of the occurrence area run across the districts of Moscow, Ivanovsky, Ryazan, Svierdlovsk, Tyumentsevsky, Omsk, Novosibirsk and Kansk to the Khemerovsky district[31,32].To the East, the range of this tick reaches theKrasnoyarsk region. In the Asiatic part of Russia, a number of populations are present across Northern Caucasus and eastern South Caucasus. The strong populations were noted in southern parts of Omsk and Nowosibirsk districts and in Altai, where the D. reticulatus tick forms sympatric populations with D. marginatus[33, 34]. The southern border of the East occurrence area of D.reticulatustick in Europe involves the CrimeanMountains, Northern Caucasus, eastern Kazakhstan, and western Altai [1].
It is difficult to establish the eastern border of the D. reticulatus range, because it is not possible to determine whether the records from Siberia regard this species, or are determinations of other, morphologically similar species from the Dermacentor genus.
In Belarus,the D. reticulatus tick is the most numerous in Polesie and its range reachesVilnius, where the biggest populations are recorded in the Gomel district.The smaller populations occur in the Minsk district[35, 36, 37]. These populations are conjoinedwith Polish populations in Podlasie and these ranges should in fact be considered as one.
In the Ukraine,the D.reticulatus tick is noted in the central part of the country, among other regions of Kiev, inDnieper River Lowland and in SamaraRiver basin[4, 38].
The populations in the eastern part of Slovakia belong to the Eastern occurrence area of D. reticulatus. The foci are placed along the southern and eastern country border, in the midcourse of the LatoricaRiver. In Romaniaand Hungary,this tick is quite common in northern provinces and relatively rare in other parts of the countries [15, 39].
There is a region where the D. reticulatus tick is absent in the middle of Europe. This area is approximately triangular in shape. The northern edge runs along the Baltic Sea coast, with the arms extended fromcentralGermany and western Poland, between 12-13 and 19 meridian of the eastern longitude; the arms of the triangle coincide, reaching the southern border of Hungary[8, 40].
3. The changes in the occurrence range of D. reticulatus tick
The occurrence area of D.reticulatus tick described above was relatively stable from the first species descriptions until the 1970s and 1980s. Since the last decade of the previous century, it has appeared in new localities, where it was previously absent.
The first comprehensive study of the occurrence area in Polandwas made by Lachmajer in 1963 [41] and later completed by Szymański (1986) [42] and Siuda in 1993-1995 [3, 11]. The picture of the occurrence area presented by these authors was the basisfor every elaboration concerningthis tick species, which appearedfrom the last years of the 20th century to the beginning ofthe 21st century. According to their data, in Poland, this tick occurred in the north-eastern parts of the country, in Podlasie, AugustowskaForest, KnyszyńskaForest, in the BiebrzaRiverValley, PiskaForest and Lublin Polesie. This occurrence area is presented inFig. 1. Siuda [11] and Siuda et al. [17] collected 10 documented foci, which were the borders of the Eastern occurrence area, which included regions on the east of the Vistula and San rivers. According to the new study and reports, it should be considered the single, contiguous area connected with the main, so-called Russian occurrence area [43], and the reports of the new foci have epidemiological importance only, because no foci are separated in the fact.
From the 1990s, in Poland, the expansion of this tick species to the westwas observed. Among others, the appearance of new localities of this tick were recorded in northern Poland, in Pomeranian province, Kashube and in Tuchola Woods [44, 45], in the central regions in KampinosForest near Warsaw, as well as in the borders of Warsaw agglomeration [7,9, 40]. In the south of the country, in Niepołomice, this tick was transferred from BiałowieżaPrimevalForest with European bisons [46]. Recently, the newly documented foci have been observed in the south-western part of Poland in Lower Silesia since 2009, when the first evidence was noted in the BolesławiecCounty[47, 48] and in LubuskieProvince [49].
The expansion of D.reticulatus tick to the new, previously free areas has been observed in all of the middle and northern parts of Europe (Fig. 2). Until the late 1970s, this tick was relatively rare in Germany[2]. In the 1980s, it remained more common in the western part of the country and still rare in eastern lands – there were three populations in present in the Leipzig district. In the last decade of the 20thcentury there were found some foci in eastern Germany in Düben-Dahlen and Annaburg, which were considered endemic [50]. D.reticulatusremains numerous in Saxony, Saxony-Anhalt, Brandenburg, and the previously small populations in Hessen and Bayern have recently enlarged [51].
A similar situation concerns the CzechRepublicand Slovakia. Until the 1980s, this tick was rarely found, and the foci were documented around Bratislava, along the Danube and Bodrog rivers, and near the Ukraine border[27]. In the last decade, many new localities have appeared; however, as they were distinct toPoland, the main expansion direction was from the west to the east, into the East Slovakian Upland. Simultaneously, the tick species in the Danube valley has spread to the west, and has come into contact with the D. reticulatus ticks from West-European and Eastern occurrence areas[52]. Apart from this, the expansion to the northhas been observed; the northern range border in Slovakia reaches Michalovce, Trebišov and Košice towns [53]. In the CzechRepublic, the distribution range of D.reticulatus has not increased to such a degree as in Poland and Slovakia and is present along the main rivers usually; however, there is evidenceof their increased abundance [6]. In Hungary, there were two, separate foci of this tick in the 1950s, and until the 1970s this tick was seldomfound. In recent decades, the expansion of this species was observed and it presently occurs in the whole country; moreover, it is more numerous [54]. The most numerous populations are recorded in north-western and south-western parts of the country[13, 14, 15, 55].
The occurrence of new areas in eastern Germany (from 20006), western Poland (from 2010) and the CzechRepublic(from 2010) are correlated in time –the expansion of the whole west-European population to the Eastis evident.
Recently, new populations of D. reticulatus ticks have been recorded in Belgium, confirming the geographical expansion in North-western Europe[56].
4. The possible sources of the separated occurrence ranges presence.
The reasons for the presence of two separate occurrence areas of D. reticulatus tick until the end of the 20th century end, as well as their present fusion, are not known. The hypotheses usually concern the environmental and climatic conditions; however, the human activity impact is also possible.
There is no geographic barrier between natural forest and meadow ecosystems in the Palaearctic zone along the lane from France to Ural between 50 and 55 northern latitudes. For this reason, human activities may be the factors that are accountable for the absence of this tick in the middle of Europe. Such factors can be melioration and the eradication of streamlets, as well as the decrease in the tick’s host ranges. Apart from the natural habitats, ticks lose their hosts. Elk (Alces alces), the most important host for adult ticks, was completely eradicated from the bigger part of Europe, and deer and wild boars remain rare [27].However, this assumption is not indemonstrable; intensive human activity has played a role in the bigger part of D. reticulatus’ range and didnot cause their elimination. Moreover, it is not possible to establish the moment of the potential retirement of the D. reticulatus tick from the areas of eastern Germany, western Poland and Slovakia, and which factors influence this, because the first study on their occurrence dates from the second part of the 19th century [57].
Although there are no geographic barriers, the division of D. reticulatus’range ties in with the climatic structure of Europe. On the Polish territory, the transitional area between oceanic and continental climatesis located. In this area, the moist air masses ingoing from the Atlanticare met with dry air masses of the continental derive [58]. This fact influences the vegetable cover and associated animals. Consequently, in Poland,there is a transitional zone between plant communities and fauna typical for oceanic climate, represented by deciduous forests and the communities occurredin coniferous forests, typical for continental climate. Through the centre of Poland run range borders of the number of species of animals and plants. It is estimated that 52% of species occurring in Polandhavethe transitional character, which means they are spread both in the West and East; the rest of the species living in this country are at the western or eastern borders of the occurrence [59].
These potential reasons are insufficient to explain the divided area of occurrence of the D. reticulatus tick, because the border of their eastern occurrence arealies in the Polish territory, and it also occurs in Western Europe.
Another potential source of the divided occurrence area can be associated with the D. reticulatus biology and changeable climatic influence. This tick occursin open areas; the fluctuationsin the weather in temperate zones cause largevariations intemperature, humidity and insulation levels. The sum of soil surface temperatures limits the oviposition and egg development, and with both the required humidity and susceptibility of larvae and nymphs to theunfavourable factors, this restricts the reproductive period to one or two months [16]. This character of the D.reticulatus tick shows the dependence of their occurrence or local absence with indigenous climatic conditions. It is possible to associate the dividedoccurrence area with the presence of five climatic regions of Europe established by Smolec [60]. The regions are variable, in accordance to the season; therefore, separate regions have been established for the whole year, for cold seasons and for the vegetable season. It is evident that the area of absence of D.reticulatus in eastern Germany and western Poland ties in with the C region for the cold season. It is a region with warm temperatures, with the mean January temperaturebeing 0C, with a range from -5 to +5C. The eastern part of Poland belongs to the D region, which is fairly cool.
The thermal conditions have the greatest influence on the overwintering ability of many invertebrates, among them, ticks. Less is known about the influence of low temperatures on various aspects of ticks’ biology; however, many authors suggest that ticks are not freeze tolerant. Dautel and Knülle [61] estimated the supercooling points of European tick species to be between -17 and -23ºC, which is the same for D. reticulatus tick; such low temperatures limit survival. Ticks spend the winter behind in the litter, coversand other safe places of the soil surface. The soil surface temperature depends on the insulationas well as from the snow cover thickness. The snow cover forms the thermal conditions of the ground, and their heat-insulating attributes, among them the small thermal conductivity, protect small overwintering organisms (animals and plants) from the frozen habitat. On frozen days, the soil can be frozen to the high deepness,wherethere is no or thin snow cover; however, when the snow cover has a thickness of 9 cm, the frozenness occurs to 12 cm,in the thickness of 26 cm to 0.5 cm only [62]. The next important factor is the number of days with thick snow cover. The moment of snow cover disappearance modulates the moment at which the temperature rises above 0°C, through the loss of heat to the process of snow melting and sublimation. These processes move the beginning of the growing season as well as dates of severalphonological appearances of plants [63] and also periods of animal activities,dependent on the vegetation.