Ixodes persulcatus Schulze, 1930

Fedorov, Denis & Hornok, Sándor, 2024, Checklist of hosts, illustrated geographical range, and ecology of tick species from the genus Ixodes (Acari, Ixodidae) in Russia and other post-Soviet countries, ZooKeys 1201, pp. 255-343 : 255-343

Ixodes persulcatus Schulze, 1930

Ixodes persulcatus Schulze, 1930: 294.

Ixodes ricinus miyazakiensis Kishida: Morel and Pérez 1978: 201.

Ixodes persulcatus diversipalpis Schulze, 1930: 294; Pomerantsev 1950: 43.

Ixodes persulcatus cornuatus Olenev: Pomerantsev 1950: 43.

Ixodes sachalinensis Filippova: Kolonin 1981: 49.

Recorded hosts.

The spectrum of hosts of I. persulcatus is extremely broad both systematically and ecologically and includes more than 200 species of mammals and 100 species of birds ( Shilova and Clabovskii 1968). Rarely it can parasitize reptiles – lizards of the family Lacertidae ( Ravkin 1969) . Literally almost all mammals and birds inhabiting various types of forests and their derivative biotopes can act as hosts for I. persulcatus . Larvae and nymphs parasitize more often small and medium-sized mammals, such as shrews, hedgehogs, rodents, and lagomorphs, as well as ground-feeding and ground-nesting birds. Adults usually feed on large and medium-sized mammals – ungulates, carnivores, lagomorphs. Humans and domestic animals can also be hosts for this tick species ( Filippova 1977).

Distribution in Russia and other post-Soviet countries

(Fig. 14 ). The range of I. persulcatus , like no other Palearctic species, is extended in the latitudinal direction by a continuous strip, covering a significant part of the taiga forest zone in Eurasia between 21 ° – 66 ° latitude in the northern hemisphere from the Scandinavian Peninsula, the Baltic states, Belarus and Ukraine in the west where it is present sporadically to the east up to the Pacific coast including the Kamchatka Peninsula and the Sakhalin Island and further to the north-east of China, the Korean Peninsula and Japan ( Filippova 1977; Wang et al. 2023). This tick belongs to the tick fauna of the next post-Soviet countries: Estonia, Latvia, Lithuania, Belarus, Russia, Ukraine, Kazakhstan, Kyrgyzstan ( Guglielmone et al. 2023). The presence of I. persulcatus in Ukraine outside the south-west border of the taiga was mentioned by Filippova (1977), although the possibility of permanent populations existing there was disputed by Nebogatkin (1993). Therefore, this probably exemplifies transportation by migratory birds.

Ecology and other information.

Ixodes persulcatus is an exophilic tick species widely distributed in the northern Palearctic along the forest zone. It may use almost all mammals and birds living in its biotopes; therefore, it is one of the most important vectors of a broad range of tick-borne pathogens. Since it can also transmit tick-borne encephalitis virus, together with I. ricinus it has the greatest medical and veterinary significance among other ticks of the genus Ixodes in the Palearctic. Another important fact is that I. persulcatus is a very aggressive species toward humans ( Uspensky 1993) and, therefore, this species represents especially high medical-epidemiological risks.

The most significant part of the range of I. persulcatus stretches across the territory of Russia where we can observe the full spectrum of biotopes where I. persulcatus can be found. There are a lot of published works about its ecology in different regions which depend on the climatic region and biotic-abiotic conditions in it.

This tick prefers various types of forest and forest-steppe biotopes, especially taiga forests and their derivatives, i. e., mixed forests and bushes (both plain and mountainous), up to 2000 m a. s. l., like in the Tian Shan. In other words, it can inhabit any herbaceous forest and forest-steppe biotope with the level of humidity high enough for reproduction and supporting the life cycle, even in urban landscapes ( Filippova 1977). In the Dzungarian Alatau there were some observations of occurring in steppe regions bordering forests and parasitizing the unusual host, namely the grey marmot Marmota baibacina Kastschenko ( Bibikov et al. 1961) . Permanent and stable populations of I. persulcatus exist in some areas adjacent to cities within its range and even inside these cities on condition that the the suitable forest environment together with hosts, such as wild animals of different sizes and stray dogs are present. Examples of such cities are Saint Petersburg, Petrozavodsk, Novosibirsk, Tomsk, Irkutsk, and Vladivostok ( Uspensky 2017).

Several studies attest the changing boundaries of the ranges of I. persulcatus . It is assumed that ticks of the I. presulcatus group appeared and evolved in forest biotopes similar to modern relict forests of the Ussuri type and the taiga of the mountains of Southern Primorye, Southern Siberia, and the Korean Peninsula in the Pliocene. The wide ecological niche of I. persulcatus was formed during the formation of the species in the process of its adaptation to various landscape and climatic conditions. This allowed the species to gradually expand its range in the northwestern direction in the Holocene ( Filippova 2017). An increase in air temperature by one or several degrees in a particular region near the boundaries of its range was probably the main driver of its expanding distribution. The fact of finding I. presulcatus populations in Sweden ( Jaenson et al. 2016) and even in the Magadan Oblast in the north-east of Russia where it was absent before ( Yamborko et al. 2015) are good examples of the distribution expansion in several directions and confirm the tendency which continues.

In Russia, high numbers of observations show noticeable changes in the distribution of I. persulcatus in certain regions. In Karelia the range expansion of I. persulcatus to the north is noted in relation to general climate warming ( Bugmyrin et al. 2013). A similar observation was also recorded in the Komi Republic ( Glushakova et al. 2011). The range expansion of this tick species in Arkhangelsk Oblast and Western and Central Siberia to the north is confirmed both by the results of their records and by the data on tick bites and morbidity in the human population, not only in places which were free from ticks before ( Pogodina 2021). Besides that, there are some data about the range expansion of I. persulcatus to the north in the Republic of Sakha (Yakutia). The reasons causing these changes are under evaluation but climate change, anthropogenic pressure in natural landscapes as well as the number of vertebrate animals are among the most influential factors. At the same time, it is also possible that inadvertent dispersal of ticks by timber material transported from tick-infested areas may be in part responsible for this phenomenon ( Danchinova et al. 2006). Although other factors are not excluded, it is believed that climate changes have made the greatest contribution to the increase in areas primarily for TBE foci in the northern regions of the country. But despite all this, as a result of the same changes, the southwestern part of the range of I. persulcatus in Belarus and the Baltic countries has decreased ( Pogodina 2021).

Often it can be found in the same biotopes together with I. ricinus in Europe and I. pavlovskyi in Siberia with complete or partial coincidence of the seasonal activity of these species at each ontogenetic stage ( Ushakova and Filippova 1968; Bolotin et al. 1977; Filippova 1999). In zones of sympatry their hybridization can occur, and their hybrids can also transmit tick-borne encephalitis virus and probably other pathogens ( Kovalev et al. 2015; Rar et al. 2019; Belova et al. 2023). Under laboratory conditions, interspecific hybridization between I. ricinus and I. persulcatus was successfully conducted as well. F 1 hybrid ticks were completely sterile, as revealed by unsuccessful attempts of their subsequent hybridization with ticks of the parent generation ( Balashov et al. 1998). In I. persulcatus and I. ricinus , any morphological barrier to crossing is undoubdetly absent and then sterility of the F 1 hybrid generation is probably a quite significant factor limiting the population size of both species in their sympatric areas. Hybrid ticks also have morphological features allowing to differentiate them at preimaginal and imaginal stages ( Bugmyrin et al. 2015, 2016). Moreover, some studies were conducted in the Southern Primorye ( Filippova 2002) in sympatric zones of I. persulcatus and I. pavlovskyi occidentalis , due to the close cohabitation of both species. These showed that in case of these two species there are distinct morphological barriers which are manifested in the fitting of organs involved in mating, in particular their size proportions. According to the result of the studies, mating and hybridization of different tick species are possible only in the next combination: female I. pavlovskyi and male I. persulcatus . Whereas in case of the reverse combination, the parameters of the genital aperture of the female exceed those of the largest width of the hypostome in the male.

There is an excellent summary on the questing behavior of I. persulcatus in the monograph by Filippova (1985). In brief, the ticks climb onto the vegetation in quest of a host. When the host approaches, the tick spreads its first pair of legs and, upon contact with the host, become attached. From time to time, ticks perform vertical migrations and go even into the soil litter for rehydration. Horizontal movements of ticks towards trails used by potential hosts are also possible, as well as crawling onto a nearby animal. Ticks react to humans by spreading their first legs from distances of ~ 15– 20 m. At short distances, ticks also react to a heat source. In general, a similar pattern of questing behavior is used by other exophilic ticks of the genus Ixodes .

In I. persulcatus there is an important signaling mechanism causing a morphogenetic diapause – a developmental delay which is the response of ticks to the duration of the diurnal photoperiod ( Belozerov 1976). Moreover, I. persulcatus has a behavioral diapause of non-engorged adult ticks, which is not connected with photoperiodic regulation ( Korenberg et al. 2021). But as the studies in the Kirov Oblast and Udmurt Republic showed, in more warmer areas, an increased proportion of engorged larvae and nymphs develop without the diapause and the reason for this is the early activation and, as a result, their mass feeding on hosts in the first half of summer. The factors determining the diapause of engorged larvae and nymphs in the compared regions practically do not differ ( Korotkov 2008). The correlation of the tick number varies, depending on the type of biotope, as well as temperature and humidity and also many other abiotic factors. For example, in boreal taiga forests of Karelia mainly I. persulcatus dominates (except the southwestern part where the mass species is I. ricinus ) ( Bugmyrin et al. 2013). The beginning of adult I. persulcatus activity also differs in different regions depending on the sum of abiotic factors listed above. For example, in the Far East the seasonal peak in the number of larvae is observed in the third decade of May – second decade of July, whereas in the European part of its range in the third decade of July ( Belozerov 1976; Filippova 1977; Balashov 1998; Korenberg et al. 2013). In the territory from the Volga River to Primorye the average activity of adult ticks varies from 60 to 140 days ( Korenberg et al. 1974). The boundaries of the range of the tick are determined mainly by the combination of photo- and hygrothermal factors. The general indicators of warmth and moisture along the range of this tick species vary widely. The fundamental ecological niche of I. persulcatus with the broad scope of its preferred conditions allows it to adapt to the wide diversity of biotopes in the forest zone.

Some type specimens of I. persulcatus are deposited at the Zoological Institute of the Russian Academy of Sciences and include I. persulcatus subsp. diversipalpis ( Schulze 1930: 300) , lectotype: male; [ Russia, Primorskii Terr.], lower Amur River, 8 km of Vyatskoe Vill., 26. VI. 1910, coll. Soldatov, det. N. О. Olenev: I. ricinus ovatus ; AL I 266, as well as the paralectotypes: 1 female, 1 male; AL I 266 a. I. persulcatus (see: Filippova 1969: 677). Description – Filippova 1977: 316–327 (female, male, nymph, larva) ( Filippova 2008). But Filippova (1969) also states that re-examination of the type material of the above subspecies demonstrated that the specimens used for describing differences of this subspecies are damaged in some morphologically important parts (not noticed before), and the key morphological characters that were previously thought to distinguish the subspecies are not specific enough and can be found in ticks throughout their entire geographical range.

Figures

Figure 14. Map of Russia and neighboring countries showing the locations where Ixodes persulcatus was reported.