Ixodes trianguliceps Birula, 1895

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 trianguliceps Birula, 1895

Ixodes trianguliceps Birula, 1895: 358.

Ixodes nivalis Rondelli, 1928: 85; Pomerantsev 1950: 84.

Ixodes tenuirostris Neumann, 1901: 286.

Endopalpiger heroldi Schulze, 1939: 35; Černý 1959: 156.

Recorded hosts.

Mammalia: Alexandromys oeconomus (Pallas) (tundra vole), Apodemus agrarius (Pallas) (striped field mouse) (dominates as the host in the Udel’ny forest park in St. Petersburg, according to Tretyakov (2009), Apodemus flavicollis (yellow-necked field mouse), Apodemus sylvaticus (Linnaeus) (wood mouse), Apodemus uralensis Pallas (Ural field mouse), Arvicola amphibius (Linnaeus) (European water vole), Chionomys gud (Caucasian snow vole), Chionomys nivalis (European snow vole), Craseomys rufocanus (Sundevall) (grey red-backed vole), Cricetus cricetus (Linnaeus) (European hamster), Crocidura leucodon (Hermann) (bicolored shrew), Crocidura suaveolens (Pallas) (lesser white-toothed shrew), Eutamias sibiricus (Laxmann) (Siberian chipmunk), Lasiopodomys gregalis (Pallas) (narrow-headed vole), Lepus europaeus Pallas (European hare), Lepus timidus Linnaeus (mountain hare), Micromys minutus (Pallas) (harvest mouse), Microtus agrestris (Linnaeus) (short-tailed field vole), Microtus arvalis (Pallas) (common vole), Microtus majori (Thomas) (Major’s pine vole), Microtus socialis (Pallas) (social vole), Microtus subterraneus (de Selys-Longchamps) (European pine vole), Mus musculus Linnaeus (house mouse), Mustela nivalis Linnaeus (least weasel), Myodes glareolus (Schreber) (bank vole), Myodes rutilus (Pallas) (northern red-backed vole), Myopus schisticolor (Lilljeborg) (wood lemming), Neomys anomalus Cabrera (Mediterranean water shrew) ( Filippova 1977), Neomys fodiens (Pennant) (Eurasian water shrew) ( Lutta 1968), Nyctalus noctula (common noctule), Ochotona alpina (Pallas) (alpine pika), Prometheomys schaposchnikowi Satunin (long-clawed mole vole), Rattus norvegicus (Berkenhout) (brown rat), Sciurus vulgaris Linnaeus (red squirrel), Sicista betulina Pallas (northern birch mouse), Sorex araneus Linnaeus (common shrew), Sorex caecutiens Laxmann (Laxmann’s shrew), Sorex daphaenodon Thomas (Siberian large-toothed shrew) ( Filippova 1977), Sorex isodon Turov (taiga shrew) ( Sapegina 1980), Sorex minutus Linnaeus (Eurasian pygmy shrew), Sorex minutissimus Zimmermann (Eurasian least shrew) ( Filippova 1977), Sorex roboratus Hollister (flat-skulled shrew) ( Shtilmark 1963; Sapegina 1980), Spermophilus suslicus (Güldenstädt) (speckled ground squirrel), Vulpes vulpes (Linnaeus) (red fox) ( Filippova 1977).

Aves: Anthus trivialis (Linnaeus) (tree pipit), Carduelis carduelis (Linnaeus) (European goldfinch), Dendrocopos major (Linnaeus) (great spotted woodpecker), Emberiza citronella Linnaeus (yellowhammer), Nucifraga caryocatactes (Linnaeus) (Eurasian nutcracker), Strix uralensis Pallas (Ural owl), Turdus viscivorus Linnaeus (mistle thrush) ( Filippova 1977).

Reptilia: Zootoca vivipara (viviparous lizard) (Lichtenstein) ( Filippova 1977).

Recorded locations

(Fig. 5 ). Russia: North Karelia – Cape Kartesh ( Stanyukovich and Fedorov 2022); Karelia ( Lutta 1968) including the village Malaya Gomselga (southern Karelia) ( Bespyatova and Bugmyrin 2015; Bespyatova et al. 2019), St. Petersburg ( Tretyakov 2009), Leningrad Oblast ( Sukhomlinova 1977), Novgorod Oblast ( Grigoryeva and Tretyakov 1998), Pskov Oblast – the village Gogolevo (own data, unpublished), Kaliningrad Oblast, the Vistula Spit (own data, unpublished); Tver Oblast ( Schipanov and Makhanko 2018), Tula Oblast ( Kozlova et al. 2014), Perm Oblast ( Korenberg et al. 2015), Eastern Upper Volga ( Egorov et al. 2016), Krasnodar Krai and the Caucasus ( Shatas 1957; Filippova and Stekol’nikov 2007), Kurgan Oblast ( Starikov and Starikova 2021), Tyumen Oblast ( Bragina et al. 2013), Omsk Oblast ( Rar et al. 2014, 2020), Kemerovo Oblast ( Kovalevsky et al. 2018), Western Sayan ( Shtilmark 1963), Eastern Sayan ( Schluger 1961), Khamar-Daban ridge ( Vershinina 1988). Belarus ( Arzamasov 1963). Ukraine: Crimea ( Filippova 2010), Polesia ( Podobivskyi and Fedonyuk 2017). Moldova: north and central Moldova ( Uspenskaya et al. 2006). Georgia: the village Bakuriani and the Roki Tunnel ( Djaparidze 1960). Armenia: the whole territory ( Ogandzhanyan 1960). Azerbaijan: the south of the country ( Ogandzhanyan 1960).

Ecology and other information.

Ixodes trianguliceps Birula has a wide geographical distribution in the Palaearctic region, occurring from the coast of Lake Baikal to Western Europe ( Filippova 2010; Estrada-Peña et al. 2018). In the north it reaches northern Karelia and the Scandinavian Peninsula ( Fedorov and Leonovich 2021). Also, an isolated southern population of this species was found in the Crimean Peninsula ( Filippova 2010) although in other parts of Ukraine it is present in forest zones, such as Polesia ( Podobivskyi and Fedonyuk 2017).

The population that was supposed to be isolated in the mountain systems of the Caucasus ( Filippova 2010) now seems to be more expanded, as proved by the recent finding in Turkey (Bolu and Kars province, the north of Turkey) ( Keskin and Selçuk 2021). The Kars province is located near the border with Georgia, where this species was known before ( Djaparidze 1960) and, therefore, the ticks reported from there are probably part of the same Caucasian population.

The map of findings of this tick species in Russia clearly illustrates that it lives in a broad range of forest biotopes throughout a vast territory including the zonal and mountain deciduous and mixed forest of the European type and forests of southern and middle-taiga types. Along the southern border of the largest part of the range in Russia, I. trianguliceps occurs in the forest-steppe zone, populating shrubby and forested biotopes. This distinctly correlates with the main habitats of shrews and rodents, because the presence of these small mammals together with well-developed soil litter, plays an important role in the abundance of ticks in the landscape, as it is known that shrews of the genus Sorex are the most preferable host for larvae ( Randolph 1975).

Interestingly, I. triangulipeps was also reported from two bat species ( Myotis myotis in Poland ( Siuda et al. 2009) and Nyctalus noctula in Russia, as well as several bird species and one reptile species ( Filippova 1977). These animals are non-typical and occasional hosts for this tick species. The single cases of parasitism on these host species can be a clear indication that I. trianguliceps is predominantly an exophilic species, because it is unlikely that ticks could contact bats and birds in a burrow. Findings of this tick species in micropores of burrow tunnels in Belarus in winter ( Arzamasov 1963) demonstrate only the ability of its larvae to remain active even during winter.

Phylogenetic trees inferred from the concatenated nucleotide sequences of 10 protein-coding genes of the mitochondrial genome of I. trianguliceps , together with consideration of its morphology, justified to establish the new subgenus Filippoviella and include there I. trianguliceps together with aforementioned I. ghilarovi ( Apanaskevich et al. 2024) both of which used to belong to the subgenus Exopalpiger .

Figures

Figure 5. Map of Russia and neighboring countries showing the locations where Ixodes trianguliceps was reported.