ISSN 0013-8738, Entomological Review, 2015, Vol. 95, No. 5, pp. 681–686. © Pleiades Publishing, Inc., 2015. Original Russian Text © M.V. Orlova, A.V. Zhigalin, A.M. Khritankov, 2015, published in Parazitologiya, 2015, Vol. 49, No. 2, pp. 119–127.

New Findings of Ectoparasites of (Chiroptera: ) in Southern M. V. Orlovaa, A. V. Zhigalina, and A. M. Khritankovb aNational Research Tomsk State University, Tomsk, 634050 Russia bErgaki Nature Park, Ermakovskoe, Krasnoyarsk Territory, Russia e-mail: [email protected] Received August 1, 2014

Abstract – Data on new findings of ectoparasites (mites and insects) of bats (Chiroptera: Vespertilionidae) in the Western Sayan and Tuva are presented. The fly Basilia mongolensis mongolensis Theodor, 1966 is reported for the first time from the territory of Russia. The gamasid mite Spinturnix bregetovae Stanyukovich, 1995 is new to the region. New hosts are described for some ectoparasites. DOI: 10.1134/S0013873815050127

Southern Siberia embraces the territory of the Altai- MATERIALS AND METHODS Sayan mountain country and is characterized by a high Bats were collected in the summer seasons of 2007– diversity of climatic conditions which are mostly de- 2013, in the southeast of Tuva Republic and the south termined by the terrain: from the dry steppe subzone in of Krasnoyarsk Territory (Table 1). Ten individuals of depressions to the mountain taiga belt in the low and bats were examined in hard-to-reach areas of the re- middle mountains (Vinogradov, 2012). gion: 5 ind. of the eastern water bat Myotis petax Hol- The bats are represented in the South Siberian fauna lister, 1912, 4 ind. of David’s myotis M. davidii Pe- by at least 13 species from 5 genera of the only family ters, 1869, and 1 ind. of the northern bat Eptesicus Vespertilionidae. The ectoparasites of bats remain nilssonii (Keyserling, Blasius, 1839); 126 ind. of para- little studied, data on them being fragmentary and sitic arthropods (mites and insects) were collected from these bats. scattered. Earlier, 17 species of bat ectoparasites, in- cluding 11 species of gamasid mites and 6 species of The ectoparasites were collected by a standard insects, were described by other authors for Kras- method, i.e., removed using tweezers and preparatory noyarsk Territory; the published data on Tuva were needles and fixed in 70% ethanol. The mites were absent. Our research in the territories of Tuva and the mounted on slides in Faure-Berlese liquid (Bregetova, south of Krasnoyarsk Territory confirmed the presence 1956) and examined under the Nikon Eclipse 50i and of 9 species previously known from Southern Siberia MBS-10 light microscopes. The collected mites, flies, (Stanyukovich, 1997; Orlova, 2014). and fleas were identified using the available keys (Theodor, 1967; Medvedev, 1985; Stanyukovich, As the result of new field studies in Southern Sibe- 1997; Lehr, 1999). ria (Table 1) we confirmed once more the presence of The ranges are described in accordance with the 9 species (Table 2), including several rare and little terminology of Gorodkov (1984). studied ones, and described new hosts for some of them. The bat fly Basilia m. mongolensis Theodor, The Bats of Southern Siberia and the Eastern 1966 was recorded for the first time in the territory of Palaearctic Russia. The gamasid mite Spinturnix bregetovae To-date, 13 bat species of the family Vespertilioni- Stanyukovich, 1995 was found for the first time in dae are known in the temperate zone of the Eastern Southern Siberia. Palaearctic. Earlier, there was an opinion that only Information on the new and little studied ecto- 6 of them had exclusively Eastern Palaearctic ranges: parasites of the Eastern Palaearctic bats is given Hilgendorf’s tube-nosed bat Murina hilgendorfi Pe- below. ters, 1880, the Ussuri tube-nosed bat Murina ussurien-

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Table 1. Collection sites of bat ectoparasites in Tuva Republic and southern Krasnoyarsk Territory Capture dates, host Geographic No. Collection site Landscape species, and number coordinates of ind. collected Tuva Republic 1 Sush River valley 52°04'N; 94°03'E Gallery forest in the steppe zone VIII.2013 Myotis petax (1) 2 Uyuk River valley 52°02'N; 94°10'E Gallery forest in the steppe zone VIII.2013 Myotis petax (2) 3 Lake Tere-Khol area 50°39'N; 93°01'E Steppe zone VII.2007 Myotis petax (2) Krasnoyarsk Territory Sayano-Shushensky National Biosphere Reserve 4 Maly Shugur and Urbun 51°48'N; 92°08'E Gallery forest in low mountain steppe VII.2012 River valleys Myotis davidii (3) 5 Khem-Terektik 51°54'N; 91°58'E Boundary between low mountain steppe VII.2012 River valley and taiga Myotis davidii (1) Ermakovsky District 6 Env. of Raz’’ezzhee 53°07'N; 92°29'E Mixed forest VII.2011 Eptesicus nilssonii (1)

sis Ognev, 1913, the Asian parti-colored bat Vesper- M. nipalensis (Dobson, 1871) (Benda and Tsytsulina, tilio sinensis Peters, 1880, the eastern long-fingered 2000; Matveev et al., 2005; Spitzenberger et al., 2006; bat Myotis macrodactylus (Temminck, 1840), the fra- Kruskop et al., 2012). ternal myotis Myotis frater G. Allen, 1823, and Ikon- Thus, the boreal Siberian-Far Eastern faunistic nikov’s myotis Myotis ikonnikovi Ognev, 1912. How- complex presently comprises 10 species of bats, in- ever, the list of Siberian-Far Eastern bats was recently cluding the most common and widely distributed spe- supplemented with new cryptic species separated from cies which form the core of the bat fauna of Southern several supposedly trans-Palaearctic forms. In particu- Siberia: the eastern water bat, Hilgendorf’s tube-nosed lar, the eastern water bat Myotis petax Hollister, 1912 bat, Siberian bat, etc. However, David’s myotis is not was long considered a subspecies of Daubenton’s bat included into this complex since it is a subboreal spe- M. daubentonii (Kuhl, 1817). The Siberian bat cies, its northern range boundary passing along the M. sibiricus Kastschenko, 1905, earlier considered south slope of the Western Sayan. a subspecies of Brandt’s bat Myotis brandtii (Evers- mann, 1845), was elevated to the species status. The Data on the ectoparasite fauna generally support the Far Eastern myotis Myotis bombinus Thomas, 1906 correctness of the newly established bat species. The core of the bat parasite fauna of the Eastern Palaearc- was separated from the Natterer’s bat Myotis nattereri tic boreal zone is formed by specific mites and insects (Kuhl, 1817). The Japanese long-eared bat Plecotus which also have Siberian-Far Eastern ranges (Orlova ognevi Kishida, 1927, earlier regarded as a subspecies et al., 2013). The most common and widespread spe- of the brown long-eared bat Plecotus auritus (Lin- cific ectoparasites of the eastern water bat are the ga- naeus, 1758), is also considered now a distinct species. masid mite Macronyssus charusnurensis Dusbabek, At the same time, a number of forms which were 1966 and the bat flies Nycteribia quasiocellata (Theo- earlier included into the Eastern Palaearctic complex dor, 1966) and Basilia rybini (Hurka, 1969). These of small light-colored brown bats, are now regarded as parasites are almost unknown in Europe and the one species, David’s myotis Myotis davidii Peters, Urals, except for extremely rare cases of occasional 1869. This complex included the whiskered bat introduction of M. charusnurensis (Orlova, 2014), M. mystacinus (Kuhl, 1817), the steppe bat M. aura- whereas the European sibling species Myotis dauben- scens (Kuzyakin, 1935), and the Nepalese myotis tonii is parasitized by the gamasid mite Macronyssus

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Table 2. Findings of bat ectoparasites in Tuva and adjacent areas Species of hosts Species of ectoparasites Myotis Myotis Eptesicus Regions of previous findings petax davidii nilssonii Spinturnix bregetovae 9 – – Primorskii Territory (Ussuri Reserve) Macronyssus charusnurensis 10 – – The Urals, East Kazakhstan, West and East Siberia, the Far East Macronyssus heteromorphus 2 – – East Siberia, the Far East, the Kuril Islands Macronyssus hosonoi 4 – – Altai, Krasnoyarsk Territory, the Far East, the Kuril Is- lands, Japan Steatonyssus spinosus 13 – – The Palaearctic from the British Isles to the Pacific Ocean Steatonyssus superans 6 – – The Urals, West and East Siberia, the Far East Basilia m. mongolensis – 10 – Kazakhstan, Central Asia, Mongolia Basilia rybini 16 – – East Kazakhstan, West and East Siberia, the Far East Nycteribia quasiocellata 42 – – East Kazakhstan, West and East Siberia, the Far East, the Kuril Islands Penicillidia monoceros 7 – – East Kazakhstan, West and East Siberia, the Far East, the Kuril Islands Myodopsylla trisellis 5 – – The Boreal zone from the Baltic coast to the Far East Cimex sp. – – 2 – Total 114 10 2 Sources of data: Senotrusova and Tagiltsev, 1968; Dusbabek and Radovsky, 1972; Uchikawa, 1979; Micherdzinski, 1980; Stanyukovich, 1995; Medvedev et al., 1991; Polkanov and Medvedev, 1997; Stanyukovich, 1997; Lehr, 1999; Orlova et al., 2013, 2014; Orlova, 2014; original data. diversipilis (Vitzthum, 1920) and the bat fly Nycteri- 2. Macronyssus hosonoi Uchikawa, 1979. This is bia kolenatii Theodor et Moscona, 1954 which, in a Central-Eastern Palaearctic species which was de- their turn, were not recorded east of the trans-Ural scribed in Japan from the whiskered bat Myotis region (Medvedev et al., 1991; Orlova et al., 2014). mystacinus (Kuhl, 1817) s. lato, i.e., probably from M. gracilis Ognev, 1927. The species is scarce and RESULTS little studied. Up till now, single individuals of A considerable part of the arthropods collected is M. hosonoi have been found in Krasnoyarsk Territory common to the region and the hosts (Medvedev et al., (Stanyukovich, 1997) and Altai (our data) on the Sibe- 1991; Orlova et al., 2014) (Table 2). However, in our rian bat M. sibiricus Kastschenko, 1905. Other re- opinion, some findings are of special interest. ported hosts are Ikonnikov’s bat M. ikonnikovi Ognev, 1912, the western barbastelle Barbastella darjelingen- Mites of the Cohort Gamasina sis (Hodgson, 1855) (Uchikawa, 1979), and the Japa- (Acari, Mesostigmata) nese long-eared bat P. ognevi (Stanyukovich, 1997). Our material (site 2) includes 4 ind. of M. hosonoi (all 1. Spinturnix bregetovae Stanyukovich, 1995. The ♀, one with an intrauterine egg) collected from the species was described from unidentified bats in the Far eastern water bat. East: Primorskii Territory, Suputin (now Ussuri) Re- serve. Our finding (site 2) is the first one since the 3. Macronyssus heteromorphus Dusbabek et Ra- original description of the species. Our material in- dovsky, 1972. This is probably a Central-Eastern cludes 9 ind. of S. bregetovae (5 ♂, 4 ♀) (Figs. 1a, 1b) Palaearctic species which was described from an acci- collected from the eastern water bat. This mite proba- dental host, the Norway rat Rattus norvegicus (Ber- bly parasitizes bats of the Siberian-Far Eastern com- kenhout, 1769), on the Kuril Islands. These mites were plex. It is distributed in the Far East and Central and collected from the eastern water bat, the Siberian bat, Eastern (probably also Western) Siberia. the northern bat, and Hilgendorf’s tube-nosed bat

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Fig. 1. Spinturnix bregetovae: (a) ♀, idiosoma ventrally; (b) ♂, idiosoma ventrally. Scale bar 100 nm.

Murina hilgendorfi Peters, 1880 in Krasnoyarsk Terri- Bed Bugs of the Family Cimicidae tory and some places in the Far East (Dusbábek and (Insecta: Hemiptera) Radovsky, 1972; Stanyukovich, 1997). We collected 6. Cimex sp. (Cimex ex gr. pipistrelli?). Two 2 ind. of M. heteromorphus (site 2, all ♀ with intrau- nymphs were collected off the northern bat (site 6). terine eggs) from the eastern water bat. Bugs feeding on bats are not sufficiently studied in the 4. Steatonyssus superans (Zemskaya, 1951). This is Western Palaearctic, whereas data on the Eastern a Central-Eastern Palaearctic oligophagous species Palaearctic are practically absent (Balvín et al., 2012, whose hosts are parti-colored bats of the genus Ves- 2013), except for Japan where Cimex pipistrelli pertilio and also the northern bat Eptesicus nylssonii Jenyns, 1839 and Cimex japonicus Usinger, 1966 were (Keyserlink et Blasius, 1839) (Stanyukovich, 1997; described from bats (The Wild of Japan, Orlova, 2013). Our material (site 2) includes 6 ind. of 2009). S. superans (all ♀, three with intrauterine eggs) from the eastern water bat. DISCUSSION Our material includes one species of bat flies new to Bat Flies of the Family Nycteribiidae (Insecta: Diptera) Russia: Basilia m. mongolensis. Of the gamasid mites, Spinturnix bregetovae was recorded in the study re- 5. Basilia m. mongolensis Theodor, 1966. This is gion for the first time, and new host species were indi- a little studied Central-Eastern Palaearctic subboreal cated for two species: Macronyssus hosonoi and Stea- species, known from Western Mongolia, Kazakhstan, tonyssus superans. It should be noted that the most Kyrgyzstan, and Central Asia (Theodor, 1967; Hůrka, common Eastern Palaearctic boreal bat species, the 1969, 1984; Polkanov and Medvedev, 1997; our data). eastern water bat, was for the first time indicated as In the territory of Russia, the species was found by us a host for all the three mite species. Thus, the list of its for the first time (sites 4 and 5): 10 ind. (3 ♂, 7 ♀) arthropod parasites currently includes 17 species and were collected from the steppe whiskered bat not 14 as it was supposed earlier (Orlova et al., 2014). (Figs. 2a, 2b). Earlier, Myotis mystacinus (Kuhl, 1817) in the old interpretation, i.e., David’s bat M. davidii, All the gamasid mites found by us belong to the Si- was indicated as the host; this bat is evidently the main berian-Far Eastern boreal complex of bat ectoparasites host of this parasite. (Orlova, 2014). The complex includes 11 mite and

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Fig. 2. Basilia mongolensis mongolensis: (a) ♀, abdomen dorsally; (b) ♂, sternite V and genital area ventrally. Scale bar 500 nm. insect species which generally have Eastern-Palae- the Palaearctic. However, since their findings in arctic ranges, three of them also extending into the the region are singular, further studies of the distribu- eastern part of the Western Palaearctic. tion and host range of these ectoparasites are neces- sary. The main host of the bat fly Basilia m. mongolensis is probably David’s myotis distributed in the arid sub- Our findings indicate that the Siberian-Far Eastern boreal landscapes of the Central and Eastern Palaearc- boreal complex of bat ectoparasites is characterized by tic. The records of B. m. mongolensis in Russia are a conservatism of the species list and remains practi- determined by the fact that David’s myotis also ex- cally the same over the vast territory from Altai to the tends into the south slope of the Western Sayan. Kuril Islands. Of special interest is the bug Cimex sp. (probably ACKNOWLEDGMENTS Cimex ex gr. pipistrelli) recorded in the south of Kras- This study was supported through the project noyarsk Territory. Findings of these ectoparasites on no. 6.657.2014/k “Biotic Ecosystem Component, Pro- boreal bat species are scarce, and those in the eastern perties, Resource Potential and Dynamics in a Trans- Palaearctic are very rare. The taxonomic status of the forming Environment of Western Siberia” (state task) Western Palaearctic bugs of the genus Cimex associ- and Russian Program for Competitiveness Enhance- ated with bats is still obscure. They are tentatively ment of Leading Russian Universities among Global included by us in the species group pipistrelli (Balvín Research and Education Centers (project 5-100). et al., 2013). Studies of the bugs of the genus Cimex REFERENCES parasitizing the bats in the Western Palaearctic boreal zone were not carried out. 1. Balvín, O., Sevcik, M., Jahelkova, H., et al., “Transport of Bugs of the Genus Cimex (Heteroptera: Cimicidae) According to the available data, the ranges of the by Bats in Western Palaearctic,” Vespertilio 16, 43–54 mites Macronyssus hosonoi and Steatonyssus superans (2012). 2. Balvín, O., Vilímová, J., and Kratochvíl, L., “Batbugs embrace the taiga zone of the Central and Eastern (Cimex pipistrelli group, Heteroptera: Cimicidae) are Palaearctic. According to our data, the gamasid mites Morphologically, but not Genetically Differentiated Spinturnix bregetovae and Macronyssus heteromor- among Bat Hosts,” J. Zool. Syst. Evol. Res. 51 (4), phus have ranges embracing the eastern part of 287–295 (2013).

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