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Hystrix It. J. Mamm. (n.s.) 22(1) 2011: 105-110

ECTOPARASITE ASSOCIATIONS OF BATS FROM THE URALS (RUSSIA)
M
ARIA

V. ORLOVA

Institute of plant and animal ecology of Ural Branch of Russian Academy of Science 8 Marta str. 202, Ekaterinburg, Russia 620144; E-mail: masha_orlova@mail.ru
Received 25 August 2010; accepted 12 March 2011

ABSTRACT - New data on bat ectoparasites from the Middle and Northern Urals are reported. Twenty species, belonging to 8 families of insects and mites were found on six bat species: Myotis dasycneme, M. daubentonii, M. brandtii, Eptesicus nilsonii, Vespertilio murinus, Plecotus auritus. All ectoparasite species are usual for Northern Eurasia. Key words: distribution, prevalence, Acari, Insecta, Russia RIASSUNTO - Ectoparassiti dei chirotteri degli Urali (Russia). Sono riportati nuovi dati sugli ectoparassiti dei chirotteri degli Urali medio -settentrionali. Venti specie, appartenenti a 8 famiglie di insetti e acari, sono stati trovati sui seguenti pipistrelli: Myotis dasycneme, M. daubentonii, M. brandtii, Eptesicus nilsonii, Vespertilio murinus, Plecotus auritus. Tutti gli ectoparassiti sono specie comuni per l'Eurasia settentrionale. Parole chiave: distribuzione, prevalenza, Acari, Insetti, Russia
DOI: 10.4404/Hystrix-22.1-4470

INTRODUCTION While some information is available about bat ectoparasites of northwestern Russia (Leningradskaya region) and the Russian Far East (Stanyukovich 1990; Medvedev et al. 1991), little is known about their occurence and distribution in the Urals. Till now, only two species, Spinturnix myoti and Macronyssus kolenatii have been reported (Stanyukovich 1997). The aim of this work was to investigate the fauna of bat ectoparasites from this Russian region. MATERIALS AND METHODS
From 2004 to 2009, bats were captured in the Northern and Middle Urals at five sites:

caves "Arakaevskaya" and "Bolshoy proval", "Olenyi ruchyi" natural park (Nizhneserginskiy district); Ekaterinburg city; Dvurechensk settlement (Sysertskiy district); Smolinskaya cave (Kamenskiy district) and Divja cave (Perm region) (Fig. 1). Overall 83 individuals were caught, belonging to three tribes and six species (Myotini: Myotis dasycneme, M. daubentonii, M. brandtii; Vespertilionini: Eptesicus nilsonii, Vespertilio murinus; Plecotini: Plecotus auritus). A total of 908 ectoparasites was collected from the animals' skin, and then fixed in 70% alcohol. Bats were released soon after their examination at the site of capture. Successively, ticks, mites and fleas were preserved in the Berlese media for permanent storage. Bat flies were stored in 70% alcohol. Ectoparasite species were determined using light microscopy, according to

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Orlova M.V.

Figure 1 - Study area (1. Divja cave; 2. Ekaterinburg city; 3. "Olenyi ruchyi" Natural park; 4. Dvurechensk Settlement; 5. Smolinskaya cave). several identification keys (Stanyukovich 1997; Rudnick 1960; Medvedev 1996; Bartonicka 2007). They included gamasid and myobiid mites, argasid ticks and three orders of insects: Siphonaptera, Diptera and Hemiptera. Voucher arthropod specimens were deposited in the Zoological Museum of the Institute of Plant and Animal Ecology, Ural Branch of Russian Academy of Sciences. Both the prevalence (percentage of infested bats) and mean intensity (mean number of ectoparasites per infested bat) of each ectoparasite were assessed.

nus in Ekateriburg. 1.2 Order Mesostigmata, Family Spinturnicidae Spinturnix myoti (Kolenati 1856): 56 specimens were found on three hosts: M. dasycneme (2 females from Smolinskaya cave), M. daubentonii (10 females, 16 males, 5 deutonymphs, 2 protonymphs near Dvurechensk and one female in Smolinskaya cave) and M. brandtii (3 females, 2 males, 3 deutonymphs, 2 protonymphs in Dvurechensk; 2 females, 7 males, one deutonymphs in Divya cave). Spinturnix plecotinus (Koch 1839): 20 specimens (14 females, 6 males) were collected on Plecotus auritus in Divya cave. Spinturnix kolenatii (Oudemans, 1910): 72 specimens (22 males, 28 females, 21 deutonymphs and one protonymphs) were found on Eptesicus nilsonii near Dvurechensk. Two females were found on E. nilsonii in Bolshoy proval cave.
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RESULTS AND DISCUSSION Twenty species of parasites, belonging to eight families (insects, mites and ticks), were obtained from bats (Tab. 1). 1. Class Arachnida, Subclass Acari 1.1 Order Ixodida, Family Argasidae Argas vespertilionis (Latreille 1802): 49 larvae were collected from V. muri-


Table 1 - Bat ectoparasites in the study area. Figures are: number of ectoparasites, prevalence (%) and mean intensity, respectively.
Myotis daubentonii (N=14) 34, 78.6, 3.1 74, 84.6, 6.7 3, 8.3, 3.0 16, 33.3, 4.0 1, 7.1, 1.0 3, 8.3, 3.0 12, 30.7, 3.0 1, 8.3, 1.0 49, 75.0, 3.3 1, 25, 1.0 1, 8.3, 1.0 20, 64.0, 2.2 1, 5, 10 8, 34.8, 1.0 3, 14.3, 1.5 9, 41.7, 1.8 1, 7.7, 1.0 2, 15.4, 1.0 1, 7.1, 1.0 20, 50.0, 3.3 Myotis brandtii (N=12) Eptesicus nilsonii (N=13) Vespertilio murinus (N=20) Plecotus auritus (N=4)

Host

Ectoparasite

Myotis dasycneme (N=23)

20, 100, 5.0

Bat ectoparasites in Russia

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1, 4.3, 1.0 21, 39.1, 2.6

ACARI, Mesostigmata, Spinturnicidae Spinturnix myoti 2, 8.7, 1.0 Spinturnix plecotinus Spinturnix kolenatii Macronyssidae Macronyssus granulosus Macronyssus charusnurensis Macronyssus corethroproctus 604,69.6, 37.8 Macronyssus diversipilis Macronyssus ellipticus Macronyssus flavus Macronyssus cyclaspis Steatonyssus sp. Ixodida, Argasidae Argas vespertilionis Trombidiformes, Trombiculidae Trombiculidae Prostigmata, Myobiidae Acantophthirius mystacinoides

INSECTA, Diptera, Nycteribiidae Nycteribia kolenatii Penicillidia monoceros Hemiptera, Cimicidae Cimex pipistrelli Siphonaptera, Ischnopsillidae Myodopsylla trisellis Ischnopsyllus obscurus Ischnopsyllus hexactenus


Orlova M.V.

1.3 Order Mesostigmata, Family Macronyssidae Macronyssus charusnurensis (Dusbabek 1962): 16 deutonymphs were found on M. brandtii in Divja cave. Macronyssus corethroproctus (Oudemans 1906): 604 individuals were recorded on M. dasycneme: one female and 96 protonymphs in Arakaevskaya cave; 11 females, one male, 495 protonimphs in Smolinskaya cave. Macronyssus cyclaspis (Oudemans 1906): one individual was collected from M. daubentonii in Dvurechensk. Macronyssus diversipilis (Vitzthum 1920): one male was found on Eptesicus nilsonii near Dvurechensk. (Kolenati Macronyssus ellipticus 1856): one male and two protonymphs were recorded on Myotis brandtii in Arakaevskaya cave. Macronyssus flavus (Kolenati 1856): six females were recorded on Eptesicus nilsonii: one in Arakaevskaya cave, five, together with six protonymphs, near Dvurechensk. Macronyssus granulosus (Kolenati 1836): one female and two protonymphs were collected on Myotis brandtii in Arakaevskaya cave. Steatonyssus sp.: one deutonymph was recorded on M. brandtii from Divja cave. 1.4 Order Prostigmata, Family Miobiidae Acantophthirius mystacinoides (Uchikawa 1981): one female on M. brandtii. 1.5 Order Acarina, Suborder Trombidiformes, Family Trombiculidae The larvae of an acarian mite belonging to family Trombiculidae was found on P. auritus.
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2. Class Insecta 2.1 Order Diptera, Family Nycteribidae Nycteribia kolenatii (Theodor et Moscona 1954): 20 specimens (12 males and 7 females near Dvurechensk, one male in Smolinskaya cave) were collected from M. daubentonii and one male from M. dasycneme in Smolinskaya cave. Penicillidia monoceros (Speiser 1900): 21 specimens were found on M. dasycneme: 2 males in Arakaevskaya cave, 1 male near Dvurechensk, 18 individuals (5 males and 13 females) in Smolinskaya cave. 2.2 Order Hemiptera, Suborder Heteroptera, Family Cimicidae Cimex pipistrelli (Jenyns 1839): one female was collected from V. murinus near Dvurechensk. 2.3 Order Siphonaptera, Family Ischnopsyllidae Myodopsylla trisellis (Jordan 1929): a total of 21 specimens was recorded: 9 were found on M. dasycneme (6 females and 3 males in Smolinskaya cave), 3 females on M. daubentonii near Dvurechensk, 2 females on M. brandtii near Dvurechensk, 6 females and 1 male on M. brandtii in Divya cave. Ichnopsillus obscurus (Wagner 1898): one female was found on Eptesicus nilsonii near Dvurechensk. Ischnopsillus hexactenus (Kolenati 1856): one male and one female were recorded on Eptesicus nilsonii in Arakaevskaya cave. Argas vespertilionis is a common ectoparasite of dendrophile and synanthropic bats from northern Eurasia (Bobkova


Bat ectoparasites in Russia

2003). Accordingly, we found it on V. murinus roosting inside a school building. Our finding of A. vespertilionis in the Urals, 560 30' North, represents the most northern site of this species for Russia. High host specificity has been reported for spinturnicid mites (Stanyukovich 1990; Bruyndonckx et al. 2009). In our investigation, Spinturnix myoti was recorded on all Myotini, the highest prevalence (78.6%) having been recorded for M. daubentonii. Spinturnix kolenatii occurred only on E. nilsonii (84.6), while all long-eared bats (P. auritus) were infested by Spinturnix plecotinus. Macronyssus corethroproctus is monophagous species infesting mostly pond bats (Radovsky 1967). The high number (N = 604) of M. Corethroproctus mites found on M. dasycneme, mostly juveniles (81.9%), depended on the mite reproductive activity, which unlike most other mites, flies and fleas, occurs in autumn. Other gamasid mites Macronyssus granulosus, M. charusnurensis and M. ellipticus, collected on M. brandtii are polyphagous, parasitizing many species of vespertilionid bats (Dusbabek 1964; Stanyukovich 1997). The almost exclusive occurrence of Penicillidia monoceros and Nycteribia kolenatii on M. dasycneme and M. daubentonii, respectively, agreed with previous information from the East Baltic coast (Farafonova 1985). A maximum of eight bat flies Penicillidia monoceros was caught on one bat individual. In Russia, the Cimicidae parasitizing on bats and their relationship with the host are poorly known. The record of
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Cimex pipistrelli from V. murinus stirs further investigations. Myodopsylla trisellis (Ischnopsyllidae) is a bat flea parasitizing vespertilionid bats of the genus Myotis (Medvedev 1996). In our study area, it was found on all analysed Myotis species. Our preliminary screening of the ectoparasite fauna of bats from the Urals allowed to find out several species. Further researches, involving a wider range of bat species, are needed to draw up an exhaustive list. ACKNOWLEDGEMENTS
I am grateful to Oleg Orlov (Ural State Pedagogical University) and Vladimir Chernov («Olenyi ruchyi» Natural park) for their help during field work and to N atalya Vinarskaya (Omsk State Research Institute of Natural Foci Infections) for her great help in ectoparasite determination.

REFERENCES
Bartonicka T. 2007. Bat bugs (Cimex pipistrelli, Heteroptera) and roost switc hing in bats. Berichte der Naturforschenden Gesellschaft der Oberlausitz 15(1): 29 -36. Bobkova O.A. 2003. Distribution of ticks (Ixodoidea, Parasitiformes) - ectoparasites of bats (Chiroptera) in Ukraine. Vestnik Zoologii 37(6): 23­28 [In Russian]. Bruyndonckx N., Dubey S., Ruedi M., Christe Ph. 2009. Molecular cophylogenetic relationships between European bats and their ectoparasitic mites (Acari, Spinturnicidae). Molecular Phylogenetics and Evolu-tion 51: 227237. Dusbabek F. 1964. Parasitische Flederma usmilben der Tschecho-slowakei. IL. Farn. Dermanyssidae Kol. 1859


Orlova M.V. (Acarina, Gamasides). Gas. Gsl. Spol. ent 11: 77-125 Farafonova G.V., Masing, M.V. 1985. Findings of nycteribiid flies in the Pr ibaltic, Parazitologiya 19 (4): 317-318 [In Russian]. Medvedev S.G. 1996. Fleas of the fam. Ischnopsyllidae (Siphonaptera) on the fauna of Russia and adjacent countries. Entomol. Rev. 75(2): 438-454 [In Russian]. Medvedev S.G., Stanyukovich M.K., Tiunov M.P., Faraphonova G.V. 1991. Ectoparasite of bats from Russian Far East. Parasitologiya 25(1): 27-37 [In Russian]. Radovsky F.J. 1967. The Macronyssidae and Laelapidae (Acarina: Mesostigmata) parasitic on bats. Univ. Calif. Publ. Entom 46. Rudnick A. 1960. A revision of the mites of family Spinturnicidae. Univ. California Publ. Entomologia, 17: 157283. Stanyukovich M.K. 1997. Keys to gamasid mites (Acari, Parasitiformes, Mesostigmata, Macronyssoidea et Laelaptoidae) parasitizing bats (Mammalia, Chiroptera) from Russia and adjacent countries. Rudolstadter naturhistorische Schriften 7: 13-46. Stanyukovich M.K. 1990. The gamasid mite and argasid ticks of bats from Baltic States and Leningrad district. Parasitologiya 24(3): 193-200 [In Russian].

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