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ECTOPARASITE ASSOCIATIONS OF BATS FROM THE URALS (RUSSIA)
M
ARIAV
.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 re- ported. 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 north- western Russia (Leningradskaya re- gion) and the Russian Far East (Sta- nyukovich 1990; Medvedev et al.
1991), little is known about their occu- rence 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 prov- al”, “Olenyi ruchyi” natural park (Nizhne- serginskiy district); Ekaterinburg city; Dvu- rechensk 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: Myo- tis dasycneme, M. daubentonii, M. brand- tii; Vespertilionini: Eptesicus nilsonii, Ves- pertilio murinus; Plecotini: Plecotus auri- tus).
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 perma- nent storage. Bat flies were stored in 70%
alcohol. Ectoparasite species were deter- mined using light microscopy, according to
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;
Bartonička 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 Ecolo- gy, 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 ecto- parasite were assessed.
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-
nus in Ekateriburg.
1.2 Order Mesostigmata, Family Spin- turnicidae
Spinturnix myoti (Kolenati 1856): 56 specimens were found on three hosts:
M. dasycneme (2 females from Smolin- skaya cave), M. daubentonii (10 fe- males, 16 males, 5 deutonymphs, 2 protonymphs near Dvurechensk and one female in Smolinskaya cave) and M. brandtii (3 females, 2 males, 3 deu- tonymphs, 2 protonymphs in Dvure- chensk; 2 females, 7 males, one deuto- nymphs 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.
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;
Bartonička 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 Ecolo- gy, 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 ecto- parasite were assessed.
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-
nus in Ekateriburg.
1.2 Order Mesostigmata, Family Spin- turnicidae
Spinturnix myoti (Kolenati 1856): 56 specimens were found on three hosts:
M. dasycneme (2 females from Smolin- skaya cave), M. daubentonii (10 fe- males, 16 males, 5 deutonymphs, 2 protonymphs near Dvurechensk and one female in Smolinskaya cave) and M. brandtii (3 females, 2 males, 3 deu- tonymphs, 2 protonymphs in Dvure- chensk; 2 females, 7 males, one deuto- nymphs 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.
Table 1 - Bat ectoparasites in the study area. Figures are: number of ectoparasites, prevalence(%)and mean intensity, respectively. Host Myotis dasycneme (N=23)Myotis daubentonii (N=14)Myotis brandtii (N=12)Eptesicus nilsonii (N=13)Vespertilio murinus (N=20)Plecotus auritus (N=4) Ectoparasite ACARI, Mesostigmata, Spinturnicidae Spinturnix myoti 2, 8.7, 1.034, 78.6, 3.120, 50.0, 3.3 Spinturnix plecotinus20, 100, 5.0 Spinturnix kolenatii 74, 84.6, 6.7 Macronyssidae Macronyssus granulosus 3, 8.3, 3.0 Macronyssus charusnurensis16, 33.3, 4.0 Macronyssus corethroproctus604,69.6, 37.8 Macronyssus diversipilis 1, 7.1, 1.0 Macronyssus ellipticus3, 8.3, 3.0 Macronyssus flavus 12, 30.7, 3.0 Macronyssus cyclaspis 1, 7.1, 1.0 Steatonyssus sp. 1, 8.3, 1.0 Ixodida, Argasidae Argas vespertilionis 49, 75.0, 3.3 Trombidiformes, Trombiculidae Trombiculidae1, 25, 1.0 Prostigmata, Myobiidae Acantophthirius mystacinoides1, 8.3, 1.0 INSECTA, Diptera, Nycteribiidae Nycteribia kolenatii 1, 4.3, 1.020, 64.0, 2.2 Penicillidia monoceros21, 39.1, 2.6 Hemiptera, Cimicidae Cimex pipistrelli1, 5, 10 Siphonaptera, Ischnopsillidae Myodopsylla trisellis 8, 34.8, 1.03, 14.3, 1.59, 41.7, 1.8 Ischnopsyllus obscurus 1, 7.7, 1.0 Ischnopsyllus hexactenus 2, 15.4, 1.0
1.3 Order Mesostigmata, Family Macronyssidae
Macronyssus charusnurensis (Dusba- bek 1962): 16 deutonymphs were found on M. brandtii in Divja cave.
Macronyssus corethroproctus (Oude- mans 1906): 604 individuals were re- corded on M. dasycneme: one female and 96 protonymphs in Arakaevskaya cave; 11 females, one male, 495 pro- tonimphs 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 Epte- sicus nilsonii near Dvurechensk.
Macronyssus ellipticus (Kolenati 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 proto- nymphs 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 Miobii- dae Acantophthirius mystacinoides (Uchi- kawa 1981): one female on M. brandtii.
1.5 Order Acarina, Suborder Trombidi- formes, Family Trombiculidae
The larvae of an acarian mite belonging to family Trombiculidae was found on P. auritus.
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 Smolin- skaya cave.
Penicillidia monoceros (Speiser 1900):
21 specimens were found on M. dasy- cneme: 2 males in Arakaevskaya cave, 1 male near Dvurechensk, 18 individu- als (5 males and 13 females) in Smolin- skaya cave.
2.2 Order Hemiptera, Suborder Hete- roptera, 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 fe- males 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 Ara- kaevskaya cave.
Argas vespertilionis is a common ecto-
parasite of dendrophile and synanthrop-
ic bats from northern Eurasia (Bobkova
1.3 Order Mesostigmata, Family Macronyssidae
Macronyssus charusnurensis (Dusba- bek 1962): 16 deutonymphs were found on M. brandtii in Divja cave.
Macronyssus corethroproctus (Oude- mans 1906): 604 individuals were re- corded on M. dasycneme: one female and 96 protonymphs in Arakaevskaya cave; 11 females, one male, 495 pro- tonimphs 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 Epte- sicus nilsonii near Dvurechensk.
Macronyssus ellipticus (Kolenati 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 proto- nymphs 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 Miobii- dae Acantophthirius mystacinoides (Uchi- kawa 1981): one female on M. brandtii.
1.5 Order Acarina, Suborder Trombidi- formes, Family Trombiculidae
The larvae of an acarian mite belonging to family Trombiculidae was found on P. auritus.
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 Smolin- skaya cave.
Penicillidia monoceros (Speiser 1900):
21 specimens were found on M. dasy- cneme: 2 males in Arakaevskaya cave, 1 male near Dvurechensk, 18 individu- als (5 males and 13 females) in Smolin- skaya cave.
2.2 Order Hemiptera, Suborder Hete- roptera, 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 fe- males 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 Ara- kaevskaya cave.
Argas vespertilionis is a common ecto- parasite of dendrophile and synanthrop- ic bats from northern Eurasia (Bobkova
2003). Accordingly, we found it on V.
murinus roosting inside a school build- ing. Our finding of A. vespertilionis in the Urals, 56
030’ 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 rec- orded 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 mono- phagous species infesting mostly pond bats (Radovsky 1967). The high num- ber (N = 604) of M. Corethroproctus mites found on M. dasycneme, mostly juveniles (81.9%), depended on the mite reproductive activity, which un- like most other mites, flies and fleas, occurs in autumn.
Other gamasid mites Macronyssus gra- nulosus, 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 max- imum of eight bat flies Penicillidia monoceros was caught on one bat indi- vidual.
In Russia, the Cimicidae parasitizing on bats and their relationship with the host are poorly known. The record of
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 ecto- parasite 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 Na- talya Vinarskaya (Omsk State Research Institute of Natural Foci Infections) for her great help in ectoparasite determination.
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