|Interaction of ectoparasites in cohabitating colonies of pond bats and species of genus Pipistrellus from Northern Poland
A. Zapart 1, M.V. Orlova 2
1 Department of Vertebrate Zoology and Ecology, Gdańsk University of Poland, e-mail : email@example.com
2 Institute of Plant and Animal Ecology, Ural Branch of Russian Academy of Sciences, e-mail: firstname.lastname@example.org
The pond bat (Myotis dasycneme (Boie, 1825)) is a very rare bat species in Europe (Hutson et al., 2011). Currently there are only two large colonies of this species recorded in northern Poland (Ciechanowski, 2007). Specific permanent ectoparasites of pond bat includes gamasid mites: Spinturnix myoti (Kolenatii, 1856) (specific ectoparasite of genus Myotis) and Macronyssus corethroproctus Oudemans, 1902 (Vitzthum, 1929; Radovsky, 1967; Beron, 1969; Dusbabek, 1972; Haitlinger, 1978b; Stanyukovich, 1990; Orlova, Orlov, 2011). Species of genus Pipistrellus harbor temporary ectoparasites (argasid ticks Carios vespertilionis and gamasid mites Steatonyssus periblepharus). However at the cohabitation in the colonies of pond bat and pipistrelle bat a suppression of specific ectoparasite fauna of the first species by temporary ectoparasites is observed.
Material was collected in northern Poland (Pomorskie province) in two locations: bat colonies of pond bats, soprano pipistrelle bats and Nathusius’s pipistrelle bats in the attic of home near Lubnia (53º56’11” N, 17º48’19” E) (May-June 2009 and June 2011) and feeding pond bats, captured on the river near Plesno (53º52’15” N, 17º33’10” E) (June 2011) (GDOS nr DOP-OZGIZ.6401.09.19.2011.km (7.06.2011)). In total 960 ectoparasites were collected from 30 individual pond bats; additionally 68 ectoparasites were collected from 5 soprano pipistrelle bats (Pipistrellus pygmaeus (Leach, 1825)) and 168 ectoparasites from 2 Nathusius’s pipistrelle bats (Pipistrellus nathusii (Keyserling et Blasius, 1839)). Preparation and species identification of ectoparasites involved standard methods (Bregetova, 1956).
Ectoparasite species were determined using light microscopy, according to several identification keys and articles (Rudnick, 1960; Filippova, 1966; Radovsky, 1967; Stanyukovich, 1997). According to Stanyukovich (1993), Spinturnix dasycnemi (Kolenati, 1859) (Estrada-Pena et Sanchez, 1989) and Spinturnix daubentoni (Kolenati, 1857) are not regarded as separate species, and require more research for confirm independence of both these species. The regarded name of this mite is Spinturnix myoti (Kolenatii, 1856) (Stanyukovich, 1993).
Mean intensity (MI) was calculated as the mean number of ectoparasites found per host individual (not including parasite-free individuals). Prevalence was calculated as the percentage of bats infested (Beklemishev, 1970).
Arthropod specimens were deposited in the Zoological Museum of the Institute of Plant and Animal Ecology, Ural Branch of Russian Academy of Sciences.
Below is an annotated list of collected ectoparasites:
Spinturnix myoti Kolenatii, 1856
44 individuals were collected: 12 (3♂, 3♀ (including 2 females with internal eggs), 3 N1, 3 N2) in 2009 and 32 (11♂, 2♀ with internal eggs, 4 N1, 15 N2) in 2011. This is an oligophagous ectoparasite species which parasitizes bats of the genus Myotis (Stanyukovich, 1990). Previously Spinturnix myoti has been recorded on pond bats in Poland (Haitlinger, 1978a), Germany (Haitlinger, 1997), Baltic region (Stanyukovich, 1990), Udmurt Republic (Orlova et al., 2011) and in the Urals (Orlova, 2011).
Macronyssus corethroproctus Oudemans, 1902
25 mites of this species were removed: 5♂, 19♀ (including 14 with internal eggs) and 1 protonimph (N1). This is a monophagous specific ectoparasite on pond bats, found in Poland (Haitlinger, 1978b), Germany (Haitlinger, 1997), Baltic region (Stanyukovich, 1990), Udmurt Republic (Orlova et al., 2011) and in the Urals (Orlova, 2011).
Steatonyssus periblepharus Kolenatii, 1858
We have 280 individuals of this species in our material. Of those, 236 mites were collected from pond bats: 10♂, 33♀ (including 7 with internal eggs) and 191 N1. 19 individuals were collected from soprano pipistrelle bats (3♂, 12♀, 4 N1). 25 individuals (2 ♂, 7♀ (including 1 individual with internal egg) and 16 N1) were found on Nathusius’s pipistrelle.
Steatonyssus periblepharus is a polyphagous species that is a parasite on many bat species in the families Vespertilionidae and Rhinolophidae. However, it occurs most frequently on pipistrelles (Pipistrellus pipistrellus, Pipistrellus nathusii) (Haitlinger, 1997; Stanyukovich, 1990).
Carios vespertilionis Latreille, 1796
Our material includes 802 ticks of this species. From pond bats we collected 611 individuals (larvae): 371 specimens were collected in 2009 and 240 in 2011. This is transpalaearctic species, occurring in areas south of 60ºN (Filippova 1966; Yamaguti 1961; Haitlinger, 1978a; Siuda et Sebesta, 1997; Siuda et al., 2009); it is a polyphagous species that parasitizes a broad spectrum of hosts but is most abundant on various species of bats (Myotis myotis (Borkhausen, 1797), Myotis brandtii (Eversmann, 1845), Myotis mystacinus (Kuhl, 1817), Nyctalus noctula (Schreber, 1774), Eptesicus serotinus (Schreber, 1774), Pipistrellus pipistrellus, P. pygmaeus, P. nathusii (Siuda et al., 2001; Piksa et al., 2011) and other, but prefers pipistrelle bats (Haitlinger, 1978a). Of the total, 49 specimens (larvae) were collected from soprano pipistrelles and 142 (larvae) from Nathusius’s pipistrelle.
Table. Species and characteristics of infrapopulations of ectoparasites on bats captured in Northern Poland.
Ectoparasites of the pond bat were investigated in Poland and Germany by Vitzthum (1929), Dusbabek (1972), Haitlinger (1978a, 1978b, 1997) and in the Baltic region by Stanyukovich (1990). We investigated the ectoparasite fauna of M. dasycneme in the Urals, in the ecological center of the range of this species (Orlova et al., 2011; Orlova, Orlov, 2010; Orlova, 2011). It was shown that the ectoparasite fauna of pond bats mainly comprises the permanent ectoparasites (Spinturnix andegavinus (Kolenati, 1857), S. myoti, S. kolenatii (Oudemans, 1910), Macronyssus corethroproctus, M. diversipilis (Vizthum, 1920), M. ellipticus (Kolenati, 1956), M. crosbyi (Ewing and Stover, 1915)).
There are two permanent ectoparasite species of M. dasycneme that can be found throughout the range of this bat: Spinturnix myoti and Macronyssus corethroproctus. These two species form a core of ectoparasite fauna of pond bats (Balashov, 2009). During the summer season the proportion of bats infested with the mite Spinturnix myoti in nursery colonies is normally high (prevalence is around 100% in nursery colonies) because life cycles of many species of the Spinturnix genus are synchronized with those of their hosts (Estrada-Pena et al., 1991; Lučan, 2006; own data). The proportion infested with the mite Macronyssus corethroproctus during summer also reaches 100% in nursery colonies (the average number of mites on one infested host bat is 11) (Orlova, Orlov, 2011). Temporary ectoparasites collected from pond bats includes Steatonyssus periblepharus in the Baltic region (Stanyukovich, 1990) and Steatonyssus spinosus (Willmann, 1936) in the Urals (Orlova, Orlov, 2011) and in the Kirov region (Orlova et al., 2011); also Carios vespertilionis has been recorded in northern Germany (Haitlinger, 1997) and the Baltic (Stanyukovich, 1990).
However, the ectoparasite fauna of pond bats in Northern Poland differs from the previously described pattern. The gamasid mite Macronyssus corethroproctus is a common species in pond bats elsewhere, but was not found on animals from Lubnia colony. Also, the proportion of animals infested by the tick Spinturnix myoti was relatively low in this local colony. Additionally all the specimens of S. myoti were collected in 2009 (16 bats were examined) but not one of this parasite species was found on the 10 bats examined from this colony in 2011. This is evidence of reduction of this ectoparasite species population. On the other hand, pond bats from Lubnia showed considerable infestation by Carios vespertilionis and Steatonyssus periblepharus (Table). Those ectoparasite species were also found on Nathusius’s pipistrelle (Pipistrellus nathusii), a large colony of which inhabited the same roof area.
The proportion of bats infested was similar for both Nathusius’s pipistrelle and pond bat. The skin of all the examined animals was extensively irritated by bites of argasid ticks.
Meanwhile two pond bats caught in Plesno showed a different ectoparasite species composition, similar to that found in other parts of the pond bat’s range (Vitzthum, 1929; Haitlinger, 1978, 1997; Stanyukovich, 1990; Orlova, 2011). The core ectoparasite fauna from Plesno was represented by Spinturnix myoti, Macronyssus corethroproctus and Steatonyssus periblepharus. Pond bats from this colony showed healthy skin, without the scratches and marks seen on animals from Lubnia. It is probable that these bats belong to another colony, in an as yet unknown locality.
Figure. Mean intensity (MI) of ectoparasites infestation in pond bat from several parts of its area.
Poland, Lubnia, soprano pipistrelle (n=5)
Poland, Lubnia, pond bat (n=28)
Poland, Plesno, pond bat (n=2)
Germany, Kiel, pond bat (own data) (n=6)
Russia, South Urals, Karabash town environs, pond bat (n=15) (Orlova, Orlov, 2011)
Russia, Northern Urals, Severouralsk town environs, pond bat (n=10) (Orlova, Orlov, 2011)
Russia, Middle Urals, Kamensk-Uralsky town environs, pond bat (n=10) (Orlova, Orlov, 2011)
Russia, Khanty-Mansiysk Autonomous Okrug, Kondinsky settlement, pond bat (n=5) (own data).
Therefore our study suggests that, throughout the investigated range of the pond bat, the common gamasid mite ectoparasite species were Spinturnix myoti and Macronyssus corethroproctus. Both species were absent on the animals of Lubnia colony in 2011, and single finds of the mite Spinturnix myoti were made in 2009 (this species is normally abundant on pond bats during summer period). The composition of the gamasid mite ectoparasite fauna is identical to that of the Nathusius’s pipistrelle colony inhabiting the same roof (fig.).
In conclusion, it appears that cohabitation of the bat species M. dasycneme and P. nathusii leads to the repression of permanent specific ectoparasite fauna of pond bats by nonspecific temporal ectoparasites of Nathusius’s pipistrelle. This phenomenon is described for the first time. It is interesting because on one hand it illustrates intraspecies relationships of ecoparasites from different ecological groups and on the other hand it can be used as “marker” for the colony. As a result we suggested that in addition to the Lubnia colony there is another colony of pond bats in Northern Poland, representatives of which were caught in Plesno. Searches were successful: two satellite colonies of pond bat females were found in Nothern Poland one year later (own data). Seeing M. dasycneme is very rare species in this region, such researches of pond bat ectoparasites is important.
The authors are grateful to Anna Nalewaja and Grażyna Sadowska (Academic Chiropterological Circle of Polish Society for Nature Protection "Salamandra" University of Gdańsk) for their assistance in the field studies, PhD Elena Kuz’mina (Institute of plant and animal ecology UB RAS) and John Haddow (Auritus Wildlife Consultancy, UK) for language correction of the text.
Financial support: grant for young scientist RFBR №12-04-31270.