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First record of Pipistrelluspygmaeus (Chiroptera:Vespertilionidae) in AnatoliaChristian Dietz a , Isabel Schunger a , Özgür Keşapli

Didrickson b , Ahmet Karataş c & Frieder Mayer d

a Department of Animal Physiology, University ofTübingen, Auf der Morgenstelle 28, 72076, Tübingen,Germanyb Kuş Araştırmaları Derneği, P.K. 311, 06443,Yenişehir, Ankara, Turkeyc Department of Biology, University of Niğde, 51200,Niğde, Turkeyd Institute of Zoology II, University of Erlangen,Staudtstrasse 5, 91058, Erlangen, GermanyVersion of record first published: 28 Feb 2013.

To cite this article: Christian Dietz , Isabel Schunger , Özgür Keşapli Didrickson , AhmetKarataş & Frieder Mayer (2005): First record of Pipistrellus pygmaeus (Chiroptera:Vespertilionidae) in Anatolia, Zoology in the Middle East, 34:1, 5-10

To link to this article: http://dx.doi.org/10.1080/09397140.2005.10638077

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First record of Pipistrellus pygmaeus (Chiroptera: Vespertilionidae) in Anatolia

by Christian Dietz, Isabel Schunger, Özgür Ke�apli Didrickson, Ahmet Karata� and Frieder Mayer

Abstract. According to morphological characters and mitochondrial DNA sequences, eight very small bats of the Pipistrellus pipistrellus complex captured at the Ku� Cenneti National Park in the Marmara Region of Turkey could be assigned to the recently discovered species Pipistrellus pygmaeus. This finding represents the first record of Pipistrellus pygmaeus in Anatolia and the second in Turkey. The species may be distributed much further along the Aegean coast of Anato-lia.

Kurzfassung. Anhand morphologischer Merkmale und mitochondrialer DNA-Sequenzen konn-ten acht sehr kleine Fledermäuse aus dem Pipistrellus pipistrellus-Komplex, die im Ku� Cenneti-Nationalpark gefangen worden waren, als Mückenfledermäuse (Pipistrellus pygmaeus) bestimmt werden. Dies ist der erste Fund der Art in Anatolien und der zweite in der Türkei. Er lässt ein Vorkommen auch entlang der anatolischen Ägäisküste erwarten.

Key words. Distribution, Pipistrellus pygmaeus, bats, Chiroptera, Anatolia, Turkey.

Introduction The first studies on the phonic discrimination of bats with bat detectors revealed two differ-ent types of echolocation calls within bats which were thought to belong to Pipistrellus pipistrellus (Schreber, 1774) (AHLEN 1981, WEID & VON HELVERSEN 1987), and these calls were subsequently identified as actually belonging to two different species, the Common Pipistrelle, P. pipistrellus, and the Midge Bat, P. pygmaeus (Leach, 1825). Both species occur sympatrically (JONES & PARIJS 1993) and show considerable genetic differences (BARRATT et al. 1993, 1995, 1997). HÄUSSLER et al. (1999) described external characters which help to distinguish German P. pipistrellus and P. pygmaeus. In recent years P. pyg-maeus has been found in most European countries (MAYER & VON HELVERSEN 2001, PRE-SETNIK et al. 2001, DIETZ et al. 2002, HULVA et al. 2004) and hence it was expected that the species would occur in Turkey as well. In 2003 BENDA et al. gave the first Turkish record of P. pygmaeus from Thrace. We now add the first record of the species for the Asiatic part of Turkey.

Material and methods On 17.9.2003, we found several groups of bats in the birdwatching tower in the Ku� Cenneti National Park, situated on the north coast of Lake Manyas (Manyas Gölü, Ku� Gölü), mainly behind the window shutters and under the roof. The total number of bats was estimated to exceed

Zoology in the Middle East 34, 2005: 5–10. ISSN 0939-7140 © Kasparek Verlag, Heidelberg

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100 individuals, but many more bats were heard crawling and chirping behind the inaccessible wooden covering of the roof. We caught four groups of bats, with a total of 22 individuals, and four additional single roosting bats from behind the window shutters. The bats were identified according to external characters and released immediately thereafter. Three individuals of the genus Pipistrellus were inspected more precisely: we took external measurements (lengths of forearm including wrist (FA+), 5th finger excluding wrist (D5-), 3rd finger excluding wrist (D3-), second phalange of the third digit (3-2) and third phalange of the third digit (3-3) with a Hommel mechanical calliper (±0.1 mm). Body mass (M) was assessed using a Soehnle 200 electronic balance (±0.1 g). Close-up photographs of the narial region, ear, tragus, penis and general appear-ance were taken using a Nikon F 100 camera with 105 mm macro-lens, close-up extension and a close-up flash. Small tissue samples of the wing membrane were taken from these three individu-als using a sterile biopsy-punch (2.5 mm). Total genomic DNA was isolated and the mitochon-drial ND1 gene was amplified and sequenced as described in MAYER & VON HELVERSEN (2001).

Results and discussion The 26 bats captured in the observation tower were assigned to three species: two single roosting individuals and the individuals of three small groups were identified as Pipistrellus nathusii (altogether 16 individuals). A tissue sample was taken from one male: the DNA-sequence of its ND1-gene did not differ from P. nathusii from different parts of Europe. Two single roosting individuals belonged to the species Eptesicus serotinus.

Whereas Eptesicus serotinus is widely distributed in Turkey (SPITZENBERGER 1994, BENDA & HORACEK 1998), Pipistrellus nathusii is only known from a few localities in Thrace and around the Marmara Sea (BENDA & HORACEK 1998). P. nathusii had already been found at Lake Manyas by LEHMANN (1966), and it may occur during migration in areas further south as well.

One more group of eight bats was captured behind a window shutter and they were identi-fied as Pipistrellus pygmaeus. These eight bats clustered closely together behind a window shutter about halfway up the observation tower. The group comprised two males and six females. One of the males was sexually active and had very big and well-filled epididymids; the other male was subadult, most probably a yearling, without any signs of reproduction and with small black epididymids. Four females had been raising young in the previous season according to their nipples, which were quite big and not covered by fur. The two other fe-males were nulliparous and most probably born in the same year. The species was identified according to the characters given by HÄUSSLER et al. (1999) and DIETZ & VON HELVERSEN (2004). All eight individuals closely resembled each other. The three younger bats (one �, two �) were dark olive-brown and had a rather dark blackish-brown skin (Fig. 1). All five older individuals were typically coloured with light brown ears and a light brown pelage with sandy-coloured tips on the back. The skin was quite light-coloured between the eyes and the ears and at the base of the ears as in most individuals of this species. All individuals had a clearly visible internarial ridge. The pattern of veins in the wing was similar to the pattern of P. pygmaeus in VON HELVERSEN & HOLDERIED (2003). In the adult male the penis was bright orange-coloured (Fig. 2), in the subadult male whitish with a slight yellowish tinge. The four adult females had orange skin around the vagina as well. All five adult bats had an obvious musk-like smell. The three younger bats had no remarkable odour.

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Mammalia 7

Fig. 1. Portrait of a sub-adult male Midge Bat (Pipistrellus pygmaeus) captured on 17.9.2003 at Ku� Cenneti National Park, Turkey.

Morphological measurements were taken from two males (Tab. 1). They are within the range of P. pygmaeus from Greece and Bulgaria (DIETZ & SCHUNGER, own data). The DNA-sequences of the ND1-gene of the same two males were identical with sequences of P. pyg-maeus from Europe and clearly distinguished from DNA-sequences of P. pipistrellus (MAYER & VON HELVERSEN 2001). The absence of substantial differences in ND1-sequences between populations of P. pygmaeus is in accordance with the results of MAYER & VON HELVERSEN (2001) and BENDA et al. (2003) for the cytochrome b gene.

The eight P. pygmaeus possibly represented a harem as only one of the two males had large testes and filled epididymids. Harem groups are well documented for P. nathusii during the mating season in various regions of Europe. Due to the single observation we do not know whether P. pygmaeus forms a resident population at Manyas Gölü. It may well be possible that the species migrates in autumn to the south from a more northern or western area where reproduction takes place (as can be expected in P. nathusii as well). The closest areas with confirmed reproduction of P. pygmaeus are situated in south-eastern Bulgaria on the coast of the Black Sea, with a nursery colony of about 120 females (town of Primorsko, District Burgas, Bulgaria, 220 km north of the Manyas Gölü: DIETZ & SCHUNGER, unpubl.), and in the Greek part of Thrace with the regular capture of pregnant or lactating females (village of Dadia, Evros region, Greece, 200 km north-west of the Manyas Gölü: DIETZ & SCHUNGER, unpubl., and PAPADATOU, pers. comm.).

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Fig. 2. Penis of an adult male Midge Bat (Pipistrellus pygmaeus) captured on 17.9.2003 at Ku� Cenneti National Park showing the species-specific yellowish-orange colour during the mating season. Tab. 1- External measurements of two male Pipistrellus pygmaeus caught on 17.9.2003 at Ku� Cenneti National Park. Measurements of Greek and Bulgarian animals are given for comparison (DIETZ & SCHUNGER, unpublished data).

� ad. Ku� Cenneti

� subad. Ku� Cenneti

n = 71 eastern Greece

n = 7 SE Bulgaria

FA+ (mm) 30.1 28.7 30.0±0.4 30.1±1.4 D5- (mm) 36.7 35.8 36.8±1.1 37.3±1.4 D3- (mm) 49.6 49.5 51.3± 0.5 52.7±1.4 3-2 (mm) 7.7 7.6 7.8±0.4 7.8±0.1 3-3 (mm) 6.9 6.7 7.2±0.4 7.2±0.5 BM (g) 4.4 4.0 4.7±0.3 5.5±1.6

Pipistrellus pygmaeus had previously been reported from Turkey only once, by BENDA et al. (2003). They captured a juvenile female and a subadult male in Turkish Thrace (Velika Köprüsü, Kirklareli prov., 180 km north of Manyas Gölü), and this indicates a reproduction site. Genetic analysis showed that another record from the Turkish Aegean coast in 1998 (mentioned by DIETZ et al. 2002) was based on misidentification. In general, P. pygmaeus is widely distributed throughout Europe including the Mediterranean region. It occurs on sev-eral Greek islands along the Anatolian coast (Rhodes, Lesbos and Cyprus, MAYER & VON HELVERSEN 2001, BENDA et al. 2003). The wide range of habitats used by this species sug-gests that it is widespread in Turkey and is also reproducing there.

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Acknowledgements. We are grateful to the members of the Turkish Bird Research Society bird-ringing team at the Ku� Cenneti National Park for their help in capturing the bats, and to Andrea SANDER for DNA isola-tion and sequencing.

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Authors’ addresses: Christian Dietz and Isabel Schunger, Department of Animal Physiology, Univer-sity of Tübingen, Auf der Morgenstelle 28, 72076 Tübingen, Germany. – Özgür Ke�apli Didrickson, Ku� Ara�t�rmalar� Derne�i, P.K. 311, 06443 Yeni�ehir, Ankara, Turkey. – Ahmet Karata�, Department of Biology, University of Ni�de, 51200 Ni�de, Turkey. – Frieder Mayer, Institute of Zoology II, Uni-versity of Erlangen, Staudtstrasse 5, 91058 Erlangen, Germany. – E-mail contact: ChristianDietz-Horb@web.de.

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