Turkish Journal of Zoology Turk J Zool (2016) 40: 73-79 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1404-19

A new species of voles, elbeyli sp. nov., from with taxonomic overview of social voles distributed in southeastern Anatolia

1 1 2 Nuri YİĞİT , Ercüment ÇOLAK , Mustafa SÖZEN 1 Department of Biology, Faculty of Science, Ankara University, Ankara, Turkey 2 Department of Biology, Faculty of Arts and Sciences, Bülent Ecevit University, Zonguldak, Turkey

Received: 10.04.2015 Accepted/Published Online: 05.09.2015 Final Version: 01.01.2016

Abstract: There are twelve Microtus species in Turkey and two of them are endemic to the steppic central Anatolian plateau. In this study, previously collected specimens that were recorded as Microtus irani from southeastern Turkey were reevaluated by karyologically comparing different species distributed throughout southeastern Turkey. The taxonomic status of this species was raised to a new species, Microtus elbeyli sp. nov., which has dark ochreous dorsal color, agrestis morphotype in M2, and 2n = 46, NF = 50, NFa = 46 karyotype. The new species described here raises the total number of Microtus species in Turkey to 13 and endemic vole species in Anatolia to three.

Key words: Microtus elbeyli, , morphology, distribution, new species, Turkey

1. Introduction record of M. irani by Çolak et al. (1997), another diploid Voles in the genus Microtus were represented by 12 species chromosome number (2n = 60) for the same species was in Turkey (Yiğit et al., 2006b; Kryštufek and Vohralík, reported from southern Turkey by Kryštufek et al. (2009). 2009). Two of these species are endemic to Turkey and Up to now, species of social voles distributed in distributed mainly in Central Anatolia and the inner region southeastern Turkey have remained doubtful, especially of in Mediterranean Anatolia (Kryštufek for M. cfr. irani with 2n = 46 (Çolak et al., 1997; Kryštufek and Kefelioğlu, 1999, 2001b; Yiğit et al., 2006b; Yavuz et and Kefelioğlu, 2001b; Kryštufek et al., 2009; 2010). al., 2009, 2011; Şekeroğlu et al., 2011). Three out of these The aim of the present research is to reevaluate 12 vole species are distributed throughout southeastern specimens previously recorded as M. cfr. irani by Çolak Anatolia and close localities in Syria including M. socialis, et al. (1997) based on its morphological and karyological features and to clarify the taxonomic status of these M. guentheri, and M. irani (Çolak et al., 1997; Shebab and specimens. Cherabi, 2006; Yiğit et al., 2006a). Microtus irani Thomas, 1921 was originally described 2. Materials and methods from Shiraz () and was also recorded from several Large numbers of social vole specimens were collected localities in eastern Turkey (Kock et al., 1972; Morlok, from Anatolia, including southeastern Turkey, between 1978; Kock and Nader, 1983). More recently Çolak et 1993 and 2012. The specimens from the southeastern and al. (1997) recorded M. cfr. irani (2n = 46) from in eastern parts of Anatolia were taken under evaluation southeastern Turkey, and the type series of M. irani from in order to solve taxonomical problems. The sampling Shiraz (Iran) was redescribed and the differences between localities are shown in Figure 1. Apart from the specimens the type series and western Iranian specimens were from southeastern Turkey, the specimens from Muş pointed out by comparing western Iranian and Turkish Province were taken into consideration in order to specimens by Kryštufek and Kefelioğlu (2001). compare them with the specimens from southeastern The diploid numbers of chromosomes of M. irani Anatolia. The specimens were karyotyped to confirm were reported to be from 2n = 60 to 64 by Zima and Kral species identification; thus, specimens were karyologically (1984) and 2n = 62 by Golenishchev et al. (2002). After the identified and were assigned to taxa as follows: * Correspondence: [email protected] 73 YİĞİT et al. / Turk J Zool

Microtus socialis, 2n = 62 (Muş Province), Type locality: 1 km NW of Karacaören village of Kilis Microtus guentheri, 2n = 54 (type locality, Türkoğlu/ Province in southeastern Turkey. Kahramanmaraş), Diagnosis: External measurements (mm) and weight Microtus cfr. irani, 2n = 60 (this species was previously (g) of holotype; TbL = 135, TL = 21, HfL = 18, EL = 12, and recorded from Ermenek town by Kryštufek et al. (2009) W = 36. Some cranial measurements (mm) of holotype: and was recorded from in the present occipitonasal length is 27.6, zygomatic breadth 16.5, basal study; see Figure 1), length 25, nasal length 7.7, width of braincase 12.16, Microtus sp. with 2n = 46 (). height of braincase with bullae 10.4, diastema length 9.0, We examined five specimens ofM. socialis, ten of M. guentheri, three of M. irani, and fifteen of the 2n = 46 form palatal length 14.6, mandible length 16.86 (Table 1). The that were previously identified as M. cfr. irani by Çolak et dorsal color is generally ochreous and slightly paler on al. (1997). sides. Ventral fur is pale buff with dark gray bases. There The occlusal patterns of molar teeth were evaluated is a prominent delineation line between flanks and belly. according to Niethammer and Krapp (1982). The Upper and ventral hair of feet are pale buff. The skull is karyotype analysis was achieved by using the conventional slender with comparatively smooth brain case (Figure bone marrow technique. The external measurements 2). M2 in all specimens was found to be the agrestis were taken from fresh specimens in the field and from morphotype. The diploid number of chromosomes is 46 each skull in the laboratory with a caliper accurate to the with 50 chromosomal arms. nearest 0.05 mm. Abbreviations are as follows: TbL = total Etymology: Elbeyli is a town of Kilis Province where body length, TL = tail length, HfL = hindfoot length, EL = most of the specimens were collected. ear length, W = weight. The skins and skulls of specimens Description: The 15 examined specimens with 2n examined were deposited in the Biology Department at = 46 and ochreous dorsal color were captured from two Ankara University. different locations in southeastern Turkey (Figure 1). 3. Results and discussion However, the dorsal pelage was found to be exceptionally Microtus elbeyli sp. nov. dark brownish in a few specimens. The dorsal colors of Holotype: An adult male (collection number: 2919) our specimens were markedly different from M. guentheri held in the Zoology Museum of the Biology Department but slightly different from M. cfr. irani with 2n = 60 from at Ankara University. Mardin. The external and cranial measurements and some

Figure 1. Record locations of the specimens evaluated: M. elbeyli (●10 km east of Kilis and ⦿ Elbeyli), M. cfr. irani (▲ Ermenek, ✸ Nusaybin), M. guentheri (■ Türkoğlu and △ Nemrut), M. socialis (□ Muş), M. irani (★ Shiraz/Iran).

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Table 1. Measurements of cranial and external characters of M. elbeyli sp. nov. (SD = standard deviation; n =number of specimens).

2919 ♂ Min–max n Mean ±SD Holotype Total length 135 120–150 11 135.91 8.34

Head and body length 114 97–120 11 110.36 6.38

Tail length 21 20–33 11 25.54 4.01

Hind foot length 18 13–20 11 18.27 1.85

Ear length 12 11–14 11 12.36 1.03

Weight (g) 36 23–36 11 30.64 4.48

Zygomatic breadth 16.5 14.35–18.08 12 16.07 1.13

Interorbital constriction 3.4 3.40–4.15 15 3.78 0.18

Condylobasal length 26.9 22.86–27.76 14 25.89 1.49

Occipitonasal length 27.6 25.28–29.50 14 27.58 1.14

Basal length 25 22.26–27.32 14 24.77 1.21

Nasal length 7.7 7.41–9.20 15 8.14 0.52

Nasal width 4.3 3.23–4.48 15 3.88 0.40

Length of facial region 16.6 13.83–17.25 15 15.60 1.07

Mastoid breadth 8 6.68–8.80 13 7.80 0.61

Skull height 8.3 7.67–9.32 14 8.35 0.49

Occipital width 13.6 11.65–13.60 14 12.78 0.56

Braincase width 12.16 10.82–12.59 14 11.68 0.62

Height of braincase with bullae 10.4 8.50–10.40 13 9.74 0.47

Rostral height 5.32 4.70–5.78 14 5.22 0.30

Diastema 9 7.08–9.40 15 8.26 0.69

Palatal length 14.6 12.64–14.92 15 14.24 0.63

Foramen incisivum 4.5 3.23–5.08 14 4.11 0.58

Tympanic bullae 8.5 7.05–8.50 13 7.72 0.40

Mandible 16.86 14.84–16.86 14 15.92 0.77

Maxillary tooth row 5.6 5.60–6.41 12 5.96 0.27

Mandibular tooth row 5.4 5.22–6.57 13 6.02 0.42 morphological structures of specimens were drawn and morphology are the main differences (Figure 2). The given in our previous work (Çolak et al., 1997). The skull braincase is smoother than those of M. guentheri and structures of these new specimens have some differences M. cfr. irani and is not shallow as in M. socialis. Apart from M. cfr. irani and M. guentheri. Even though the from these differences, the nasal area in M. guentheri is skull is similar to that of M. guentheri, the sharp slope of markedly bent down compared to the other two species. the supraoccipital region in the braincase and mandible The parietal bones of M. irani are narrow and exo-occipital

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Figure 2. Skulls (dorsal and lateral views) and mandible (labial views) of species: A) M. elbeyli, B) M. cfr. irani, C) M. guentheri. condyles are almost visible in the dorsal aspect of skull. from the condyloid process. The skull is slender with a Incisive foramina do not project beyond the M1. The comparatively smooth brain case and the suprameatal ventral parts of tympanic bullae are enlarged and are more triangle is markedly a more rounded oval than in the other marked than in M. socialis but are almost similar to those species. of M. guentheri. The mandible is slender and its coronoid Dentition: The occlusal molar patterns of 2M are found and angular processes are different from other species in to be the non-agrestis morphotype and M3 patterns were the manner of markedly separating the coronoid process observed as 50% normal, 29% complex, and 21% duplicate

Figure 3. Dentition of M. elbeyli sp. nov. A) Upper tooth row, B) lower tooth row. M1: First upper molars, M2: second upper molars, M3: third upper molars. M1: First lower molars, M2: second lower molars, M3: third lower molars. La.: Labial side, Li.: lingual side. Type specimen, No: 2919, ♂, collected 10 km east of Kilis.

76 YİĞİT et al. / Turk J Zool forms (Figure 3). M2 patterns of all other specimens of irani karamani, based on phylogenetic analyses of social M. guentheri and M. cfr. irani were found to be the non- vole specimens. agrestis morphotype; therefore, it was concluded that Karyology: The karyotype of five specimens from the M2 patterns are not distinctive among taxa. Kefelioğlu Microtus population in 2n = 46 from Kilis was described (1995) reported 40% non-agrestis morphotype for M. by Çolak et al. (1997) as 2n = 46, NF = 50, and NFa = socialis in Turkey. Similarly, the agrestis morphotype was 46. The X chromosome was large metacentric and the Y observed in high frequencies in M. socialis specimens of chromosome was the smallest metacentric (Figure 4). Turkish, Caucasian, Lebanese, Syrian, and Iranian origin In the phylogenetic analyses of Kryštufek et al. (2009), (Kefelioğlu and Kryštufek, 1999; Kryštufek and Kefelioğlu, M. anatolicus with 2n = 60, M. irani with 2n = 60, and M. 2001a). In the type specimen of M. irani, the M2 occlusal socialis with 2n = 62 were grouped into the same cluster, molar pattern was also reported as the agrestis morphotype indicating the close genetic resemblance. In our previous in the figure given by Kryštufek and Kefelioğlu (2001b). study (Yiğit et al., 2006), the specimens with 2n = 60 were Taxonomic remarks: According to morphological and also found and identified as Microtus schidlovskii in eastern karyological examinations of the specimens captured from Turkey, and we also pointed out the cranial similarities southeastern Anatolia and its adjacent locations, it was between M. schidlovskii and M. socialis. Even though the determined that four species (M. socialis, M. guentheri, three taxa have the same karyotype (2n = 60), M. anatolicus M. cfr. Irani, and M. elbeyli sp. nov.) are distributed in the and M. schidlovskii have more marked distinctive cranial peculiarities than those of M. cfr. irani (Kefelioğlu and area (Figure 1). The habitat preference of M. guentheri Kryštufek, 1999; Kryštufek and Kefelioğlu, 2001b; Yiğit was found to be different as indicated by Çolak et al. et al., 2006b; Kryštufek et al., 2009, 2010). However, the (1997), Yiğit and Çolak (2002), and Yiğit et al. (2012). karyotypes of M. irani were reported to be 2n = 60 and 64 The other two species (M. elbeyli sp. nov. and M. cfr. irani) by Zima and Kral (1984) and 2n = 62 by Golenishchev et al. are usually captured in the same type of habitat (semidry (2002), and these findings emphasize the current taxonomic grain fields and steppe), but no sympatric occurrence conflict between M. irani and M. cfr. irani (Table 2). was determined. Kryštufek and Kefelioğlu (2001b) stated The morphological examinations of our specimens that M. irani has pale and sandy buff dorsal color and indicate the cryptic differences in the dorsal coloration also pointed out the cranial differences between the type between M. elbeyli sp. nov. (previously identified as M. series of M. irani and other Iranian specimens of M. irani irani by Çolak et al., 1997) and M. cfr. irani (Mardin such as bullae lengths, the zygomatic arches, and the specimens); the first is ochreous and the second incisive foramina. They also suggested that M. irani is an cinnamon buff in dorsal colorations. M. elbeyli sp. nov. independent species known solely from its type locality. also karyologically differs from M. cfr. irani recorded at Astonishingly, Kryštufek et al. (2009, 2010) extended M. Balkusan (Ermenek) by Kryštufek et al. (2009). Apart irani’s distribution to the Mediterranean coast of southern from these, the specimens (N = 3) captured around Turkey (Figure 1), describing a new subspecies, Microtus Mardin Province with 2n = 60 were identified as M.

A B X Y Figure 4. The metaphase plate (A) and karyotype (B) of the type specimen of M. elbeyli sp. nov. 2n = 46, NF = 50, NFa = 46.

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Table 2. The karyotype of Microtus species from Turkey.

Species Locality 2n NF NFa X Y Reference Velikaköprüsü 52 60 56 M M Çolak et al., 1997b Thrace 52 60 56 M M Macholan et al., 2001 1 M. subterraneus Akçaalan 54 60 56 M A Çolak et al., 1997b Anatolia 54 60 56 SM A Macholan et al., 2001 Meryemana 54 60 56 ST - Çolak et al. 1997b 2 M. majori Anatolia 54 60 56 SM A Macholan et al., 2001 3 M. dahgestanicus Bağdasan, Handere 54 58 54 SM Y Kryštufek and Vohralík, 2005 4 M. socialis Erzurum 62 62 60 A A Kefelioğlu, 1995; Kefelioğlu and Kryštufek, 1999 M. irani Balkusan 60 60 58 A A Kryštufek et al., 2010 5 M. cfr. irani Kilis 46 50 46 M M Çolak et al., 1997 6 M. elbeyli sp. nov. Kilis 46 50 46 SM A This study 7 M. schidlovskii Özalp, Yüksekova 60 60 58 A A Yiğit et al., 2006 Anatolia 54 56 52 A A Kefelioğlu, 1995; Çolak et al., 1997b 8 M. guentheri Anatolia 54 58 54 SM A Çolak et al., 1997b 9 M. hartingi Thrace 54 56 52 M A Kefelioğlu, 1995 Amasya, Konya 48 50 46 M SM/A Kefelioğlu and Kryštufek, 1999; Şekeroğlu et al., 2011 10 M. dogramacii Amasya 48 52 48 M SM/A Kefelioğlu and Kryštufek, 1999; Şekeroğlu et al., 2011 Amasya 48 54 50 M SM/A Kefelioğlu and Kryštufek, 1999 Cihanbeyli 60 62 60 A SM Kefelioğlu and Kryštufek, 1999 11 M. anatolicus Antalya 60 60 58 A A Yavuz et al. 2009 Şavşat 46 71 67 M A Kefelioğlu, 1995 12 M. obscurus Şavşat 46 71 67 M - Yorulmaz et al., 2013 13 M. levis Anatolia 54 56 54 A A Kefelioğlu, 1995; Arslan and Zima, 2014 cfr. irani and have different skull structures with curved Nomenclatural acts: This work and the nomenclatural acts braincase with ventrally enlarged bullae rather than typical it contains have been registered in ZooBank. The ZooBank smooth and shallow braincase of Anatolian specimens of Life Science Identifier (LSID) for this publication is: http:// M. socialis. M. cfr. irani recorded from Balkusan (Ermenek) zoobank.org/urn:lsid:zoobank.org:pub:56024C79-A2C6- was also reported to be different from the type series of true 461F-97D8-DECCCF050E18 M. irani from Shiraz (Iran) (Kryštufek et al., 2009, 2010). However, the cranial peculiarities of the Mardin specimens Acknowledgement are consistent with the given characteristics of M. cfr. irani This research was partly sponsored by TÜBİTAK (the by Kryštufek et al. (2009) and support the idea of its cryptic Scientific and Technological Research Council of Turkey, distribution through southeastern Anatolia to the west. Thus, project no: 109T593, TBAG/U113) and by the Research Fund this taxon also needs further investigation for taxonomic of Ankara University (project no: 98050302). We thank Dr B confirmation or to be assigned to another new species. Çoban (BEUN) for linguistic revision.

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