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Turkish Journal of Zoology Turk J Zool(2016) 40: 73-79© TÜBİTAKdoi:10.3906/zoo-1404-19

A new species of voles, Microtus elbeyli sp. nov., from Turkey with taxonomicoverview of social voles distributed in southeastern Anatolia

Nuri YİĞİT1, Ercüment ÇOLAK1, Mustafa SÖZEN2

1Department of Biology, Faculty of Science, Ankara University, Ankara, Turkey 2Department of Biology, Faculty of Arts and Sciences, Bülent Ecevit University, Zonguldak, Turkey

* Correspondence: spalaxtr@hotmail.com

1. IntroductionVoles in the genus Microtus were represented by 12 species in Turkey (Yiğit et al., 2006b; Kryštufek and Vohralík, 2009). Two of these species are endemic to Turkey and distributed mainly in Central Anatolia and the inner region of Antalya Province in Mediterranean Anatolia (Kryštufek and Kefelioğlu, 1999, 2001b; Yiğit et al., 2006b; Yavuz et al., 2009, 2011; Şekeroğlu et al., 2011). Three out of these 12 vole species are distributed throughout southeastern Anatolia and close localities in Syria including M. socialis, M. guentheri, and M. irani (Çolak et al., 1997; Shebab and Cherabi, 2006; Yiğit et al., 2006a).

Microtus irani Thomas, 1921 was originally described from Shiraz (Iran) and was also recorded from several localities in eastern Turkey (Kock et al., 1972; Morlok, 1978; Kock and Nader, 1983). More recently Çolak et al. (1997) recorded M. cfr. irani (2n = 46) from Kilis in southeastern Turkey, and the type series of M. irani from Shiraz (Iran) was redescribed and the differences between the type series and western Iranian specimens were pointed out by comparing western Iranian and Turkish specimens by Kryštufek and Kefelioğlu (2001).

The diploid numbers of chromosomes of M. irani were reported to be from 2n = 60 to 64 by Zima and Kral (1984) and 2n = 62 by Golenishchev et al. (2002). After the

record of M. irani by Çolak et al. (1997), another diploid chromosome number (2n = 60) for the same species was reported from southern Turkey by Kryštufek et al. (2009).

Up to now, species of social voles distributed in southeastern Turkey have remained doubtful, especially for M. cfr. irani with 2n = 46 (Çolak et al., 1997; Kryštufek and Kefelioğlu, 2001b; Kryštufek et al., 2009; 2010).

The aim of the present research is to reevaluate specimens previously recorded as M. cfr. irani by Çolak et al. (1997) based on its morphological and karyological features and to clarify the taxonomic status of these specimens.

2. Materials and methodsLarge numbers of social vole specimens were collected from Anatolia, including southeastern Turkey, between 1993 and 2012. The specimens from the southeastern and eastern parts of Anatolia were taken under evaluation in order to solve taxonomical problems. The sampling localities are shown in Figure 1. Apart from the specimens from southeastern Turkey, the specimens from Muş Province were taken into consideration in order to compare them with the specimens from southeastern Anatolia. The specimens were karyotyped to confirm species identification; thus, specimens were karyologically identified and were assigned to taxa as follows:

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, taxonomy, morphology, distribution, new species, Turkey

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

Research Article

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Microtus socialis, 2n = 62 (Muş Province), Microtus guentheri, 2n = 54 (type locality, Türkoğlu/

Kahramanmaraş),Microtus cfr. irani, 2n = 60 (this species was previously

recorded from Ermenek town by Kryštufek et al. (2009) and was recorded from Mardin Province in the present study; see Figure 1),

Microtus sp. with 2n = 46 (Kilis Province). We examined five specimens of M. socialis, ten of M.

guentheri, three of M. irani, and fifteen of the 2n = 46 form that were previously identified as M. cfr. irani by Çolak et al. (1997).

The occlusal patterns of molar teeth were evaluated according to Niethammer and Krapp (1982). The karyotype analysis was achieved by using the conventional bone marrow technique. The external measurements were taken from fresh specimens in the field and from each skull in the laboratory with a caliper accurate to the nearest 0.05 mm. Abbreviations are as follows: TbL = total body length, TL = tail length, HfL = hindfoot length, EL = ear length, W = weight. The skins and skulls of specimens examined were deposited in the Biology Department at Ankara University.

3. Results and discussionMicrotus elbeyli sp. nov.

Holotype: An adult male (collection number: 2919) held in the Zoology Museum of the Biology Department at Ankara University.

Type locality: 1 km NW of Karacaören village of Kilis Province in southeastern Turkey.

Diagnosis: External measurements (mm) and weight (g) of holotype; TbL = 135, TL = 21, HfL = 18, EL = 12, and W = 36. Some cranial measurements (mm) of holotype: occipitonasal length is 27.6, zygomatic breadth 16.5, basal length 25, nasal length 7.7, width of braincase 12.16, height of braincase with bullae 10.4, diastema length 9.0, palatal length 14.6, mandible length 16.86 (Table 1). The dorsal color is generally ochreous and slightly paler on sides. Ventral fur is pale buff with dark gray bases. There is a prominent delineation line between flanks and belly. Upper and ventral hair of feet are pale buff. The skull is slender with comparatively smooth brain case (Figure 2). M2 in all specimens was found to be the agrestis morphotype. The diploid number of chromosomes is 46 with 50 chromosomal arms.

Etymology: Elbeyli is a town of Kilis Province where most of the specimens were collected.

Description: The 15 examined specimens with 2n = 46 and ochreous dorsal color were captured from two different locations in southeastern Turkey (Figure 1). However, the dorsal pelage was found to be exceptionally dark brownish in a few specimens. The dorsal colors of our specimens were markedly different from M. guentheri but slightly different from M. cfr. irani with 2n = 60 from 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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morphological structures of specimens were drawn and given in our previous work (Çolak et al., 1997). The skull structures of these new specimens have some differences from M. cfr. irani and M. guentheri. Even though the skull is similar to that of M. guentheri, the sharp slope of the supraoccipital region in the braincase and mandible

morphology are the main differences (Figure 2). The braincase is smoother than those of M. guentheri and M. cfr. irani and is not shallow as in M. socialis. Apart from these differences, the nasal area in M. guentheri is markedly bent down compared to the other two species. The parietal bones of M. irani are narrow and exo-occipital

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

2919 ♂ Holotype Min–max n Mean ±SD

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

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condyles are almost visible in the dorsal aspect of skull. Incisive foramina do not project beyond the M1. The ventral parts of tympanic bullae are enlarged and are more marked than in M. socialis but are almost similar to those of M. guentheri. The mandible is slender and its coronoid and angular processes are different from other species in the manner of markedly separating the coronoid process

from the condyloid process. The skull is slender with a comparatively smooth brain case and  the suprameatal triangle is markedly a more rounded oval than in the other species.

Dentition: The occlusal molar patterns of M2 are found to be the non-agrestis morphotype and M3 patterns were observed as 50% normal, 29% complex, and 21% duplicate

Figure 2. Skulls (dorsal and lateral views) and mandible (labial views) of species: A) M. elbeyli, B) M. cfr. irani, C) M. guentheri.

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.

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forms (Figure 3). M2 patterns of all other specimens of M. guentheri and M. cfr. irani were found to be the non-agrestis morphotype; therefore, it was concluded that M2 patterns are not distinctive among taxa. Kefelioğlu (1995) reported 40% non-agrestis morphotype for M. socialis in Turkey. Similarly, the agrestis morphotype was observed in high frequencies in M. socialis specimens of Turkish, Caucasian, Lebanese, Syrian, and Iranian origin (Kefelioğlu and Kryštufek, 1999; Kryštufek and Kefelioğlu, 2001a). In the type specimen of M. irani, the M2 occlusal molar pattern was also reported as the agrestis morphotype in the figure given by Kryštufek and Kefelioğlu (2001b).

Taxonomic remarks: According to morphological and karyological examinations of the specimens captured from southeastern Anatolia and its adjacent locations, it was determined that four species (M. socialis, M. guentheri, M. cfr. Irani, and M. elbeyli sp. nov.) are distributed in the area (Figure 1). The habitat preference of M. guentheri was found to be different as indicated by Çolak et al. (1997), Yiğit and Çolak (2002), and Yiğit et al. (2012). The other two species (M. elbeyli sp. nov. and M. cfr. irani) are usually captured in the same type of habitat (semidry grain fields and steppe), but no sympatric occurrence was determined. Kryštufek and Kefelioğlu (2001b) stated that M. irani has pale and sandy buff dorsal color and also pointed out the cranial differences between the type series of M. irani and other Iranian specimens of M. irani such as bullae lengths, the zygomatic arches, and the incisive foramina. They also suggested that M. irani is an independent species known solely from its type locality. Astonishingly, Kryštufek et al. (2009, 2010) extended M. irani’s distribution to the Mediterranean coast of southern Turkey (Figure 1), describing a new subspecies, Microtus

irani karamani, based on phylogenetic analyses of social vole specimens.

Karyology: The karyotype of five specimens from the Microtus population in 2n = 46 from Kilis was described by Çolak et al. (1997) as 2n = 46, NF = 50, and NFa = 46. The X chromosome was large metacentric and the Y chromosome was the smallest metacentric (Figure 4).

In the phylogenetic analyses of Kryštufek et al. (2009), M. anatolicus with 2n = 60, M. irani with 2n = 60, and M. socialis with 2n = 62 were grouped into the same cluster, indicating the close genetic resemblance. In our previous study (Yiğit et al., 2006), the specimens with 2n = 60 were also found and identified as Microtus schidlovskii in eastern Turkey, and we also pointed out the cranial similarities between M. schidlovskii and M. socialis. Even though the three taxa have the same karyotype (2n = 60), M. anatolicus and M. schidlovskii have more marked distinctive cranial peculiarities than those of M. cfr. irani (Kefelioğlu and Kryštufek, 1999; Kryštufek and Kefelioğlu, 2001b; Yiğit et al., 2006b; Kryštufek et al., 2009, 2010). However, the karyotypes of M. irani were reported to be 2n = 60 and 64 by Zima and Kral (1984) and 2n = 62 by Golenishchev et al. (2002), and these findings emphasize the current taxonomic conflict between M. irani and M. cfr. irani (Table 2).

The morphological examinations of our specimens indicate the cryptic differences in the dorsal coloration between M. elbeyli sp. nov. (previously identified as M. irani by Çolak et al., 1997) and M. cfr. irani (Mardin specimens); the first is ochreous and the second cinnamon buff in dorsal colorations. M. elbeyli sp. nov. also karyologically differs from M. cfr. irani recorded at Balkusan (Ermenek) by Kryštufek et al. (2009). Apart from these, the specimens (N = 3) captured around Mardin Province with 2n = 60 were identified as M.

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

A BX Y

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cfr. irani and have different skull structures with curved braincase with ventrally enlarged bullae rather than typical smooth and shallow braincase of Anatolian specimens of M. socialis. M. cfr. irani recorded from Balkusan (Ermenek) was also reported to be different from the type series of true M. irani from Shiraz (Iran) (Kryštufek et al., 2009, 2010). However, the cranial peculiarities of the Mardin specimens are consistent with the given characteristics of M. cfr. irani by Kryštufek et al. (2009) and support the idea of its cryptic distribution through southeastern Anatolia to the west. Thus, this taxon also needs further investigation for taxonomic confirmation or to be assigned to another new species.

Nomenclatural acts: This work and the nomenclatural acts it contains have been registered in ZooBank. The ZooBank Life Science Identifier (LSID) for this publication is: http://zoobank.org/urn:lsid:zoobank.org:pub:56024C79-A2C6-461F-97D8-DECCCF050E18

Acknowledgement This research was partly sponsored by TÜBİTAK (the Scientific and Technological Research Council of Turkey, project no: 109T593, TBAG/U113) and by the Research Fund of Ankara University (project no: 98050302). We thank Dr B Çoban (BEUN) for linguistic revision.

Table 2. The karyotype of Microtus species from Turkey.

Species Locality 2n NF NFa X Y Reference

1 M. subterraneus

Velikaköprüsü 52 60 56 M M Çolak et al., 1997b

Thrace 52 60 56 M M Macholan et al., 2001

Akçaalan 54 60 56 M A Çolak et al., 1997b

Anatolia 54 60 56 SM A Macholan et al., 2001

2 M. majoriMeryemana 54 60 56 ST - Çolak et al. 1997b

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

5M. irani Balkusan 60 60 58 A A Kryštufek et al., 2010

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

8 M. guentheriAnatolia 54 56 52 A A Kefelioğlu, 1995; Çolak et al., 1997b

Anatolia 54 58 54 SM A Çolak et al., 1997b

9 M. hartingi Thrace 54 56 52 M A Kefelioğlu, 1995

10 M. dogramacii

Amasya, Konya 48 50 46 M SM/A Kefelioğlu and Kryštufek, 1999; Şekeroğlu et al., 2011

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

11 M. anatolicusCihanbeyli 60 62 60 A SM Kefelioğlu and Kryštufek, 1999

Antalya 60 60 58 A A Yavuz et al. 2009

12 M. obscurusŞavşat 46 71 67 M A Kefelioğlu, 1995

Şavşat 46 71 67 M - Yorulmaz et al., 2013

13 M. levis Anatolia 54 56 54 A A Kefelioğlu, 1995; Arslan and Zima, 2014

ReferencesÇolak E, Yiğit N, Kıvanç E, Sözen M (1997a). Distribution and taxonomic

status of the genus Microtus (Mammalia: Rodentia) in southeastern Turkey. Isr J Zool 43: 391–396.

Çolak E, Yiğit N, Sözen M, Özkurt Ş (1997b). A study on taxonomic status of Microtus subterraneus (de Selys Longchamps, 1836) and Microtus majori Thomas, 1906 (Mammalia: Rodentia) in Turkey. Turk J Zool 22: 119–129 (in Turkish with English summary).

79

YİĞİT et al. / Turk J Zool

Golenishchev FN, Sablina VO, Borodin PM, Gerasimov S (2002). Taxonomy of voles of the subgenus Sumeriomys Argyropulo, 1933 (Rodentia, Arvicolinae, Microtus). Russian Journal of Theriology 1: 43–55.

Kefelioğlu H, Kryštufek B (1999). The taxonomy of Microtus socialis group (Rodentia: Microtinae) in Turkey, with the description of a new species. J Nat Hist 33: 289–303.

Kock D, Malec F, Storch G (1972). Rezente und subfossile Kleinsauger aus dem Vilayet Elazig, Ostanatolien. Z Säugetierkd 37: 204–229 (in German).

Kock D, Nader IA (1983). Pygmy shrew and rodents from the Near East (Mammalia: Soricidae, Rodentia). Senck Biol 64: 13–23.

Kryštufek B, Bužan EV, Vohralík V, Zareie R, Özkan B (2009). Mitochondrial cytochrome b sequence yields new insight into the speciation of social voles in south-west Asia. Biol J Linn Soc 98: 121–128.

Kryštufek B, Kefelioğlu H (2001a). The social vole Microtus socialis in the Near East. Mammal Rev 31: 229–237.

Kryštufek B, Kefelioğlu H (2001b). Redescription and species limits of Microtus irani Thomas, 1921, and description of a new social vole from Turkey (Mammalia: Arvicolinae). Bonn Zool Beitr 50: 1–14.

Kryštufek B, Vohralík V (2009). Mammals of Turkey and Cyprus (Rodentia II: Cricetinae, Muridae, Spalacidae, Calomyscidae, Capromyidae, Hystricidae, Castoridae). Koper, Slovenia: Univerza na Primorskem.

Kryštufek B, Vohralík V, Zima J, Koubinova D, Bužan EV (2010). A new subspecies of the Iranian Vole, Microtus irani Thomas, 1921, from Turkey. Zool Middle East 50: 11–20.

Macholan M, Filippucci MG, Zima J (2001). Genetic variation and zoogeography of pine voles of the Microtus subterraneus/majori group in Europe and Asia Minor. J Zool London 255: 31–42.

Morlok WF (1978). Nagetiere aus der Turkei (Mammalia: Rodentia). Seckenberg Biol 59: 155–162 (in German).

Niethammer J, Krapp F (1982). Handbuch der Säugetiere Europas, Band 2/1. Wiesbaden, Germany: Akademische Verlagsgesellschaft.

Şekeroğlu ZA, Kefelioğlu H, Şekeroğlu V (2011). Cytogenetic characteristics of Microtus dogramacii (Mammalia: Rodentia) around Amasya, Turkey. Turk J Zool 35: 593–598.

Shebab AH, Charabi MA (2006). Food of the barn owl Tyto alba in the Yahmool Area, Northern Syria. Turk J Zool 30: 175–179.

Yavuz M, Öz M, Albayrak İ (2009). Two new locality records extend the distribution of Anatolian vole, Microtus anatolicus Kryštufek and Kefelioglu, 2002 (Mammalia: Rodentia) into Antalya Province in Turkey. North-West J Zool 5: 364–369.

Yavuz M, Öz M, Albayrak İ (2011). Bir Anadolu endemiği; Anadolu tarla faresi Microtus anatolicus’nin ekolojik tercihleri. Ekoloji 20: 59–6 (in Turkish).

Yiğit N, Çolak E (2002). On the distribution and taxonomic status of Microtus guentheri (Danford and Alston, 1880) and Microtus lydius Blackler, 1916 (Mammalia: Rodentia) in Turkey. Turk J Zool 26: 197–204.

Yiğit N, Çolak E, Sözen M, Karataş A (2006). Rodents of Türkiye. Ankara, Turkey: Meteksan Co.

Yiğit N, Markov G, Çolak E, Kocheva M, Saygılı F, Yüce D, Çam P (2012). Phenotypic features of the “guentheri” group vole (Mammalia: Rodentia) in Turkey and the Southeast Bulgaria: evidence for its taxonomic detachment. Acta Zool Bulgar 64: 23–32.

Yiğit N, Moradi MG, Çolak E, Özkurt Ş, Bulut Ş, Kankılıç T, Çolak R (2006). The Karyotypes of Some Rodent Species (Mammalia: Rodentia) from Eastern Turkey and Northern Iran with a New Record, Microtus schidlovskii Argyropulo, 1933, from Eastern Turkey. Turk J Zool 30: 459–464.

Yorulmaz T, Zima J, Arslan A, Kankılıç T (2013). Variations in the C-heterochromatin and AgNOR distribution in the common vole (Microtus arvalis sensu lato) (Mammalia: Rodentia). Arch Biol Sci Belgrade 65: 989–995.

Zima J, Kral B (1984). Karyotypes of European mammals II. Acta Sc Nat Brno 18: 1–62.