Journal of Asia-Pacific Biodiversity 8 (2015) 233e237

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Short communication Morphological and morphometric characterization of the new records of the East European vole ( levis Miller, 1908) from northeast Iran

Fatemeh Ghorbani a,*, Zeinolabedin Mohammadi a, Jamshid Darvish a,b, Haji Gholi Kami c, Roohollah Siahsarvie b,d a Department of Biology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, Iran b Rodentology Research Department (RRD), Institute of Applied (IAA), Ferdowsi University of Mashhad, Mashhad, Iran c Department of Biology, Faculty of Sciences, Golestan University, Gorgan, Iran d Institut des Sciences de l’Evolution, Université de Montpellier, Montpellier, Cedex, France article info abstract

Article history: Thirteen specimens of Microtus levis were collected from Golestan province, northeast Iran. The speci- Received 12 March 2015 mens were studied based on their external characters, skull and dental morphology, and specially Received in revised form karyology. Specimens of M. levis from the northeast of Iran were also compared with other species of the 13 July 2015 arvalis group from Iran and specimens of M. levis from Turkey. The specimens demonstrated that 2n ¼ 54 Accepted 18 July 2015 and fundamental number FN ¼ 54. The karyological results were similar between specimens from Available online 29 July 2015 northeast Iran and those from Turkey, but they were different from specimens of Europe. In addition, the morphometric characters of M. levis, including head and body length (mean ¼ 105.77 7.53), length of Keywords: ¼ ¼ Hyrcanian region condylobasal (mean 24.96 0.97), length of bullae (mean 6.57 0.34), and dental characters con- ¼ ¼ Microtus levis sisting of maxillary tooth row (mean 6.17 0.25) and mandibular tooth row (mean 5.60 0.33), were morphometry different from those of other species of the arvalis group. northeast Iran Copyright Ó 2015, National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA). Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/).

Introduction Indeed, there is a nomenclature problem in the Microtus arvalis species group to which M. levis is attributed. Ognev (1950) recorded The East European vole (Microtus levis Miller, 1908) was first M. levis as Microtus arvalis rossiaemeridionalis and Microtus arvalis recorded from the Carpathian Mountains in Romania. Musser and caspicus. Ondrias (1966) reported it as Microtus epiroticus from Carleton (2005) proposed the distribution range of this species Greece, and Mejer et al (1972) described it under the name Microtus from south Finland and the Baltic region to west Siberia, and from subarvalis. Moreover, Corbet (1978) synonymized all these names, Ukraine in the north through Caucasus toTurkey in the south. Musser except 54-chromosome M. subarvalis, with M. arvalis. Finally, Meyer and Carleton (2005) expressed doubt about assigning the voles of et al (1996) considered M. levis and M. arvalis as two sympatric northeast Iran (previously described as Microtus mystacinus De Fili- sibling species. ppi,1865) to M. levis by Lay (1967) and Malygin and Yatsenko (1986). Jaarola et al (2004) confirmed the closeness of these two spe- Karami et al (2008) stated that several specimens from Arasbaran cies, showing a divergence of only 6e8% in cytochrome b. Even Wildlife Refuge in the northwest of Iran, preserved in the Museum of though, these sibling species have different diploid numbers A. Koenig, Bonn, correspond morphologically to M. levis but empha- (M. arvalis,2N ¼ 46; M. levis,2N ¼ 54). Moreover, they can be sized that the voles of the region should be studied karyologically. discriminated based on their allozyme profile, hemoglobin elec- trophoresis (Dobrokhotov and Malygin 1982; Zakijan et al 1984; Suchentrunk et al 1998), and sequencing of mitochondrial DNA * Corresponding author. Tel.: þ98 91117 04728, þ98 17122 21886; fax: þ98 51187 and nuclear DNA genes (Baker et al 1996; DeWoody 1999; 62019. DeWoody et al 1999; Jaarola et al 2004; Triant and DeWoody E-mail address: [email protected] (F. Ghorbani). Peer review under responsibility of National Science Museum of Korea (NSMK) and 2006); they are nearly indistinguishable, according to classic Korea National Arboretum (KNA). morphological studies (Malygin 1983; Markova et al 2009). Masing http://dx.doi.org/10.1016/j.japb.2015.07.002 pISSN2287-884X eISSN2287-9544/Copyright Ó 2015, National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA). Production and hosting by Elsevier. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 234 F Ghorbani et al. / Journal of Asia-Pacific Biodiversity 8 (2015) 233e237

(1999) proposed seven distinctive cranial characters to distinguish (Figure 1). Thirteen specimens were captured using live traps. M. levis from M. arvalis. However, Krystufek and Vohralik (2005) Standard vouchers of the specimens (skins, skulls, and tissues) challenged his idea after studying specimens from Turkey. They were deposited in the Zoology Museum of Ferdowsi University of mentioned that recognition of these species based on morphology Mashhad, Mashhad, Iran. only, without karyological or molecular study, is inaccurate. However, some differences in frequencies of the molar charac- Morphological and karyological study ters are present (Zagorodnyuk 1991; Mazeikyte et al 1999; Uhlíková 2004; Markova et al 2009) and applying canonical craniometric Five standard external, and 12 cranial and dental characters function (Markov et al 2009) were suggested to distinguish were measured using a vernier caliper, accurate to the nearest M. arvalis and M. levis as M. rossiaemeridionalis. Hotzi et al (2008) 0.05 mm (Insize Inc., Suzhou New District, China), or a measuring also separated these two species using the results of discriminant microscope, accurate to 0.001 mm (Nikon MM40 Measuring Mi- analysis based on morphological characters. croscope; Used Microscope OME-Top Systems Co., Ltd, New Taipei To date, nine species of the genus Microtus have been reported City, Taiwan; for details, see Krystufek and Vohralik 2005). from Iran, including M. arvalis (Pallas, 1778); Microtus transcaspicus Morphological studies of dental and cranial characters were carried Satunin, 1905; Microtus socialis (Pallas, 1773); Microtus irani out using a research stereomicroscope (Olympus SZH10; Olympus, Thomas, 1921; Microtus qazvinensis Golenishchev, Malikov, Nazari, Tokyo, Japan) equipped with a camera lucida (Olympus). Chromo- Vaziri, Sablina et Polyakov, 2002; Microtus paradoxus (Ognev et somes were prepared directly from the bone marrow of colchicine- Heptner, 1928); Microtus schelkovnikovi (Satunin, 1907); Microtus treated (Ford and Hamerton 1956). Thirty slides and at majori (Thomas, 1906), Microtus obscurus (Eversmann, 1841); the least 60 metaphase cells were studied for preparing idiograms. The occurrence of M. levis Miller, 1908, besides Microtus guentheri mean value and standard errors of characters were estimated using (Danford et Alston, 1880), has still been under debate (Karami et al SPSS version 16 (SPSS Inc., Chicago, IL, USA; for descriptions of 2008; Darvish et al 2014). Considering the important role of kary- characters, see Krystufek and Vohralik 2005; Yavuz et al 2011). ological studies in the identification of species of the genus Microtus, karyology was applied for identification of the specimens Results of the genus Microtus from northern Alborz, in addition to morphometric and morphological investigations. This study is the Diagnostic characters first record of the East European vole (M. levis) from the Hyrcanian region in northeast Iran. Pelage is yellowish brown; flanks are yellowish brown and demarcation along flanks is relatively clear; the underpart is dirty Materials and methods white with a yellowish tint between forelimbs; tail is well haired and slightly bichromatic; the tail is over 31% head and body length Sampling (31e39%; Table 1); and hind feet are hairy above and with six plantar pads. Dorsal profile of the skull is straight; posterior inner Sampling was conducted at high elevations from 1800 m (above parts of orbits are angular in adults but rounded in juveniles; sea level; 364102200 N; 543400500 E) to 2300 m (above sea level; posterior section of bony palates are with two large isolated palatal 363901800 N; 543402600 E) of the northern slopes of the Alborz pits and a bony bridge between them; incisive foramens are rather Mountains, which includes the Hyrcanian region, northeast Iran broad, terminating on a line with first molars; in juveniles,

Figure 1. Collection site of Microtus levisdHyrcanian region, northeast Iran (black circle). F Ghorbani et al. / Journal of Asia-Pacific Biodiversity 8 (2015) 233e237 235

Table 1. Mean SE, minimum and maximum values for external and cranial measurements, and karyological characters of four Microtus species from the north and northeast Iran.

Variables Microtus levis from Iran M. levis from Turkey Microtus obscurus from Iran Microtus transcaspicus from Iran N ¼ 13 N ¼ 61 N ¼ 10 N ¼ 11

Mean SE Min Max Mean SE Min Max Mean SE Mean SE

W 21.22 3.17 18.20 26.60 38.89 1.35 21.45 54.34 e 38.8 8.7 HBL 105.77 7.53 92 119 122.15 1.7 110.8 138.5 94.56 11.85 145.9 12.4 TL 36.08 2.69 33 42 34.17 0.66 23.35 42.56 85.66 4.04 34.63 5.92 FL 16.92 0.49 16 18 19.96 0.14 18.21 21.81 21.33 0.58 20.09 0.7 EL 12.31 1.38 10 15 14.07 0.15 12.01 15.97 14.16 1.53 7.82 1.60 CL 24.96 0.97 23.35 26.25 25.19 0.20 22.61 28.02 23.6 1.41 e RL 14.97 0.70 13.90 15.95 e eee e OL 24.60 0.96 23.15 26.30 25.73 0.21 23.12 28.38 23.29 1.21 29.36 1.82 ZB 14.15 0.60 13 15.05 14.37 0.12 12.81 15.85 13.11 1.06 15.92 0.39 BB 12.07 0.40 11.30 12.65 eee11.62 12.55 0.46 IC 3.63 0.21 3.15 3.95 3.60 0.02 3.30 3.87 3.54 0.14 3.95 0.16 RH 6.54 0.33 6 7 eee5.84 e WR 4.92 0.23 4.50 5.25 eee3.95 0.16 e BU 6.57 0.34 6 7.10 6.74 0.05 6.10 7.40 7.44 0.51 e LLM 14.80 0.56 13.75 15.60 14.62 0.10 13.30 16.08 13.54 0.56 18.26 0.50 MnT 5.60 0.33 5.16 6.22 eee5.23 0.138 7.00 0.16 MT 6.17 0.25 5.65 6.55 6.14 0.05 5.50 6.73 5.32 0.204 7.01 0.26 2n 54 54 e 52 FN 54 54 e 54 Tail color Slightly bicolored Bicolored Bicolored Bicolored Nipples 4 pairs e 4 pairs 4 pairs Hind feet plantar pads 6 6 6 6

Measurements are in millimeters and weights in grams. Data for M. transcaspicus were taken from the work of Darvish et al (2006), for M. levis from Turkey from Yavuz et al (2011), and for M. obscurus from Darvish et al (2014). BB ¼ breadth of braincase; BU ¼ length of bullae; CL ¼ condylobasal length of skull; EL ¼ ear length; FL ¼ hind foot length; FN ¼ fundamental number; HBL ¼ head and body length; IC ¼ interorbital constriction; LLM ¼ length of lower mandible; MnT ¼ mandibular tooth-row length; MT ¼ maxillary tooth-row length; OL ¼ occipitonasal length of skull; RH ¼ height of rostrum; RL ¼ length of rostrum; SE ¼ standard error; TL ¼ tail length; W ¼ weight; WR ¼ width of rostrum; ZB ¼ zygomatic breadth. interparietal is pentagonal and its posterior edge is rather straight, Karyological features but in fully grown specimens, interparietal is nearly hexagonal (Figure 2). Karyological study was performed on two males and three fe- Incisors are yellowish; lower M.1 has a pot-shaped anterior loop, males. The diploid number of chromosomes was 2n ¼ 54, funda- one open and two closed labial triangles; it even has one open and mental number was FN ¼ 54, and the number of autosomal arms three nearly closed lingual triangles and a posterior loop found in this study was FNa ¼ 52. The autosomal set contains 54 (Figures 3B and 3C). Upper M3, which has an anterior loop, is acrocentrics. The X chromosome is a large acrocentric, and the Y complex, especially at the posterior side, with three or four lingual chromosome is a small acrocentric (Figure 5). re-entrant folds that the fourth one cuts slightly, if exists, and two or three slight re-entrant folds at labial side. These folds form one Discussion closed lingual triangle, two closed labial ones, and a small outer denticle on the wearing surface of the upper M3 (Figures 3A and 4). The East European vole (M. levis) lives in dense colonies in the These general patterns were observed in specimens, with some northern slopes of east Alborz. Relict Arcto-Tertiary Hyrcanian variations (Figures 3C and 4). forests form the main part of the vegetation cover in the region. The area is covered with Fagus orientalis, Acer laetum, and subalpine species Quercus macranthera and Quercus pubescens surrounded by Irano-Turanian flora (Browicz 1989; Klein and Lacoste 1996; Akhani et al 2010). Alborz and Zagros Mountains beside the Caspian Sea and Turkmenistan deserts (Misonne 1959) may constitute a sig- nificant barrier constraining migration of isolated populations of M. levis in the Hyrcanian forests. This isolation was reported for some small in the Hyrcanian region such as Glis glis (Naderi et al 2014), Crocidura suaveolens (Dubey et al 2007), and Crocidura caspica (Hutterer 2005), resulting in the origination of new lineages. M. levis is included in the arvalis group, which is discriminated from the socialis group of voles inhabiting Iran (M. irani, M. paradoxus, M. socialis, and M. qazvinensis) by six plantar pads on hind feet, different patterns of prismatic molar, and different karyological features (Musser and Carleton 2005; Siahsarvie et al 2008; Mohammadi et al 2013). It is also different from M. majori and M. schelkovnikovi, the majori group, in terms of different fundamental numbers of chromosomes, FN ¼ 54 in M. levis versus ¼ ¼ Figure 2. Skull of Microtus levis: A, dorsal view; B, ventral view; C, outside view of the FN 60 in M. majori (Baskevich 1997) and FN 62 in lower mandible. M. schelkovnikovi (Akhverdyan et al 1992); different molar patterns; 236 F Ghorbani et al. / Journal of Asia-Pacific Biodiversity 8 (2015) 233e237

same karyological results may indicate that the population of M. levis from the Hyrcanian region is closely related to that of M. levis from central Turkey. In the specimens of M. levis from Iran, the tail is longer (over 31% HB) than that of the specimens from Turkey (25% HB; Yavuz et al 2011). In general, the specimens from Iran show a lower average in measurements except for tail length, length of lower mandible, maxillary tooth-row length, and interorbital constriction, e.g. the condylobasal length of the specimens (mean ¼ 24.96 mm) is shorter than that of specimens from Turkey (mean ¼ 25.19 mm; Table 1). However, because of high rates of evolution and speciation in the genus Microtusdw30,000 years for each species, according to deduction from fossil records, 100,000 years based on molecular clock estimation (Repenning 1980; Chaline et al 1999; Brunet- Lecomte and Chaline 1991; Triant and DeWoody 2006)dand longtime separation of the colonies of M. levis in the Hyrcanian forests by three main barriers, mountainous Caucasus, Caspian Sea,

Figure 3. Dental pattern of Microtus levis: A, left upper tooth row; B, left lower tooth and Turkmenistan deserts (Misonne 1959), these isolated pop- row; C, variability of the left lower M.1 in M. levis. ulations should be further tested using molecular data.

Acknowledgments

Authorization for the experiments was given by the Department of Environment of Golestan Province, Iran (Permission Number: 125/6856; December 5, 2007). I (F. Ghorbani) would like to thank Professor Boris Krystufek from University of Primorska, Slovenia, who helped me identify specimens of Microtus.

References

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