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Morphological and morphometric characterization of the new records of the

East European vole (Microtus levis Miller, 1908) from northeastern Iran

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DOI: 10.1016/j.japb.2015.07.002

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Morphological and morphometric characterization of the new recordsof the East European vole (Microtus levis Miller, 1908) fromnortheast Iran

Fatemeh Ghorbani a,*, Zeinolabedin Mohammadi a, Jamshid Darvish a,b, Haji Gholi Kami c,Roohollah Siahsarvie b,d

aDepartment of Biology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, IranbRodentology Research Department (RRD), Institute of Applied Animal (IAA), Ferdowsi University of Mashhad, Mashhad, IrancDepartment of Biology, Faculty of Sciences, Golestan University, Gorgan, Irand Institut des Sciences de l’Evolution, Université de Montpellier, Montpellier, Cedex, France

a r t i c l e i n f o

Article history:Received 12 March 2015Received in revised form13 July 2015Accepted 18 July 2015Available online 29 July 2015

Keywords:Hyrcanian regionMicrotus levismorphometrynortheast Iran

* Corresponding author. Tel.: þ98 91117 04728, þ9862019.

E-mail address: biosys2050@gmail.com (F. GhorbaPeer review under responsibility of National Science MKorea National Arboretum (KNA).

http://dx.doi.org/10.1016/j.japb.2015.07.002pISSN2287-884X eISSN2287-9544/Copyright � 2015,This is an open access article under the CC BY-NC-ND

a b s t r a c t

Thirteen specimens of Microtus levis were collected from Golestan province, northeast Iran. The speci-mens were studied based on their external characters, skull and dental morphology, and speciallykaryology. Specimens of M. levis from the northeast of Iran were also compared with other species of thearvalis group from Iran and specimens of M. levis from Turkey. The specimens demonstrated that 2n¼ 54and fundamental number FN¼ 54. The karyological results were similar between specimens fromnortheast Iran and those from Turkey, but they were different from specimens of Europe. In addition, themorphometric characters of M. levis, including head and body length (mean¼ 105.77� 7.53), length ofcondylobasal (mean¼ 24.96� 0.97), length of bullae (mean¼ 6.57� 0.34), and dental characters con-sisting of maxillary tooth row (mean¼ 6.17� 0.25) and mandibular tooth row (mean¼ 5.60� 0.33), weredifferent from those of other species of the arvalis group.

Copyright � 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

The East European vole (Microtus levis Miller, 1908) was firstrecorded from the Carpathian Mountains in Romania. Musser andCarleton (2005) proposed the distribution range of this speciesfrom south Finland and the Baltic region to west Siberia, and fromUkraine in the north throughCaucasus toTurkey in the south.Musserand Carleton (2005) expressed doubt about assigning the voles ofnortheast Iran (previously described as Microtus mystacinus De Fili-ppi,1865) toM. levis by Lay (1967) andMalygin and Yatsenko (1986).Karami et al (2008) stated that several specimens from ArasbaranWildlife Refuge in the northwest of Iran, preserved in theMuseumofA. Koenig, Bonn, correspond morphologically to M. levis but empha-sized that the voles of the region should be studied karyologically.

17122 21886; fax: þ98 51187

ni).useum of Korea (NSMK) and

National Science Museum of Korealicense (http://creativecommons.

Indeed, there is a nomenclature problem in the Microtus arvalisspecies group towhichM. levis is attributed. Ognev (1950) recordedM. levis as Microtus arvalis rossiaemeridionalis and Microtus arvaliscaspicus. Ondrias (1966) reported it as Microtus epiroticus fromGreece, andMejer et al (1972) described it under the nameMicrotussubarvalis. Moreover, Corbet (1978) synonymized all these names,except 54-chromosomeM. subarvalis, withM. arvalis. Finally, Meyeret al (1996) considered M. levis and M. arvalis as two sympatricsibling species.

Jaarola et al (2004) confirmed the closeness of these two spe-cies, showing a divergence of only 6e8% in cytochrome b. Eventhough, these sibling species have different diploid numbers(M. arvalis, 2N¼ 46; M. levis, 2N¼ 54). Moreover, they can bediscriminated based on their allozyme profile, hemoglobin elec-trophoresis (Dobrokhotov and Malygin 1982; Zakijan et al 1984;Suchentrunk et al 1998), and sequencing of mitochondrial DNAand nuclear DNA genes (Baker et al 1996; DeWoody 1999;DeWoody et al 1999; Jaarola et al 2004; Triant and DeWoody2006); they are nearly indistinguishable, according to classicmorphological studies (Malygin 1983; Markova et al 2009). Masing

(NSMK) and Korea National Arboretum (KNA). Production and hosting by Elsevier.org/licenses/by-nc-nd/4.0/).

F Ghorbani et al. / Journal of Asia-Pacific Biodiversity 8 (2015) 233e237234

(1999) proposed seven distinctive cranial characters to distinguishM. levis from M. arvalis. However, Kry�stufek and Vohralik (2005)challenged his idea after studying specimens from Turkey. Theymentioned that recognition of these species based on morphologyonly, without karyological or molecular study, is inaccurate.

However, some differences in frequencies of the molar charac-ters are present (Zagorodnyuk 1991;Ma�zeikyte et al 1999; Uhlíková2004; Markova et al 2009) and applying canonical craniometricfunction (Markov et al 2009) were suggested to distinguishM. arvalis and M. levis as M. rossiaemeridionalis. Hotzi et al (2008)also separated these two species using the results of discriminantanalysis based on morphological characters.

To date, nine species of the genus Microtus have been reportedfrom Iran, including M. arvalis (Pallas, 1778); Microtus transcaspicusSatunin, 1905; Microtus socialis (Pallas, 1773); Microtus iraniThomas, 1921; Microtus qazvinensis Golenishchev, Malikov, Nazari,Vaziri, Sablina et Polyakov, 2002; Microtus paradoxus (Ognev etHeptner, 1928); Microtus schelkovnikovi (Satunin, 1907); Microtusmajori (Thomas, 1906), Microtus obscurus (Eversmann, 1841); theoccurrence of M. levis Miller, 1908, besides Microtus guentheri(Danford et Alston, 1880), has still been under debate (Karami et al2008; Darvish et al 2014). Considering the important role of kary-ological studies in the identification of species of the genusMicrotus, karyology was applied for identification of the specimensof the genus Microtus from northern Alborz, in addition tomorphometric and morphological investigations. This study is thefirst record of the East European vole (M. levis) from the Hyrcanianregion in northeast Iran.

Materials and methods

Sampling

Sampling was conducted at high elevations from 1800 m (abovesea level; 36�4102200 N; 54�3400500 E) to 2300 m (above sea level;36�3901800 N; 54�3402600 E) of the northern slopes of the AlborzMountains, which includes the Hyrcanian region, northeast Iran

Figure 1. Collection site of Microtus levisdHyrc

(Figure 1). Thirteen specimens were captured using live traps.Standard vouchers of the specimens (skins, skulls, and tissues)were deposited in the Zoology Museum of Ferdowsi University ofMashhad, Mashhad, Iran.

Morphological and karyological study

Five standard external, and 12 cranial and dental characterswere measured using a vernier caliper, accurate to the nearest0.05 mm (Insize Inc., Suzhou New District, China), or a measuringmicroscope, accurate to 0.001 mm (Nikon MM40 Measuring Mi-croscope; Used Microscope OME-Top Systems Co., Ltd, New TaipeiCity, Taiwan; for details, see Kry�stufek and Vohralik 2005).Morphological studies of dental and cranial characters were carriedout using a research stereomicroscope (Olympus SZH10; Olympus,Tokyo, Japan) equipped with a camera lucida (Olympus). Chromo-somes were prepared directly from the bone marrow of colchicine-treated animals (Ford and Hamerton 1956). Thirty slides and atleast 60 metaphase cells were studied for preparing idiograms. Themean value and standard errors of characters were estimated usingSPSS version 16 (SPSS Inc., Chicago, IL, USA; for descriptions ofcharacters, see Kry�stufek and Vohralik 2005; Yavuz et al 2011).

Results

Diagnostic characters

Pelage is yellowish brown; flanks are yellowish brown anddemarcation along flanks is relatively clear; the underpart is dirtywhite with a yellowish tint between forelimbs; tail is well hairedand slightly bichromatic; the tail is over 31% head and body length(31e39%; Table 1); and hind feet are hairy above and with sixplantar pads. Dorsal profile of the skull is straight; posterior innerparts of orbits are angular in adults but rounded in juveniles;posterior section of bony palates are with two large isolated palatalpits and a bony bridge between them; incisive foramens are ratherbroad, terminating on a line with first molars; in juveniles,

anian region, northeast Iran (black circle).

Table 1.Mean� SE, minimum and maximum values for external and cranial measurements, and karyological characters of fourMicrotus species from the north and northeastIran.

Variables Microtus levis from IranN¼ 13

M. levis from TurkeyN¼ 61

Microtus obscurus from IranN¼ 10

Microtus transcaspicus from IranN¼ 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� 8.7HBL 105.77� 7.53 92 119 122.15� 1.7 110.8 138.5 94.56� 11.85 145.9� 12.4TL 36.08� 2.69 33 42 34.17� 0.66 23.35 42.56 85.66� 4.04 34.63� 5.92FL 16.92� 0.49 16 18 19.96� 0.14 18.21 21.81 21.33� 0.58 20.09� 0.7EL 12.31� 1.38 10 15 14.07� 0.15 12.01 15.97 14.16� 1.53 7.82� 1.60CL 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 e e e e

OL 24.60� 0.96 23.15 26.30 25.73� 0.21 23.12 28.38 23.29� 1.21 29.36� 1.82ZB 14.15� 0.60 13 15.05 14.37� 0.12 12.81 15.85 13.11� 1.06 15.92� 0.39BB 12.07� 0.40 11.30 12.65 e e e 11.62 12.55� 0.46IC 3.63� 0.21 3.15 3.95 3.60� 0.02 3.30 3.87 3.54� 0.14 3.95� 0.16RH 6.54� 0.33 6 7 e e e 5.84 e

WR 4.92� 0.23 4.50 5.25 e e e 3.95� 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� 0.50MnT 5.60� 0.33 5.16 6.22 e e e 5.23� 0.138 7.00� 0.16MT 6.17� 0.25 5.65 6.55 6.14� 0.05 5.50 6.73 5.32� 0.204 7.01� 0.262n 54 54 e 52FN 54 54 e 54Tail color Slightly bicolored Bicolored Bicolored BicoloredNipples 4 pairs e 4 pairs 4 pairsHind 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).BB¼ breadth of braincase; BU¼ length of bullae; CL¼ condylobasal length of skull; EL¼ ear length; FL¼ hind foot length; FN¼ fundamental number; HBL¼ head and bodylength; IC¼ interorbital constriction; LLM¼ length of lower mandible; MnT¼mandibular tooth-row length; MT¼maxillary tooth-row length; OL¼ occipitonasal length ofskull; RH¼ height of rostrum; RL¼ length of rostrum; SE¼ standard error; TL¼ tail length; W¼weight; WR¼width of rostrum; ZB¼ zygomatic breadth.

F Ghorbani et al. / Journal of Asia-Pacific Biodiversity 8 (2015) 233e237 235

interparietal is pentagonal and its posterior edge is rather straight,but in fully grown specimens, interparietal is nearly hexagonal(Figure 2).

Incisors are yellowish; lowerM.1 has a pot-shaped anterior loop,one open and two closed labial triangles; it even has one open andthree nearly closed lingual triangles and a posterior loop(Figures 3B and 3C). Upper M3, which has an anterior loop, iscomplex, especially at the posterior side, with three or four lingualre-entrant folds that the fourth one cuts slightly, if exists, and twoor three slight re-entrant folds at labial side. These folds form oneclosed lingual triangle, two closed labial ones, and a small outerdenticle on the wearing surface of the upper M3 (Figures 3A and 4).These general patterns were observed in specimens, with somevariations (Figures 3C and 4).

Figure 2. Skull of Microtus levis: A, dorsal view; B, ventral view; C, outside view of thelower mandible.

Karyological features

Karyological study was performed on two males and three fe-males. The diploid number of chromosomes was 2n¼ 54, funda-mental number was FN¼ 54, and the number of autosomal armsfound in this study was FNa¼ 52. The autosomal set contains 54acrocentrics. The X chromosome is a large acrocentric, and the Ychromosome is a small acrocentric (Figure 5).

Discussion

The East European vole (M. levis) lives in dense colonies in thenorthern slopes of east Alborz. Relict Arcto-Tertiary Hyrcanianforests form themain part of the vegetation cover in the region. Thearea is covered with Fagus orientalis, Acer laetum, and subalpinespecies Quercus macranthera and Quercus pubescens surrounded byIrano-Turanian flora (Browicz 1989; Klein and Lacoste 1996; Akhaniet al 2010). Alborz and Zagros Mountains beside the Caspian Seaand Turkmenistan deserts (Misonne 1959) may constitute a sig-nificant barrier constraining migration of isolated populations ofM. levis in the Hyrcanian forests. This isolation was reported forsome small mammals in the Hyrcanian region such as Glis glis(Naderi et al 2014), Crocidura suaveolens (Dubey et al 2007), andCrocidura caspica (Hutterer 2005), resulting in the origination ofnew lineages.

M. levis is included in the arvalis group, which is discriminatedfrom the socialis group of voles inhabiting Iran (M. irani,M. paradoxus, M. socialis, and M. qazvinensis) by six plantar pads onhind feet, different patterns of prismatic molar, and differentkaryological features (Musser and Carleton 2005; Siahsarvie et al2008; Mohammadi et al 2013). It is also different from M. majoriand M. schelkovnikovi, the majori group, in terms of differentfundamental numbers of chromosomes, FN¼ 54 in M. levis versusFN¼ 60 in M. majori (Baskevich 1997) and FN¼ 62 inM. schelkovnikovi (Akhverdyan et al 1992); differentmolar patterns;

Figure 3. Dental pattern of Microtus levis: A, left upper tooth row; B, left lower toothrow; C, variability of the left lower M.1 in M. levis.

Figure 4. Variability of the left upper M.3 in Microtus levis.

Figure 5. Metaphase spread of Microtus levis: A, female; B, male.

F Ghorbani et al. / Journal of Asia-Pacific Biodiversity 8 (2015) 233e237236

and different body size (Nadachowski 2007). Compared toM. transcaspicus and M. obscurus, the species of the arvalis groupdistributed in the north of Iran M. levis represents different kary-ological features (2n¼ 54, FN¼ 54 inM. levis vs. 2n¼ 52, FN¼ 54 inM. transcaspicus) and measurements, e.g. different head and bodylength (mean¼ 105.77� 7.53 inM. levis vs.mean¼ 94.56�11.85 inM. obscurus and mean¼ 145.9�12.4 in M. transcaspicus) and con-dylobasal length of the skull (mean¼ 24.96� 0.97 in M. levis vs.mean¼ 23.6�1.41 in M. obscurus; Table 1).

Karyological results were the same as that of M. levis reportedpreviously from Kirikkale, central Turkey (Gözütok and Albayrak2009), but different from M. levis from Taurus Mountains(2n¼ 54, FNa¼ 54; Yavuz et al 2011) and M. rossiaemeridionalisfrom Lithuania (2n¼ 54 and FN¼ 56; Ma�zeikyte et al 1999). The

same karyological results may indicate that the population ofM. levis from the Hyrcanian region is closely related to that ofM. levis from central Turkey.

In the specimens ofM. levis from Iran, the tail is longer (over 31%HB) than that of the specimens from Turkey (25% HB; Yavuz et al2011). In general, the specimens from Iran show a lower averagein measurements except for tail length, length of lower mandible,maxillary tooth-row length, and interorbital constriction, e.g. thecondylobasal length of the specimens (mean¼ 24.96 mm) isshorter than that of specimens from Turkey (mean¼ 25.19 mm;Table 1). However, because of high rates of evolution and speciationin the genus Microtusdw30,000 years for each species, accordingto deduction from fossil records, 100,000 years based on molecularclock estimation (Repenning 1980; Chaline et al 1999; Brunet-Lecomte and Chaline 1991; Triant and DeWoody 2006)dandlongtime separation of the colonies of M. levis in the Hyrcanianforests by three main barriers, mountainous Caucasus, Caspian Sea,and Turkmenistan deserts (Misonne 1959), these isolated pop-ulations should be further tested using molecular data.

Acknowledgments

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

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