462

http://journals.tubitak.gov.tr/zoology/

Turkish Journal of Zoology Turk J Zool(2013) 37: 462-469© TÜBİTAKdoi:10.3906/zoo-1108-25

Cytotypes of Nannospalax xanthodon (Satunin, 1898) (Rodentia: Spalacidae)from western Anatolia

Mustafa SÖZEN, Faruk ÇOLAK, Murat SEVİNDİK, Ferhat MATUR*Department of Biology, Faculty of Arts and Science, Bülent Ecevit University, Zonguldak, Turkey

* Correspondence: ferhat.matur@gmail.com

1. IntroductionChromosomal differentiation between populations may initiate the process of speciation (Zima, 2000). Certain kinds of chromosomal change may tend to promote speciation, because of reduced fertility in hybrids (King, 1993).

Although 8 living species are included in recent taxonomic checklists (Kryštufek and Vohralík, 2005; Yiğit et al., 2006), more than 50 cytotypes have been reported in blind mole rats and there is still doubt about the taxonomy of this taxon (Savić and Nevo, 1990; Nevo et al., 2001; Arslan et al., 2011; Kankılıç et al., 2011; Sözen et al. 2011). Topachevskii (1969) proposed 2 genera: Microspalax and Spalax. Later, Gromov and Baranova (1981) recognized 2 genera (Nannospalax and Spalax) since Microspalax was a homonym of an arachnid species. After that, most recent taxonomic sources accepted the generic name Nannospalax as valid for blind mole rats in Turkey (Kryštufek and Vohralík, 2005; Yiğit et al., 2006). Therefore, we used here the generic name Nannospalax, and 3 Nannospalax species (N. leucodon, N. xanthodon, and N. ehrenbergi) are distributed in Turkey (Topachevskii, 1969; Kryštufek and Vohralík, 2005; Yiğit et al., 2006).

The results of karyological studies showed that more than 30 cytotypes of Nannospalax are reported from Turkey. N. xanthodon is distributed in most of Turkey and has a diploid chromosome number ranging between 2n = 36 and 60, while its NF value ranges between 66 and 92 (Nevo et al., 1994, 1995; Sözen et al., 1998a, 1998b, 1999,

2000a, 2000b, 2011; Coşkun, 2003, 2004; Matur and Sözen, 2005; Kankılıç et al. 2005, 2007, 2010; Ivanitskaya et al., 2008; Aşan and Yağcı, 2008; Matur et al., 2011).

Although extensive karyological studies have been conducted since 1978 in Turkey, some karyological gaps still exist in some areas and need to be filled. The purpose of the present study was to describe the karyotypic characteristics of various localities to fill the gaps in our knowledge about cytotypes and their distributional areas in western Turkey.

2. Materials and methodsWe studied 121 (43 males, 78 females) blind mole rats from 54 localities in western Anatolia. The Table gives the sampled localities, the number of individuals analyzed, and the karyological results, while Figure 1 shows the distribution of cytotypes and collection sites.

We prepared the karyotypes from bone marrow according to Ford and Hamerton (1956) and about 25–30 metaphase cells, which were well-stained and contained well-separated and distinct chromosomes, were examined from each animal. We determined the diploid number of chromosomes (2n), the number of autosomal arms (NFa), and the total number of chromosomal arms (NF) as well as the sex chromosomes from photos of the metaphase plates according to centromere position.

The karyotype preparations and voucher specimens are deposited in the Department of Biology, Faculty of Arts and Science, Bülent Ecevit University (formerly named Zonguldak Karaelmas University).

Abstract: We performed this study on the subterranean mole rat Nannospalax xanthodon (Nehring, 1898) in western Turkey and we analyzed karyotypes of 121 specimens from 54 localities. We determined that N. xanthodon has 2n = 36, NF = 70; 2n = 38, NF = 74; 2n = 40, NF = 72; 2n = 50, NF = 70; 2n = 50, NF = 74; 2n = 52, NF = 70; 2n = 56, NF = 72; and 6 different cytotypes of 2n = 60, NF = 74, 76, 78, 80, 82, 84 in the specimens analyzed from western Turkey. We filled most of the karyological gaps in western Anatolia and documented distributional areas of cytotypes.

Key words: Rodentia, Spalacidae, blind mole rats, karyotype, Turkey

Received: 01.09.2011 Accepted: 17.02.2013 Published Online: 24.06.2013 Printed: 24.07.2013

Research Article

SÖZEN et al. / Turk J Zool

463

Table. Localities, sample size (M: males, F: females), diploid chromosome numbers (2n), and chromosomal arm numbers (NF) of animals examined.

No. Locality Province M F 2n NF NFa X Y

1 Kemer cemetery, Aydın Aydın 0 2 36 70 66 sm -2 Yatağan Muğla 1 0 36 70 66 sm a3 Denizkent Balıkesir 2 2 38 74 70 sm a4 Dursunbey Balıkesir 1 0 38 74 70 sm a5 Karacabey Bursa 0 4 38 74 70 sm -6 Bozcaada Çanakkale 1 0 38 74 70 sm a7 Ezine Çanakkale 1 1 38 74 70 sm a8 Gökçeada Çanakkale 1 4 38 74 70 sm a9 Gelenbe Manisa 1 3 38 74 70 sm a

10 Zeytinova village, Akhisar Manisa 0 2 38 74 70 sm -11 Duallar village, Gelenbe Manisa 0 1 38 74 70 sm -12 Beyşehir 12 km SW Konya 1 2 40 72 68 sm a13 Ovacık, Pamukören Aydın 0 3 50 74 70 sm -14 Kahyalar Karabük 0 1 50 70 66 sm -15 Seyitler Karabük 1 1 50 70 66 sm a16 Akören Karabük 0 1 50 70 66 sm -17 Yeşiltepe Karabük 1 1 50 70 66 sm a18 Karabük organized industry area Karabük 1 0 50 70 66 sm a19 Yeşilyurt way fork-Alaşehir Manisa 2 1 50 74 70 sm a20 1 km N of Dörtdivan Bolu 1 1 52 70 66 sm a21 Around Gölköy pond Bolu 1 2 52 70 66 sm a22 Yelkenler village Bolu 0 1 52 70 66 sm -23 30 km W of Mengen Bolu 0 2 52 70 66 sm -24 2 km SE of Gerede Bolu 1 0 52 70 66 sm a25 10 km W of Gerede Bolu 1 2 52 70 66 sm a26 1 km W of Gerede Bolu 2 2 52 70 66 sm a27 Yalova center, Bursa road Yalova 2 1 52 70 66 sm a28 7 km S of Kula, Çiftçiibrahim village Manisa 2 1 56 72 68 sm a29 Gediz way fork, organized industry area Uşak 1 1 56 72 68 sm a30 Karabük Kastamonu way fork Karabük 0 1 56 72 68 sm -31 10 km N of Antalya Antalya 1 1 60 74 70 sm a32 Dağbeli, Antalya Antalya 1 1 60 74 70 sm a33 Korkuteli, Fethiye exit Antalya 1 2 60 74 70 sm a34 20 km W of Korkuteli Antalya 0 1 60 74 70 sm -35 Kızlar Sivrisi, Elmalı Antalya 0 3 60 82 78 sm -36 Around Aladağ pond Bolu 0 2 60 78 74 sm -37 Yağbaşlar village Bolu 1 1 60 78 74 sm a38 Sorkun village Bolu 1 1 60 78 74 sm a39 12 km E of Gerede Bolu 0 2 60 78 74 sm -40 Bucak, center Burdur 0 1 60 74 70 sm -41 Entrance from Gemlik side Bursa 2 1 60 80 76 sm a42 Ece Mahallesi, Harmancık Kütahya 1 1 60 80 76 sm a43 Kale village Denizli 2 1 60 80 76 sm a44 Kaklık village, 32 km W of Denizli Denizli 0 2 60 80 76 sm -45 Çivril town Denizli 1 1 60 80 76 sm a46 Çameli village Denizli 1 1 60 84 80 sm a47 5 km N of Eskipazar Karabük 1 1 60 78 74 sm a48 Kütahya exit, Tavşanlı Kütahya 1 1 60 80 76 sm a49 Emet 7 km N Kütahya 1 1 60 80 76 sm a50 Simav 8 km W Kütahya 1 1 60 80 76 sm a51 Söbüalan area, Murat Dağı Kütahya 2 3 60 78 74 sm a52 Selendi 2 km S Manisa 0 3 60 76 72 sm -53 Seki village Denizli 0 1 60 84 80 sm -54 Banaz 16 km S, Kızılcasöğüt Uşak 0 2 60 78 74 sm -

Total 43 78

SÖZEN et al. / Turk J Zool

464

3. ResultsWe found 7 different diploid numbers of chromosomes (2n = 36, 38, 40, 50, 52, 56, and 2n = 60).

The populations with karyotype of 2n = 36: we found this cytotype in Aydın and Yatağan (Muğla) (Figure 1; Table). The karyotype had NF = 70, NFa = 66. The X chromosome was submetacentric and the Y was acrocentric. The autosomal set consisted of 2 groups: 16 pairs of meta-submetacentric chromosomes and a pair of acrocentric chromosomes (Figure 2).

The populations with karyotype of 2n = 38: we collected this cytotype from Bozcaada (Tenedos) island, Gökçeada (Imbros) island (in the Aegean Sea), Ezine (Çanakkale), Denizkent, Dursunbey (Balıkesir), Kırkağaç, Zeytinova, Gelenbe (Manisa), and Karacabey (Bursa) (Figure 1; Table). The X chromosome was submetacentric and the Y was acrocentric. The autosomal set consisted of 2 groups: 16 pairs of bi-armed chromosomes and 2 pairs of acrocentric chromosomes. We calculated NF and NFa for this cytotype as 74 and 70, respectively.

The populations with karyotype of 2n = 40: we determined the karyotype of the population collected 12

km southwest of Beyşehir (Konya) (Figure 1; Table) as 2n = 40 NF = 72, NFa = 68. The X chromosome was a medium-sized metacentric and the Y chromosome was a small-sized acrocentric. The autosomal set consisted of 2 groups: 15 pairs of bi-armed chromosomes and 4 pairs of acrocentric chromosomes (Figure 3).

The populations with karyotype of 2n = 50: we found these karyotypes in populations from Alaşehir, Pamukören (Manisa) (Figure 1; Table) as 2n = 50; NF = 74; NFa = 70. The X chromosome was a middle-sized submetacentric. The autosomal set contained 11 pairs of bi-armed and 13 pairs of acrocentric chromosomes.

The populations with karyotype of 2n = 52: we found 2n = 52, NF = 70, NFa= 66 cytotypes from Yalova, Gölköy, Dörtdivan, Yelkenler, Mengen, and Gerede (Figure 1; Table). The X chromosome was a middle-sized metacentric. The autosomal set consisted of 2 groups: 8 pairs of bi-armed and 17 pairs of acrocentric chromosomes.

The populations with karyotype of 2n = 56: these karyotypes in animals from Uşak, Manisa, and Karabük (Figure 1; Table) had a diploid number of 2n = 56; NF = 72 and NFa= 68 (Figure 4). The X chromosome was a

1

10

2

11

8

7

9

18

21

1 19

13

22

12

14-17

20

3

41

5

6

7

23 24 25 26

27

28

30

40

31 32 33 34

35

36 37 38 39 41 42

43

44

45

46

47

48 49

50 52

53

54

42

51 29

40 56

38

52 60

36

50

100 0 100 200 300 km

Figure 1. Map of study area in Turkey and distribution of N. xanthodon cytotypes determined. The numbers of localities are as in the Table.

SÖZEN et al. / Turk J Zool

465

middle-sized submetacentric and the Y chromosome was a small acrocentric. The autosomal set contained 7 pairs of bi-armed and 20 pairs of acrocentric chromosomes.

The populations with karyotype of 2n = 60: Most localities studied have karyotypes with 2n = 60 (Table; Figure 1). Six different NF and NFa values we determined for the 2n = 60 cytotype (Figure 5). The number of

chromosome arms in the populations studied is shown in the Table and Figure 5. The distribution of bi-armed and acrocentric chromosomes is given in Figure 5.

4. DiscussionSözen et al. (1999) and Kankılıç et al. (2010) gave the 2n = 36 cytotype in west Anatolia. We gave additional distribution information for these cytotypes.

1 2 3 4 5

10 9 8 7 6

11 12 13 14 15

Y X 16 17

Figure 2. The karyotype of a male N. xanthodon from Aydın (2n = 36, NF = 70).

1 2 3 4 5 6

7 8 9 10 11 12

13 14 15

16 17

X Y

18 19

Figure 3. Karyotype of a male N. xanthodon from Beyşehir, Konya (2n = 40, NF = 72).

SÖZEN et al. / Turk J Zool

466

The 2n = 38 cytotype was recorded from the Aegean region in western Anatolia (Savić and Soltdatović, 1979; Giagia et al., 1982; Nevo et al., 1994, 1995; Tez et al., 2002; Sözen, 2004). We karyotyped for the first time blind mole rats from Turkish islands, Bozcaada (Tenedos) and Gökçeada (Imbros) in the Aegean Sea, and found 2n = 38, NF = 74 in the present study. Similarly, the karyotypes of mole rats from Denizkent, Ezine, and Karacabey were determined as 2n = 38, NF = 74. Therefore, the range of the 2n = 38 cytotype reached the Marmara Sea. Özkan (1999) stated that the morphological peculiarities of mole

rats from Gökçeada (Imbros) were similar to those of mole rats in Thrace and corresponding to the subspecies Nannospalax leucodon turcicus from southeastern Europe, while mole rats from Bozcaada (Tenedos) were similar to mole rats in western Anatolia and recognized as the subspecies N. l. anatolicus. However, we have shown here that the 2n = 38 cytotype is distributed on both the islands as in western Anatolia.

Nevo et al. (1994) recorded the 2n = 40 cytotype from Beyşehir first. Recently, Kankılıç et al. (2006) and Arslan et al. (2011) reported it again from the Beyşehir area. We

1 2 3 4 5 6

7

8 9 10 11 12 13

14 15 16 17

X Y

18 19

20

26

21 22

23

24 25

27

74

76

78

80

82

84

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 X Y

Figure 4. Karyotype of a male N. xanthodon from 7 km S of Kula, Çiftçiibrahim village, Manisa (2n = 56, NF = 72).

Figure 5. Arranged chromosomes of all NF variations of the 2n = 60 cytotypes. Chromosomes with double arms are shown in the black line, and black dot at the end of NF = 82 line means that the animal was female and had no Y chromosome.

SÖZEN et al. / Turk J Zool

467

recorded here that the same cytotype is present 12 km southwest of Beyşehir.

Nevo et al. (1994) found the 2n = 50 cyotype in western Anatolia, 35 km east of Aydın. We recorded the same cytotype from 2 additional localities: Aydın and Manisa. Sözen (2004) first recorded 2n = 50 from northern Anatolia from Keltepe around Karabük. Later, Sözen et al. (2006a) reported an additional record from Kahyalar about 5 km away from Keltepe. We found 4 new localities for this cytotype (numbers 15–18 in Figure 1) and the distribution area of this cytotype can generally be determined as about 20–25 km2. This cytotype is surrounded by 2n = 60 to the south, 2n = 56 to the east, and 2n = 52 to the west.

Sözen (2004) reported the 2n = 52 karyotype from northwestern Anatolia, in Karamürsel, Abant, Mudurnu, Nallıhan, Seben, Yeniçağa, Kartalkaya, and Mengen. Later, Matur and Sözen (2005) reported records from Gölpazarı, Taraklı, Geyve, and Yenipazar. We found new localities in the present study and clarified the distribution area of this cytotype to a large extent. According to previous records, the Yalova locality recorded here is the most westerly point and 2 km SE of Gerede is the most easterly point of this cytotype. The distance between Dörtdivan 1 km N (locality 26 in Figure 1) and Sorkun (locality 38 in Figure 1) was about 3 km and no geographical barrier exists between these 2 localities. However, the cytotype in Dörtdivan was 2n = 52 and the cytotype in Sorkun was 2n = 60. Interestingly, although very suitable steppe habitats separate these 2 localities, we did not observe any blind mole rat distribution there.

The mobility of blind mole rats is quite restricted and karyological rearrangements could be easily fixed in small populations (Nevo, 1991). Matur et al. (2011) found that four 2n = 50 cytotypes from south, north, west, and east Anatolia were different, inferred from G- and C-banding. That is why the distance is very important for mole rat distribution as well. If cytotypes with the same diploid number are isolated, it may be possible to regard them as different cytotypes.

Sözen (2004) and Sözen et al. (2006b) recorded the 2n = 56 cytotype from Safranbolu and Kastamonu in northern Anatolia. In western Anatolia, the 2n = 56 cytotypes were previously recorded from Isparta (Kankılıç et al., 2007) and Uşak (Kankılıç et al., 2010). These 2 cytotypes appear to be identical and are regarded as 1 cytotype. Here we found a cytotype similar to that given by Kankılıç et al. (2010) in a nearby locality in Uşak Province (Çiftçiibrahim village).

The 2n = 56 cytotypes from Karabük are differentiated from cytotypes with the same diploid number from western Anatolia by having 2 large metacentrics and a large acrocentric pair. Matur et al. (2011) reported that even though the cytotypes have similar diploid number

in Anatolia, those cytotypes have different G-banding patterns. Similar results might be observed for these 2n = 56 cytotypes.

The karyotype 2n = 60 was mostly recorded from central Anatolia (Yüksel, 1984; Gülkaç and Yüksel, 1989; Nevo et al., 1994; Nevo et al., 1995; Sözen et al., 1999; Sözen et al., 2000b; Tez et al., 2001; Yüksel and Gülkaç, 2001; Sözen, 2004; Matur and Sözen, 2005; Kankılıç et al., 2006; Sözen et al., 2006a, 2006b). The 2n = 60 cytotype has several different NF values in its distribution area (see Table in Sözen et al., 2006a).

We recorded this cytotype from 24 additional localities here and these were new localities generally indicating the western distribution points for the 2n = 60 cytotype. Figure 1 shows that distribution of these cytotypes is not restricted to central Anatolia and extends from the Mediterranean area in Antalya 10 km N up to the coastal Marmara region in Bursa (Figure 1).

Nevo et al. (2004) found the 2n = 54 cytotype from Bolu, and they referred to this cytotype as 2n = 54W. So far we have not found this cytotype from Bolu. We eventually omitted here 2n = 54W from the list of the cytotypes of N. xanthodon.

Nevo (1991) and Sözen (2004) suggested that speciation in the Spalacidae is presumably peripatric. Matur (2009) determined G- and C-banding pattern of 10 cytotypes of mole rats from western Anatolia and investigated these cytotypes grouped as a different clade named the northern group (2n = 54N, 58N, 60R), the middle group (2n = 52, 56W and 60), and the western group (2n = 36, 38, 40, 50W). Moreover, the northern group occupies a smaller area than the western group.

This study filled most of the gaps in the distribution of blind mole rat cytotypes in western Turkey. The next step in studies on blind mole rats should deal with the taxonomical status of cytotypes. It is very possible that most of the cytotypes in Turkey represent different biological species (Nevo et al., 1994, 1995; Sözen et al., 1999, 2000a, 2000b, 2006a, 2006b; Sözen, 2004). Depending on cytotypes determined, new studies in the near future on these cytotypes may solve such taxonomical problems by using more detailed chromosome banding, genetic, molecular, behavioral, physiological etc. studies.

AcknowledgmentsWe would like to thank Dr Ahmet Karataş preparing the map in Figure 1. We also thank the 3 anonymous reviewers for their contribution during the evaluating process. This study was supported by TÜBİTAK (TBAG HD-164) and Zonguldak Karaelmas University (Nr: 2004-13- 06-07, 2007/2.13.06.18).

SÖZEN et al. / Turk J Zool

468

References

Arslan, A., Akan, Ş. and Zima, J. 2011. Variation in C-heterochromatin and NOR distribution among chromosomal races of mole rats (Spalacidae) from Central Anatolia, Turkey. Mamm. Biol. 76: 28–35.

Aşan, N. and Yağcı, T. 2008. Karyotype and hair scale structure of Nannospalax leucodon (Nordmann, 1840) from Central Anatolia (Rodentia: Spalacidae). Turk. J. Zool. 32: 125–130.

Coşkun, Y. 2003. A study on the morphology and karyology of Nannospalax nehringi (Satunin, 1898) (Rodentia: Spalacidae) from North-eastern Anatolia, Turkey. Turk. J. Zool. 27: 171–176.

Coşkun, Y. 2004. Morphological and karyological characteristics of Nannospalax ehrenbergi (Nehring, 1898) (Rodentia: Spalacidae) from Hatay Province, Turkey. Turk. J. Zool. 28: 205–212.

Ford, C. and Hamerton, J. 1956. A colchicine hypotonic citrate, squash for mammalian chromosomes. Stain Technol. 31: 247–251.

Giagia, E., Savić, I. and Soltdatović, B. 1982. Chromosomal forms of the mole rat Microspalax from Greece and Turkey. Z. Saugetierkd. 47: 231–236.

Gromov, I. and Baranova, G. 1981. Catalogue of Mammals in USSR, Nauka, Leningrad.

Gülkaç, M.D. and Yüksel, E. 1989. Malatya yöresi körfareleri (Rodentia; Spalacidae) üzerine sitogenetik bir inceleme. DOĞA TU. Biyol. D. 13: 63–71.

Ivanitskaya, E., Sözen, M., Rashkovetsky, L., Matur, F. and Nevo, E. 2008. Discrimination of 2n=60 Spalax leucodon cytotypes (Spalacidae, Rodentia) in Turkey by means of classical and molecular cytogenetic techniques. Cytogenet. Genome Res. 122: 139–149.

Kankılıç, T., Çolak, E., Çolak, R. and Yiğit, N. 2005. Allozyme variation in Spalax leucodon Nordmann, 1840 (Rodentia: Spalacidae) in the area between Ankara and Beyşehir. Turk. J. Zool. 29: 377–384.

Kankılıç, T., Kankılıç, T., Çolak, R., Kandemir, İ. and Çolak, E. 2006. Morphological comparison of seven chromosomal forms of Spalax leucodon Nordman, 1840 (Mammalia: Rodentia) in Turkey. Pak. J. Biol. Sci. 9: 2419–2425.

Kankılıç, T., Kankılıç, T., Çolak, R., Çolak, E. and Karataş, A. 2007. Karyological comparison of populations of the Spalax leucodon Nordmann, 1840 superspecies (Rodentia: Spalacidae) in Turkey. Zool. Middle East 42: 15–24.

Kankılıç, T., Kankılıç, T., Şeker, P.S., Çolak, R., Selvi, E. and Çolak, E. 2010. Contributions to the karyology and distribution areas of cytotypes of Nannospalax leucodon (Rodentia: Spalacidae) in Western Anatolia. Acta Zool. Bulgar. 62(2): 161–167.

King, M. 1993. Species Evolution: The Role of Chromosomal Change. Cambridge University Press, Cambridge.

Kryštufek, B. and Vohralík, V. 2005. Mammals of Turkey and Cyprus, Vol. 2: Rodentia I: Sciuridae, Dipodidae, Gliridae, Arvicolinae, Annales Majora Koper, Slovenia.

Matur, F. 2009. Comparison of chromosomal form of Nannospalax (Mammalia: Rodentia) from Western Turkey inferred from G and C Banding. PhD dissertation. Department of Biology. 117 pp. Zonguldak Karaelmas University, Zonguldak, Turkey 2009.

Matur, F. and Sözen, M. 2005. A karyological study on subterrranean mole rats of the Spalax leucodon Nordmann, 1840 (Mammalia: Rodentia) superspecies in northwestern Turkey. Zool. Middle East 36: 5–10.

Matur, F., Çolak, F., Sevindik, M. and Sözen, M. 2011. Chromosomal evolution of Nannospalax nehringi inferred from cytogenetic comparison of 2n = 50 karyotypic forms in Türkiye. Zool. Science 28: 61–67.

Nevo, E. 1991. Evolutionary theory and processes of active speciation and adaptive radiation in subterranean mole rats, Spalax ehrenbergi superspecies, in Israel. Evol. Biol. 25: 1–125.

Nevo, E., Filippucci, M.G., Redi, C., Korol, A. and Beiles, A. 1994. Chromosomal speciation and adaptive radiation of mole-rats in Asia Minor correlated with increased ecological stress. P. Natl. Acad. Sci. USA 91: 8160–8164.

Nevo, E., Filippucci, M.G., Redi, C., Simson, S., Heth, G. and Beiles, A. 1995. Karyotype and genetic evolution in speciation of subterranean mole rats of the genus Spalax in Turkey. Biol. J. Linn. Soc. 54: 203–229.

Nevo, E., Ivanitskaya, E. and Beiles, A. 2001. Adaptive radiation of blind subterranean mole rats: naming and revisiting the four sibling species of the Spalax ehrenbergi superspecies in Israel: Spalax galili (2n=52), S. golani (2n=54), S. carmeli (2n=58) and S. judaei (2n=60), Backhuys Publishers, Leiden.

Özkan, B. 1999. The rodent fauna of Gökçeada and Bozcaada (Rodentia: Mammalia). Turk. J. Zool. 23: 133–147.

Savić, I. and Nevo, E. 1990. The Spalacidae: Evolutionary history, speciation, and population biology. In: Nevo E., Reig O.A. (Eds). Evolution of Subterranean Mammals at the Organismal and Molecular Levels, Alan R. Liss, Inc, New York, pp. 129–153.

Savić, I. and Soldatović, B. 1979. Contribution to the knowledge of the genus Spalax (Microspalax) karyotype from Asia Minor. Arhiv Bioloskih Nauka, Beograd 31: 1–2.

Sözen, M. 2004. A karyological study on subterranean mole rats of the Spalax leucodon Nordmann, 1840 superspecies in Turkey. Mamm. Biol. 69: 420–429.

Sözen, M. 2005. A biological investigation on Turkish Spalax Guldentaedt, 1770 (Mammalia: Rodentia). G. U. Journal of Science 18: 167–181.

Sozen, M. and Kivanc, E. 1998a. Two new karyotypic forms of Spalax leucodon (Nordmann, 1840) (Mammalia: Rodentia) from Turkey. Z Saugetierkd. -Mamm. Biol. 63: 307–310.

Sozen, M. and Kivanc, E. 1998b. A new karyotype of Spalax leucodon cilicicus Mehely, 1909 (Mammalia: Rodentia) from the type locality in Turkey. Israel J. Zool. 44: 53–55.

Sözen, M., Çolak, E., Yiğit, N., Özkurt, S. and Verimli, R. 1999. Contributions to the karyology and taxonomy of the genus Spalax Guldenstaedt, 1770 (Mammalia: Rodentia) in Turkey. Mamm. Biol. 64: 210–219.

SÖZEN et al. / Turk J Zool

469

Sözen, M., Çolak, E. and Yiğit, N. 2000a. Contributions to the karyology and taxonomy of Spalax leucodon nehringi Satunin, 1898 and Spalax leucodon armeniacus Mehely, 1909 (Mammalia: Rodentia) in Turkey. Z Saugetierkd-Mamm. Biol. 65: 309–312.

Sözen, M., Yiğit, N. and Çolak, E. 2000b. A study on karyotypic evolution of the genus Spalax Guldenstaedt, 1770 (Mammalia: Rodentia) in Turkey. Israel J. Zool. 46: 239–242.

Sözen, M., Matur, F., Çolak, E., Özkurt, Ş. and Karatas, A. 2006a. Some karyological records and a new cytotype for Spalax (Mammalia: Rodentia) in Turkey. Folia Zool. 55: 247–256.

Sözen, M., Sevindik, M. and Matur, F. 2006b. Karyological and some morphological characteristics of Spalax leucodon Nordmann, 1840 (Mammalia: Rodentia) superspecies around Kastamonu province, Turkey. Turk. J. Zool. 30: 205–219.

Sözen, M., Çataklı, K., Eroğlu, F., Matur, F. and Sevindik, M. 2011. Distribution of chromosomal forms of Nannospalax nehringi (Satunin, 1898) (Rodentia: Spalacidae) in Çankırı and Çorum provinces, Turkey. Turk. J. Zool. 35(3): 367–374.

Tez, C., Gündüz, İ. and Kefelioğlu, H. 2001. Karyological study of Spalax leucodon Nordmann, 1840 in central Anatolia. Pak. J. Biol. Sci. 4: 869–871.

Tez, C., Gündüz, İ. and Kefelioğlu, H. 2002. Note: New data on the distribution of 2N=38 Spalax leucodon (Nordmann, 1840) cytotype in Turkey. Israel J. Zool. 48: 155–159.

Topachevskii, W. 1969. Fauna USSR Spalacidae (English translation; US Dept. Commerce. Natn. Info. Serv., Springfield, Virginia), Nauka, Leningrad.

Yiğit, N., Çolak, E., Sözen, M. and Karataş, A. 2006. Rodents of Türkiye. Meteksan, Ankara.

Yüksel, E. and Gülkaç, M.D. 2001. The cytogenetical comparisons of Spalax (Rodentia: Spalacidae) populations from middle Kızılırmak Basin, Turkey. Turk. J. Biol. 25: 17–24.

Yüksel, E. 1984. Cytogenetic study in Spalax (Rodentia; Spalacidae) from Turkey. Communications. C. Biologie 2: 1–12.

Zima, J. 2000. Chromosomal evolution in small mammals (Insectivora, Chiroptera, Rodentia). Hystrix 11: 5–15.