New records of Eurasian Blind Snake, Xerotyphlops vermicularis (Merrem, 1820) from the Black Sea region of Turkey and its updated distribution

BIHAREAN BIOLOGIST 10 (2): 98103 Biharean Biologist, Oradea, Romania, 2016 Article No.: e161301 http://biozoojournals.ro/bihbiol/index.html New records of Eurasian Blind Snake, Xerotyphlops vermicularis (Merrem, 1820) from the Black Sea region of Turkey and its updated distribution Murat AFSAR 1, *, Kerim ÇIÇEK 2, Yahya TAYHAN 3 and Cemal Varol TOK 4 1. Department of Biology, Faculty of Arts and Sciences, Celal Bayar University, Manisa, Turkey. 2. Zoology Section, Department of Biology, Faculty of Science, Ege University, 35100, Izmir, Turkey. 3. Hakkari University, Health Vocational College, Hakkari, Turkey. 4. Department of Biology, Faculty of Arts and Sciences, Çanakkale Onsekiz Mart University, 17100, Çanakkale, Turkey. *Corresponding author, M. Afsar, Email: murat.afsar@bayar.edu.tr Received: 07. November 2015 / Accepted: 28. December 2015 / Available online: 30. October 2016 / Printed: December 2016 Abstract. In this study, we report two new localities of Xerotyphlops vermicularis from western and central Black Sea Region. With these records, the distribution of the species is extended about 90km to the north. The specimens were examined morphologically and compared with the relevant literature. In addition, on the basis of the new and literature records, the potential distribution of the species was modelled with ecological niche modelling. The main factors affecting the distribution of the species are the annual mean temperature (bio1, 55.3%), precipitation of driest month (bio14, 18.5%), and annual precipitation (bio12, 10.1%) and account for 84% of the distribution model. Key words: Xerotyphlops vermicularis, Typhlopidae, distribution, new record, ecological niche modeling, Black Sea Region, Anatolia. Introduction Family Typhlopidae is mostly distributed in the Neotropic, Australasian, IndoMalayan and Afrotropic ecoregions (Kornilios et al. 2013) and consists of 389 species (Uetz & Hošek 2015). Genus Xerotyphlops has recently been described by Hedges et al. (2014), consists of 4 valid species (Xerotyphlops etheridgei, X.wilsoni, X.socotranus, and X.vermicularis), and is distributed in the xeric regions of three continents, including the Sahara Desert and the Socotra Island (Africa), southwestern Asia, and southeastern Europe (Hedges et al., 2014). Eurasian Blind Snake, X.vermicularis (Merrem 1820), is distributed from the southeast of Europe to the Middle East (Hedges et al. 2014, Pyron & Wallach 2014), and although the genus occurs in xeric regions, X.vermicularis generally prefers more humid microhabitats than other conspecifics (Kornilios et al. 2011). In Turkey, the available information on the distribution of X.vermicularis particularly in the Western and Central Black Sea regions are limited (Baran et al. 1992). To date, there are only two old records of the species in the Black Sea Region (from Trabzon [Bedriagae (1879)] and Amasya [Boettger (1880)]). Since no material could be obtained from the Black Sea Region by subsequent researchers (Baran et al. 1992, Baran et al. 1997, Kumlutaş et al. 1998, Baran et al. 2001b, Kutrup 2001, Dinçaslan et al. 2013), no evaluation could be made regarding the distribution and taxonomic situation of the species in this region. In the recent years, X. vermicularis was also phylogenetically evaluated (Kornilios et al. 2011, 2012) and populations from Turkey except for Black Sea Region were divided into six clades. Most of these clades are deeply divergent what suggests that X. vermicularis is a complex of several morphologically cryptic species. Besides, Gül et al. (2015) have tried to reveal the climatic preferences and distributions of these six isolated lineages in Anatolia. In this study, we report two new localities for X.vermicularis from Western and Central Black Sea region, and the distributional range of the species is extended with these new localities. Besides, the potential distribution of the species was modelled by ecological niche model. Material and Methods Overall Some twelve specimens of X.vermicularis were caught from Sinop (10 specimens) and Samsun (2 specimens) in the Western and Central Black Sea regions of northern Anatolia during the herpetological excursions carried out between April and August 2014. The morphological characters were taken according to Baran (1976) and measured by means of digital calipers with 0.02 mm sensitivity and a tape measure with 0.1 mm sensitivity (for the body and tail lengths). The ventral scales of the specimens were counted according to Dowling (1951) method. Colour and pattern characteristics were recorded while the specimens were still alive, and colour slides taken while the animals were alive and utilized in the study. The material is preserved at the department of Zoology at Celal Bayar University (CBU, Manisa, Turkey) and in the collection of Ondokuz Mayıs University. The distribution of the species in Turkey were formed using the records provided by Bodenheimer (1944), Clark & Clark (1973), Baran (1976), Baran (1977 a,b), Baran (1982), Teynie (1991), Mulder (1995), Tok (1993), Demirsoy (1996), Arıkan et al. (1994, 1998), Başoğlu & Baran (1998), Uğurtaş et al. (2000, 2007), Katılmış et al. (2002), Özdemir & Baran (2002), Baran et al. (2001a,b, 2004, 2006), Kumlutaş et al. (2000, 2004a,b),, Hür et al. (2008), Tosunoğlu et al. (2010), Afsar et al. (2013), Afsar and Tok (2011), Cihan & Tok (2014), Eser & Erişmiş (2014), Tok & Çiçek (2014), and Özcan & Üzüm (2014). The locality information with no coordinate data was obtained by using Google Earth vers. 7.1.2 (Google Inc.). All records were georeferenced into WGS84 coordinate system and checked with ArcGIS v9.0 (ESRI). Some 20 climatic and topographical variables were used as predictors for the current distribution. 19 climate data were obtained from WorldClim ver.1.4 data set (Hijmans et al. 2005, http://www.worldclim.org) at the spatial resolution of 30 arc seconds (approx. 1 km), which represents monthly temperature and rainfall data as averages of the period 1950 2000. Elevation data were resampled from Shuttle Radar Topography Mission (SRTM) in UTM projection at 90 m resolution (Jarvis et al. 2008; http://srtm.csi.cgiar.org/). To reduce the negative effect that might result from multicollinearity among the environmental variables (Heikkinen et al. 2006), we selected a subset of the bioclimatic variables based on the ecological requirements of the species and a pairwise Pearson correlation (R 2 < 0.75). We chose 8 environmental variables [bio1 = annual mean temperature, bio2= mean diurnal range (mean of monthly (max temp min temp)), bio3 = isothermality (bio2 / bio7) (* 100), bio7 = annual temperature range (bio5 bio6), bio8 = mean temperature of wettest

New records of Xerotyphlops vermicularis from the Black Sea region of Turkey and its updated distribution 99 quarter, bio14 = precipitation of driest month, and bio15 = precipitation seasonality (coefficient of variation)] that underlay the current distribution model for the species. MAXENT vers. 3.3.3k (Phillips et al. 2006, 2008, 2009) program was used to model the potential distribution of the species. The MAXENT algorithm estimates the potential distributions of species from locality point data by finding the probability distribution of the maximum entropy (i.e. closest to uniform) subject to the constraint that the expected value of each of a set of features (environmental variables or functions thereof) under this estimated distribution closely matches its empirical average (Phillips et al. 2006, 2008). MAXENT logistic outputs represent the habitat suitability ranging from 0 (unsuitable) to 1 (suitable). The randomly selected background (pseudoabsences) approach (Phillips et al. 2006) and 15fold crossvalidation were used in modeling. We applied the 10 percentile training presence logistic threshold approach as recommended by Liu et al. (2005), and the logistic output was transformed into a continuous map of the presenceabsence distribution. Model accuracy was evaluated from Area under the receiveroperator curve (AUC), and the average of all models was imported and visualized with ArcGIS v9.0. Results Xerotyphlops vermicularis (Merrem, 1820) Material: N= 2 OMUK student material, between Ladik and Taşova, the Collection of Ondokuz Mayıs University, leg. Y.Tayhan, coordinates= 40.873919 0 N, 36.095744 0 E, Material: N=10: CBU 1/2014, 14 +, Boyabat, Sinop, 28.04.2014, Leg. M.Afsar, Coordinates= 34.76193 0 N, 41.46702 0 E, 445 m a.s.l. CBU 2/2014, 510 +, Çarşak, Boyabat, Sinop, 09.07.2014, Leg.= M.Afsar, coordinates= 34.90515 0 N, 41. 463395 0 E, 282 m a.s.l. General appearance and pholidosis: The ground colour of the dorsum is particularly light or dark brown in the eight specimens under examination, while it is pinkish pale brown in the two specimens from Çarşak (Sinop). The ventral side is yellowish white in all specimens. The tail width and length are almost equal to each other. There is a spike at the tip of the tail. The eyes have become blind and look like black points under the ocular plates. The rostral scale, the largest plate among the head plates, originates from the rim of the mouth in the lower part and continues as far as the top of the head. There is a pair of nasalia. The preocular scale is 1/1; the supralabial scales are 4/4; the sublabial scales are 4/4; the midbody scale rows are counted as 24 in 11 specimens and as 22 in one specimen; and the midtail scale rows are 17 in one specimen, 18 in four specimens, 19 in two specimens, 20 in four specimens, and 21 in one specimen. The number of scales in the anal region is 5. The head+body length ranges from 185 to 248 mm in the specimens under examination. The tail length was measured to be between 2.01 and 5.08 mm. The pholidosis characteristics and the statistical values of the body measurements and rates are presented in Table 1. Biological and ecological observations: The four specimens caught within the city walls of the Boyabat Castle were found under the stone fragments in the rocky regions where the Gramineae vegetation partially prevailed (Fig. 1). On the other hand, the specimens detected from the Çarşak village were collected from the sparsely vegetated and stony areas by a desiccated stone channel. The specimens obtained from both localities were encountered in the afternoon. Stelliagama stellio were also encountered at the Boyabat Castle; however, the specimens could be observed as the castle was a protected site. Table 1. Summary statistics of pholidosis, morphometric measurements (in millimeters) and ratios of X.vermicularis from SinopSamsun. Characters N Mean SE Min Max SD VentralRostral Length (VL) 12 204.83 4.99 185 248 17.30 Tail Length (TL) 12 3.49 0.26 2.01 5.08 0.90 Midbody Diamater (MBD) 12 4.40 0.13 3.66 5.01 0.45 Tail Diamater (TD) 12 3.45 0.19 2.50 4.33 0.67 Total Length (TOL) 12 208.38 5.23 188.10 253.80 18.12 Head Width (HW) 12 3.07 0.10 2.5 3.6 0.37 Head Length (HL) 12 2.84 0.06 2.33 3.09 0.22 Rostral Width (RW) 12 1.16 0.04 1.03 1.55 0.15 Rostral Length (RL) 12 1.67 0.05 1.39 2.02 0.18 Internarial Distance (ID) 12 1.81 0.06 1.55 2.21 0.22 Preocular Width (ProW) 12 0.80 0.01 0.70 0.90 0.05 Preocular Heigth (ProH) 12 1.54 0.05 1.25 1.85 0.19 Ocular Width (OW) 12 0.96 0.04 0.77 1.27 0.15 Ocular Heigth (OH) 12 1.71 0.02 1.52 1.88 0.08 HW/HL 12 1.08 0.02 0.89 1.25 0.08 TL/TOL 12 0.01 0.00 0.009 0.02 0.00 TOL/MBD 12 47.54 1.17 42.93 53.65 4.06 TL/MBD) 12 1.04 0.089 0.57 1.52 0.31 Supralabialia (SpL) 12 4 0.00 4 4 0.00 Sublabialia (SbL) 12 4 0.00 4 4 0.00 Midbody scale rows (MSR) 12 23.83 0.16 22 24 0.57 Midtail scale rows (MtSR) 12 19.00 0.34 17 21 1.20 Subcaudals (SC) 12 9.83 0.34 8 11 1.19 Total Scale row (TSR) 12 392.67 2.237 380 408 7.75

100 M. Afsar et al. quite high (0.80). According to the model, the primary factors affecting the distribution of the species are the annual mean temperature (bio1, 55.3%), precipitation of driest month (bio14, 18.5%), and mean diurnal range [mean of monthly (max temp min temp)] (bio2, 10.1%). These parameters explain about 93% of the distribution of the species. The contributions of the other variables range from 1.4 to 6.9 (annual temperature range [bio5 bio6] (bio7, 6.9%), mean temperature of wettest quarter (bio8, 3%), isothermality [bio2 / bio7] [* 100] (bio3, 1.8%), and precipitation seasonality [coefficient of variation] (bio15, 1.4%)). Discussion Figure 1. Habitat of Xerotyphlops vermicularis from Boyabat Castle (Sinop, Backsea Region) Distribution: The species is generally widely observed in Western and Southern Anatolia (Figs 2 and 3). The mean AUC values of the current distribution consensus model are Our results reveal that the pholidolial, colourpattern and morphometric characteristics of the specimens were generally similar with the literature (Tok 1993, Kumlutaş et al. 2004, Franzen et al. 2008, Afsar & Tok 2011, Afroosheh et al. 2013, Hedges et al. 2014) (Table 2). The variation of the midbody scale rows was provided as 2224 in the above Figure 2. The current potential distribution model of Xerotyphlops vermicularis in Turkey. The circles denote the known literature records, whereas the stars denotes the new locality. Figure 3. Habitat suitability of Xerotyphlops vermicularis in Turkey. Red indicating suitable habitat and and green representing unsuitable habitat.

New records of Xerotyphlops vermicularis from the Black Sea region of Turkey and its updated distribution 101 C Table 2. Comparison of the morphometric measurements and pholidosis of X.vermicularis from SinopSamsun with literatüre. The present study SinopSamsun specimens (n=12) SL 4 (44) SbL 4 (44) Baran (1982) SW and E Anatolia N=31 Tok (1992) Datça peninsula (n=5) (33) MSR 23.83± 0.57 (2224) (2224) (2224) MtSR 19.00± 1.20 (1721) (1721) SC 9.83±1.19 (811) TSR 392.67±7.75 (380408) TOL 208.38±18.12 (188.10253.80) VL 204.83±17.30 (185248) TL 3.49±0.90 (2.015.08) MBD 4.40±0.45 (3.665.01) MTD 3.45±0.67 (2.504.33) HL 2.84±0.22 (2.333.09) HW 3.07±0.37 (2.53.6) RW 1.16±0.15 (1.031.55) RL 1.67±0.18 (1.392.02) 9.94 (712) Kumlutaş et al. (2004) W. Taurus (n=9) M Franzen et al. (2008) Köyceğiz (n=30) 2 (22) (44) 3 (33) 23.22 (2224) (2224) 20.77 (2021) Afsar and Tok (2011) Sultan M. (n=5) M 3 (33) Afroosheh et al. (2013) Turkey n=16 Hedges et al. (2014) M (713) 23 (2224) 20.33 (2021) (137214) 190.12 (101.32243.22) 195±4.0 (100.8260.4) 190.3±3.90 (100.70260) 3.0±0.1 (1.05.0) 231.80 (198262) 22.93±0.09 (2224) 23.5 (2224) 9.31±1.07 (711) 390±22.70 357440 178±38.66 (96.79247.92) 355 (206435) 292 (220350) 3.05±0.63 (1.923.84) 3.64±0.93 (2.015.45) 2.76±0.52 (1.823.73) 2.89±0.48 (2.144.07) 2.66±0.40 (1.923.60) 1.16±0.20 (0.751.61) 1.86±0.33 (1.412.67) mentioned studies. In the specimens examined from Sinop and Samsun, the variation of this character (range= 2224, mean= 23.83) is in agreement with the other populations compared (midbody scale rows MSR). Furthermore, the mean value of the total scale rows (Total Scale row TSR) (380408, 392.67) and the mean value of the number of subcaudals (Subcaudals, SbC) (811, 9.83) in our specimens are congruent with the mean values of the specimens examined from the other regions of Turkey (Table 2). On the other hand, the mean value of the midtail scale rows in our specimens from Sinop and Samsun was found slightly lower than the mean value of the specimens from the Western Taurus and Sultan Mountains. Nevertheless, the variation of this value (1721, 19) (Midtail scale rows MtSR) is in agreement with the specimens from the Datça peninsula. The number of supralabial scales (4) in our specimens was found similar to the specimens from Thrace and Southwestern Anatolia (Table 2). The numbers of supralabial scales (SpL) were provided in different values in the specimens examined from the other regions (Datça peninsula as well as the Western Taurus and Sultan Mountains), which might have resulted from researchers ways of counting. As a result of comparing the variation limits of the values of the total body length (TOL), the head+body length, and the Tail length (TL) out of the metric characters measured in the present study and the data obtained from the literature, no significant differences were detected between the specimens from Sinop and Samsun and the populations known from the other regions of Turkey (Table 2). Additionally, when the values of HL, RW, MBD, TD and HW were compared with the data by Afroosheh et al. (2013), the Head length (HL) and the Rostral width (RW) were found similar to the values provided for the specimens examined from Turkey; the midbody diameter (MBD), the Tail Diameter (TD) and the Head Width (HW) were found slightly high; and the Rostral length (RL) was found at a slightly low mean value. According to the molecular data, Kornilios et al. (2012) stated that X. vermicularis was represented by 10 distinct lineages within its whole distributional area but by 6 distinct lineages in Anatolia. No significant differences in meristic and metric characters were detected among the 12 populations examined by Afroosheh et al. (2013), who comparatively evaluated the geographical variation of the morphometric characters in the populations of X.vermicularis in Iran, Turkey, and Turkmenistan. In the study concerned, it was thereupon stated that X. vermicularis was a homogeneous and preserved taxon in terms of morphological charac

102 ters despite its occupation of different habitats within its wide distributional range. In the present study, the view concerned was supported by determining that there were no marked differences between the mean values or variation limits of the characters examined on the specimens from Sinop and Samsun and the literature data. Furthermore, there is a need for the studies which will reveal new distributional areas of X.vermicularis in the Black Sea Region. The taxonomic situations of the populations inhabiting Northern Anatolia can be set forth by making a detailed morphological and molecular evaluation of the specimens belonging to the new populations to be determined from the north of Turkey. Even though genus Xerotyphlops is generally distributed in xeric regions (Hedges et al. 2014), X.vermicularis generally prefers more humid microhabitats (Kornilios et al. 2011) and X.socotranus often inhabits biotopes with little moisture and vegetation (Razzetti et al. 2011). Gül et al. (2015) state that there are significant bioclimatic factors for the species, namely annual mean temperature (bio1), mean temperature of the coldest quarter (bio11), and precipitation seasonality (bio15). In this study as well, it was observed that the annual mean temperature, precipitation of driest month and mean diurnal range were effective on the distribution of the species. This implies temperature and precipitation fluctuation mainly affected distribution of the species. In conclusion, by incorporating new localities into the distributional areas of X.vermicularis in the Black Sea Region, its distributional range in Northern Anatolia was extended as far as Sinop and the northernmost border of the distributional range of the species in Anatolia was determined as Sinop. Acknowledgements. 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