Morphology and blood proteins of Dice snakes from western Turkey.

370

© 2011 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Rheinbach, Germany

Morphology and Blood Proteins of Dice Snakes from Western Turkey*

Yunus Emre Dinçaslan, Hüseyin Arikan, İsmail Hakki Uğurtaş & Konrad Mebert

Abstract. Dice snakes Natrix tessellata from the Lakes Region in southwestern Turkey (Beyşehir, Akşehir-Eber, Kar-amuk lakes) and from Uluabat Lake, Marmara Region in northwestern Turkey were compared by means of morphol-ogy (pholidosis, body measurement ratio, color pattern) and blood-serum proteins that were analyzed by polyacryla-mide gel electrophoresis and densitometry methods. Pholidosis (number of preocular and supralabial scales) and color-pattern, as well as electrophoretic figures of blood serum proteins, showed significant differences between the dice snakes from Beyşehir Lake compared to those of other lakes in the region, as well as those from Uluabat Lake. Some thoughts on those differences and its relevance to taxonomic questions are presented.

Key words. Ophidia, colubridae, morphology, polyacrylamide gel electrophoresis, south- and northwestern Turkey.

Introduction

The dice snake Natrix tessellata (Laurenti, 1768) has a widespread distribution from Germany and Italy in the west to southeast Europe and Egypt in the south, across Russia and Arabian countries to Central Asia such as North Afghanistan (possibly North Pakistan) and West China (Gruschwitz et al. 1999, Sindaco et al. 2000). This species can be found across Turkey up to an alti-tude of 2500 m in suitable biotopes (Başoğlu & Baran 1980). There are many studies that tried to shed light on the taxonomy and systematic of N. tessellata. Initial tax-onomic grouping was based on morphological compar-isons, including morphometric characters and ratios, pholidosis and color-pattern (Strauch 1873, Bedria-ga 1879, Boettger 1888, Boettger 1890, Schreiber 1912, Venzmer 1919, Werner 1902, Werner 1903, Wer-ner 1919, Hecht 1930, Bodenheimer 1944, Mertens & Wermuth 1960, Fuhn & Vancea 1961, Kramer & Schnurrenberger 1963, Mertens 1969, Baran 1976, Lanka 1978, Lenz & Gruschwitz 1993, Mebert 1993, 1996, and Göçmen & Böhme 2002). Baran (1976) in-dicated that N. tessellata from Turkey is consistent with the nominate subspecies N. tessellata tessellata. Howev-er, only one supposedly morphologically distinct sub-species has been accepted up to the last century (Hecht 1930), with that being questioned as well by Grus-chwitz et al. (1999).

The first indication of a different Natrix tessellata subspecies living in Turkey originated from Bedria-ga’s (1879) assignation of dice snakes caught around Çanakkale, Trabzon, and Valley Fırat as Tropidonotus hydrus (based on Pallas’ 1771 Coluber hydrus with typ-ically 3 preoculars and 4 postoculars), whereby Tropi-donotus is the former generic name of Natrix. Although Boettger (1888, 1890), Venzmer (1919) and Wer-ner (1902, 1919) agreed with this idea for Turkish dice

* Some data in this manuscript were included in the Ph.D. thesis of Yunus Emre Dinçaslan.

snakes, Dürigen (1897), Schreiber (1912), Hecht (1930), Bodenheimer (1944), and Mebert (2011) re-ported variably that the arrangements of ocular scales exhibits a more complex geographic variation and that 3 preocular and 4 postouclar scales were also found in samples from other areas of N. tessellata. Therefore, the former authors declared T. hydrus and N. tessellata as synonyms, which was followed by other authors for dice snakes from the same general area (e.g. Mertens 1969, Gruschwitz et al. 1999, Mebert 2011).

Other described subspecies of the dice snake from Turkey have been disregarded after additional analyses. For example, Baran (1976) suggested in his review of material collected across Turkey that N. tessellata vos-seleri (Werner 1914) from the area between Antalya and Burdur should be accepted as synonymous with the nominate subspecies. Hecht (1930) described N. vipe-rinus from Turkey. But Mertens & Wermuth (1960) declared that the characteristics of N. viperinus actually belonged to N. maura, a closely relates species whose nearest populations are 1000s of km away in northern Italy. Kramer & Schnurrenberger (1963) also shared this idea of those individuals being N. maura, whereas Baran (1976) accepted N. viperinus as a synonym of the nominate species (N. tessellata). Regardless, whether the former ssp. designation originates from, for example, mislabeled and foreign N. maura or whether those Na-trix specimens are somewhat aberrant Turkish N. tessel-lata, there is no clear argument based on morphological data to maintain any other taxonomic unit for Turkey than the nominate form up to this moment. However, genetic investigation indicates that northern and east-ern Turkey (southern, central and western areas have not been studied) is inhabited be a different clade of N. tessellata than specimens from the extreme northwest-ern area of Turkey (Guicking et al. 2009, Guicking & Joger 2011).

MERTENSIELLA 18 370-382 20 September 2011 ISBN 978-3-9812565-4-3

371


Due to the extensive and often clinal variation of morphological characters across the vast range of dice snakes (see Mebert 2011), it may not be sufficient to elaborate the taxonomic and systematic arrangement in this species based on morphological properties alone. In order to fine-scale the morphological variation, test for geographic differences and infer phylogeographic pat-tern and determine taxonomic affiliations for N. tessel-lata from western Turkey, dice snakes from populations in the Lakes Region and from the Marmara Region were compared, morphologically and serologically.

Material and Methods

A total of 93 dice snakes, Natrix tessellata, were collect-ed from the Lakes Region in southwestern Turkey (Fig. 1): lakes of Beyşehir (15 females, 18 males, 3 juveniles), Akşehir-Eber (10 females, 8 males, 11 juveniles), Eğirdir (none found), Karamuk (6 females, 4 males), and from the Uluabat Lake, Marmara Region in northwestern Turkey (7 females, 10 males, 1 juvenile). Each specimen was photographed before they were fixed with 4% for-maldehyde in 70% ethanol, and subsequently preserved in 70% ethanol, as described by Başoğlu & Baran (1980). All samples were deposited at ZDEU, the Mu-seum of the Zoological Department, Aegean University (see Appendix). Snakes from the Akşehir and Eber lakes were combined for this analysis, as these lakes are con-nected over a short distance by the canal of Taşköprü.

Following morphological characters were record-ed: preoculars, postoculars, temporal scales, sublabi-als, supralabials, gular scales, dorsal scales, anal plate, supracaudals, ventrals, and various body proportions. Kruskall-Wallis test was applied to investigate differenc-es in non-parametric characters, such as the pholidosis. Mann-Whitney U tests were performed to investigate specific differences among the lakes. To test for differ-ences in body proportions among populations, males and females were lumped for a subsequent ANOVA. Tukey dispersion test method was selected from Multi-ple Comparisons options of ANOVA.

For the serological investigation, blood was taken from the postorbital sinuses following Maclean et al. (1973) and was centrifuged at 600 g for 5 minutes, and subsequently stored at -20 C before further analysis. Electrophoretic separation of the blood-serum proteins was performed according to Özeti & Atatür (1979) and Davis (1964), using a “Canalco Model 1200” appa-ratus at room temperature. Gels containing separated proteins were stained with 0.5% Amido Black (Naphtol Blue Black 10-B) stain. Excessive stain was removed pas-sively by 7% acetic acid baths. Qualitative evaluations of the gels were made directly from electropherograms. Densitometry curves of the separations were obtained from Gelman ACD-15 39430 densitometry at 500 nm and photographed.

Digital calipers with 0.001 mm precision were used for obtaining biometric parameters. All statistical analy-ses for comparing the pholidosis, body proportions and ratios were processed using SPSS 10.0, Statistica 5.4 and MS Office Excel programs. Analyses were considered to be significant at the 95% confidence level (p < 0.05).

Results and DiscussionMorphometric and Pholidotic Analysis

Mean, standard deviation, and range of pholidosis of the dice snake, Natrix tessellata, from western Turkey are presented in Table 1. Three preocular scales are most common (61.3%), followed by 2 preoculars (35.4%) and

Fig. 1. Collected localities of Natrix tessellata. 1. Uluabat Lake, 2. Eber Lake, 3. Akşehir Lake, 4. Karamuk Lake, 5. Eğirdir Lake, 6. Beyşehir Lake.

372

Morphology and Blood Proteins of Dice Snakes from Western Turkey

Beyşehir LakeCharacters

Females Malesn Ext. M ± SE SD n Ext. M ± SE SD

Preoculars 15 2–3 2.87 ± 0.12 0.35 18 2–3 2.89 ± 0.14 0.32Postoculars 15 3–4 3.93 ± 0.12 0.26 18 3–4 3.89 ± 0.14 0.32Temporals 15 3–3 3.00 ± 0.00 0.00 18 3–4 3.06 ± 0.12 0.24Sublabials 15 9–10 9.67 ± 0.13 0.49 18 9–10 9.67 ± 0.11 0.49Supralabials 15 8–9 8027 ± 0.12 0.46 18 7–9 8.06 ± 0.15 0.64Gulars 15 3–6 4.00 ± 0.29 1.13 18 3–6 4.50 ± 0.32 1,34Dorsal scales 15 19–19 19.00 ± 0.00 0.00 18 19–19 19.00 ± 0.00 0.00Anal scale 15 2–2 2.00 ± 0.00 0.00 18 2–2 2.00 ± 0.00 0.00Subcaudals 15 60–72 64.73 ± 1.00 3.88 18 56–72 64.50 ± 1.11 4.72Ventral 15 161–182 174.60 ± 1.76 6.82 18 167–185 175.78 ± 1.16 4.91Beyşehir LakeCharacters

JUV JUV + both sexesn Ext. M ± SE SD n Ext. M ± SE SD

Preoculars 3 3–3 3.00 ± 0.00 0.00 36 2–3 2.89 ± 0.15 0.32Postoculars 3 4–4 4.00 ± 0.00 0.00 36 3–4 3.92 ± 0.14 0.28Temporals 3 3–3 3.00 ± 0.00 0.00 36 3–4 3.03 ± 0.12 0.17Sublabials 3 9–9 9.00 ± 0.00 0.00 36 9–10 9.61 ± 0.18 0.49Spralabials 3 7–8 7.67 ± 0.33 0.58 36 7–9 8.11 ± 0.19 0.57Gulars 3 4–4 4.00 ± 0.00 0.00 36 3–6 4.25 ± 0.20 1.20Dorsal scales 3 19–19 19.00 ± 0.00 0.00 36 19–19 19.00 ± 0.00 0.00Anal scale 3 2–2 2.00 ± 0.00 0.00 36 2–2 2.00 ± 0.00 0.00Subcaudals 3 58–67 61.67 ± 2.73 4.73 36 56–72 64.36 ± 0.72 4.34Ventrals 3 175–179 176.67 ± 1.20 2.08 36 161–185 175.36 ± 0.93 5.57Akşehir–Eber L.Characters


Preoculars 10 1–3 2.40 ± 0.27 0.84 8 1–3 2.63 ± 0.26 0.74Postoculars 10 3–4 3.60 ± 0.16 0.52 8 3–4 3.63 ± 0.18 0.52Temporale 10 3–4 3.50 ± 0.17 0.53 8 3–4 3.25 ± 0.16 0.46Sublabials 10 9–10 9.30 ± 0.15 0.48 8 9–10 9.13 ± 0.12 0.35Supralabials 10 7–8 7.70 ± 0.15 0.48 8 7–8 7.25 ± 0.16 0.46Gulars 10 3–6 4.80 ± 0.33 1.03 8 4–6 4.63 ± 0.32 0.92Dorsal scales 10 19–19 19.00 ± 0.00 0.00 8 19–19 19.00 ± 0.00 0.00Anal scales 10 2–2 2.00 ± 0.00 0.00 8 2–2 2.00 ± 0.00 0.00Subcaudals 10 53–72 62.00 ± 1.71 5.40 8 59–74 67.00 ± 1.93 5.45Ventrals 10 168–185 174.80 ± 1.76 5.57 8 168–179 174.88 ± 1.16 3.27Akşehir–Eber L.Characters


Preoculars 11 2–3 2.73 ± 0.14 0.47 29 1–3 2.59 ± 0.13 0.68Postoculars 11 3–4 3.85 ± 0.10 0.34 29 3–4 3.70 ± 0.08 0.46Temporals 11 3–4 3.09 ± 0.09 0.30 29 3–4 3.28 ± 0.08 0.45Sublabials 11 9–9 9.00 ± 0.00 0.00 29 9–10 9.14 ± 0.07 0.35Supralabials 11 7–8 7.82 ± 0.12 0.40 29 7–8 7.62 ± 0.09 0.49Gulars 11 4–6 5.45 ± 0.28 0.93 29 3–6 5.00 ± 0.19 1.00Dorsal scales 11 19–19 19.00 ± 0.00 0.00 29 19–19 19.00 ± 0.00 0.00Anal scales 11 2–2 2.00 ± 0.00 0.00 29 2–2 2.00 ± 0.00 0.00Supracaudals 11 60–72 66.55 ± 1.18 3.91 29 53–74 65.10 ± 0.97 5.25Ventrals 11 171–182 176.64 ± 0.96 3.17 29 168–185 175.52 ± 0.77 4.13

Tab. 1. Pholidosis values of dice snakes from lakes Uluabat, Eber, Akşehir, Karamuk, and Beyşehir, western Turkey.

373

Karamuk LakeCharacters


Preoculars 6 2–3 2.50 ± 0.22 0.55 4 2–2 2.00 ± 0.00 0.00Postoculars 6 3–4 3.67 ± 0.21 0.52 4 4–4 4.00 ± 0.00 0.00Temporals 6 3–4 3.67 ± 0.21 0.52 4 4–4 4.00 ± 0.00 0.00Sublabials 6 9–10 9.33 ± 0.21 0.52 4 9–10 9.75 ± 0.25 0.50Supralabials 6 7–8 7.33 ± 0.21 0.52 4 7–8 7.25 ± 0.25 0.50Gulars 6 4–6 5.50 ± 0.34 0.84 4 6–6 6.00 ± 0.00 0.00Dorsal scales 6 19–19 19.00 ± 0.00 0.00 4 19–19 19.00 ± 0.00 0.00Anal scales 6 2–2 2.00 ± 0.00 0.00 4 2–2 2.00 ± 0.00 0.00Subcaudals 6 56–65 58.83 ± 1.66 4.07 4 51–57 53.75 ± 1.60 3.20Ventrals 6 166–174 171.00 ± 1.46 3.58 4 165–175 169.00 ± 2.16 4.32Karamuk LakeCharacters


Preoculars – – – – 10 2–3 2.30 ± 0.15 0.48Postoculars – – – – 10 3–4 3.80 ± 0.13 0.42Temporals – – – – 10 3–4 3.80 ± 0.13 0.42Sublabials – – – – 10 9–10 9.50 ± 0.17 0.53Supralabials – – – – 10 7–8 7.30 ± 0.15 0.48Gulars – – – – 10 4–6 5.70 ± 0.21 0.67Dorsal scales – – – – 10 19–19 19.00 ± 0.00 0.00Anal scales – – – – 10 2–2 2.00 ± 0.00 0.00Subcaudals – – – – 10 51–65 56.80 ± 1.40 4.42Ventrals – – – – 10 165–175 170.20 ± 1.20 3.79

Uluabat LakeCharacters


Preoculars 7 2–3 2.57 ± 0.20 0.53 10 2–3 2.50 ± 0.17 0.53Postoculars 7 3–5 3.71 ± 0.29 0.76 10 3–4 3.80 ± 0.13 0.42Temporals 7 3–3 3.00 ± 0.00 0.00 10 3–3 3.00 ± 0.00 0.00Sublabials 7 9–10 9.43 ± 0.20 0.53 10 9–10 9.40 ± 0.16 0.52Supralabials 7 8–9 8.14 ± 0.14 0.38 10 8–9 8.10 ± 0.10 0.32Gulars 7 3–5 3.57 ± 0.30 0.79 10 3–5 3.80 ± 0.25 0.79Dorsal scales 7 19–19 19.00 ± 0.00 0.00 10 19–19 19.00 ± 0.00 0.00Anal scales 7 2–2 2.00 ± 0.00 0.00 10 2–2 2.00 ± 0.00 0.00Subcaudals 7 64–79 66.33 ± 0.71 1.75 10 64–79 68.20 ± 1.31 4.13Ventrals 7 170–178 173.29 ± 0.99 2.63 10 170–186 175.20 ± 1.55 4.92Uluabat LakeCharacters


Preoculars 1 3 3.00 ± 0.00 – 18 2–3 2.56 ± 0.12 0.51Postoculars 1 4 4.00 ± 0.00 – 18 3–5 3.78 ± 0.13 0.55Temporals 1 3 3.00 ± 0.00 – 18 3–3 3.00 ± 0.00 0.00Sublabials 1 10 10.00 ± 0.00 – 18 9–10 9.44 ± 0.12 0.51Supralabials 1 8 8.00 ± 0.00 – 18 8–9 8.11 ± 0.70 0.32Gulars 1 3 3.00 ± 0.00 – 18 3–5 3,67 ± 0.18 0.77Dorsal scales 1 19 19.00 ± 0.00 – 18 19–19 19.00 ± 0.00 0.00Anal scales 1 2 2.00 ± 0.00 – 18 2–2 2.00 ± 0.00 0.00Subcaudals 1 64 64.00 ± 0.00 – 18 64–79 67.29 ± 0.84 3.48Ventrals 1 174 174.00 ± 0.00 – 18 170–186 174.39 ± 0.95 4.02

Tab. 1. (continued)


374

3 specimens from Akşehir with only 1 preocular (3.2%). Specimens with 4 preoculars, reported by Mebert (1993) from the lakes Brienz and Geneva in Switzerland, were encountered neither in this study nor by Baran (1976) from other parts of Turkey. The mean value of preocular and supralabial scales were found to signifi-cantly differ among the populations studied here (p < 0.05). The preoculars of dice snakes from Beyşehir had a slight but significantly higher mean than those of dice snakes from Akşehir, Karamuk, and Uluabat (Tab. 2). This is due to a higher proportion of specimens with 3 preoculars in the Beyşehir population than in the other ones. But the general trend of exhibiting rather 3 than 2 preoculars confirms the general pattern for dice snakes from south of a geographic line between the Hungar-ian Plains to the Dalmatian Coast of Croatia and east of the Carpathian Mountains (see refs. in Gruschwitz et al. 1999) and was found in other areas in Turkey (Black Seas coast and northeastern Turkey; Mebert 1993, Me-bert 2011). But Mebert (1993, 1996) showed, that even in some western European populations of dice snakes, a preponderance of 3 versus 2 precoulars can exist, hence, rendering this character less suitable for large, regional separation of dice snakes.

Postocular scales are 5 in 4 specimens (4.3%), 4 in 68 specimens (73.12%) and 3 in 21 specimens, which is in accordance with the general findings summarized in Gruschwitz et al. (1999) and Mebert (1993). Findings of Baran (1976) were in accordance with the findings of Başoğlu & Baran (1980) and Baran & Atatür (1988). Specimens with only 2 postoculars, as mentioned by Lanka (1978), Lenz & Gruschwitz (1993), and Me-bert (1993) for many specimens from the Czech Repub-lic, Germany, and Switzerland respectively, were not en-countered in this study, but do occur at a low frequency in Turkey (Mebert 1993, 2011).

The supralabial scales in all the populations were predominantly 8 in 65 specimens (69.9%), 7 in 22 spec-imens (23.7%), and 9 in 6 specimens (6.6%) in accor-dance with current literature. The number of temporal, supralabial, sublabial and gular scales were also consis-tent with the current literature (Baran 1976, Başoğlu & Baran 1980, Baran & Atatür 1988, Mebert 1993). The mean of supralabials showed significant differences between the Beyşehir-Akşehir and Beyşehir-Karamuk populations (Tab. 3).

The number of ventral scales varies geographically little in our study area (Tab. 1), and is generally higher in males (mean = 175.5) than females (mean = 173) across all populations in this study. The data we have found is tentatively in accordance with the literature, albeit the sexualdimorphic difference is rather small within and between populations and even reversed for the speci-mens from Lake Karamuk. For males, Baran (1976) re-ported a value of 172.4 ventrals as an average across all Turkey. Mebert (1993) reported a mean of 171.4 (n = 7) and 168.0 (n = 6) ventrals for male and female dice snakes from Akşehir. Even though, the sample size for his Aksehir dice snakes is a little lower than in this study, the difference between the sexes was evident. Con-cerning the situation across all Turkey, Mebert (1993) showed a high geographic variation of ventral counts in Turkey, with mean values of ~175 for males from the Black Sea coast, 178.4 for males from the Northeast Tur-key (region between Kars and Van Lake), 173.1 for the Turkish west coast, and 172.0 for southeastern Turkey (region between Urfa and Adiyaman). Comparatively for female dice snakes, Baran (1976) found an average of 168.8 ventrals, whereas 171.2 ventrals were reported for the Black Sea coast, 174.0 for the Northeast Turkey, 167.1 for the Turkish west coast, and 166.5 for southeast-ern Turkey (Mebert 1993). A constant and average gen-der difference of 5 scales for the number of ventrals was found across the entire range of N. tessellata (Mebert 1993, Gruschwitz et al. 1999, Mebert 2011), includ-ing Turkey (see above). The decreased sexualdimorphic expression of ventrals in our study may partly due to the small sample size in some of the populations inves-tigated herein, and partly may be based on uncertainties of sex determination. Only further investigations could clarify some of the inconsistencies.

Similarly, a lack of sexualdimorphic expression was also found for the subcaudal scales with an average value of 65 (range 51 to 79) in males and 66 in females (range 53 to 79). This is inconsistent with Baran (1976), who found an average difference of approximately 10 scales between the gender, with 70 subcaudals for males and 61 for females. Mebert (1993) showed similar ventral mean values for males from Akşehir, 68 (n = 7) vs. 67 (n = 8) in this study, but females showed substantially low-er mean values of 56 (n = 5) in Mebert (1993) vs. 62 (n = 10) in this study (see Tab. 1). Mebert (1993) indicated

Preocular scalesPopulations U W PBeyşehir-Akşehir 412.000 847.000 0.037Beyşehir-Karamuk 74.000 129.000 0.000Beyşehir-Uluabat 216.000 387.000 0.000

Supralabial scalesPopulations U W PBeyşehir-Akşehir 310.000 745.000 0.001Beyşehir-Karamuk 62.000 117.000 0.000Beyşehir-Uluabat 320.000 491.000 0.924

Tab. 3. Mann-Whitney-U test evaluation of the number su-pralabial scales with significant differences among popula-tions based on a Kruskall-Wallis analysis (see Tab. 2 for col-umn discriptors).

Tab. 2. Mann-Whitney-U test evaluation of the number of preocular scales that showed significant differences among populations according to the result of Kruskall-Wallis analy-sis. U: Mann-Whitney-U value, W: Kruskall-Wallis value, P: significance level.


375

Tab.

4. M

orph

omet

ric d

ata

and

ratio

s in

both

sexe

s of N

atrix

tess

ellat

a fr

om se

lect

ed p

opul

atio

ns in

wes

tern

Tur

key.

RH: R

ostr

al H

eigh

t, RW

: Ros

tral

Wid

th, F

L: F

ront

al L

engt

h, F

W:

Fron

tal W

idth

, HL:

Hea

d Le

ngth

from

the

tip o

f the

rosr

al sc

ale

to th

e po

ster

ior e

nd o

f the

par

ieta

l sca

le, H

W: H

ead

Wid

th a

s the

gre

ates

t tra

nsve

rse

dist

ance

bet

wee

n th

e su

prao

cula

r sc

ales

, BL:

Bod

y Le

ngth

(=

SVL)

, TL:

Tai

l Len

gth,

RW

/RH

: Ros

tral

Rat

io, F

W/F

L: F

ront

al R

atio

, HW

/HL:

Hea

d Ra

tio, T

L/BL

: Tai

l Rat

io)

(a. B

eyşe

hir

Popu

latio

n, b

. Akş

ehir–

Eber

Po

pula

tion,

c. K

aram

uk P

opul

atio

n, d

. Ulu

abat

Pop

ulat

ion)

.

Beyş

ehir

Lake

Cha

ract

ers

Fem

ales

Mal

esBo

th se

xes

nEx

t.M

± S

ESD

nEx

t.M

± S

ESD

nEx

t.M

± S

ESD

RH

151.

8–3.

62.

88 ±

0.1

60.

6318

1.9–

3.4

2.66

± 1

.11

0.46

331.

8–3,

62.

76 ±

0.0

90.

55RW

152.

58–5

.21

4.16

± 0

.23

0.89

183.

02–5

.27

4.02

± 0

.13

0.53

332.

58–5

.27

4.08

± 0

.12

0.71

FL15

3.99

–7.5

16.

16 ±

2.2

91.

1218

4.32

–7.1

86.

02 ±

0.1

50.

6533

3.99

–7.5

16.

08 ±

0.3

50.

88FW

152.

82–5

.14

3.84

± 0

.17

0.66

183.

07–5

.54

3.93

± 0

.13

0.54

332.

82–5

.54

3.89

± 0

.10

0.59

HL

1511

.63–

24.0

218

.16

± 1.

003.

8618

15.2

1–22

.50

18.2

1 ±

0.51

2.15

3311

.63–

24.0

218

.19

± 0.

523.

00H

W15

5.60

–10.

918.

59 ±

0.4

51.

7518

7.08

–10.

368.

66 ±

0.2

20.

9533

5.60

–10.

918.

63 ±

0.2

31.

35BL

1532

1–83

058

5 ±

41.3

316

0.09

1846

1–71

056

2.58

± 1

6.77

71.1

533

321–

830

572.

77 ±

20.

6211

8.45

TL15

50.1

–180

.713

6.44

± 9

.62

37.2

718

110.

20–1

70.5

014

2.59

± 4

.77

18.9

933

50.1

–180

.713

9.80

± 4

.95

28.4

4RW

/RH

151.

29–1

,57

1.45

± 0

.02

0.09

181.

13–2

.26

1.55

± 0

.07

0.30

331.

13–2

.26

1.50

± 0

.04

0.23

FW/F

L15

0.50

–0.7

20.

63 ±

0.0

20.

0618

0.55

–0.8

60.

65 ±

0.0

20.

0733

0.50

–0. 8

60.

64 ±

0.0

10.

07H

W/H

L15

0.42

–0.5

70.

48 ±

0.0

10.

0418

0.43

–0.5

80.

48 ±

0.0

10.

0433

0.42

–0.5

80.

48 ±

0.0

10.

04TL

/BL

150.

15–0

.30

0.23

± 0

.01

0.04

180.

21–0

.29

0.25

± 0

.01

0.03

330.

15–0

.30

0.25

± 0

.01

0.03

Akş

ehir-

Eber

La

kes C

hars

.Fe

mal

esM

ales

Both

sexe

sn

Ext.

M ±

SE

SDn

Ext.

M ±

SE

SDn

Ext.

M ±

SE

SDR

H10

1.76

–3.7

62.

74 ±

0.2

10.

668

1.64

–3.7

52.

52 ±

0.2

50.

7218

1.64

–3.7

62.

64 ±

0.1

60.

68RW

102.

36–5

.92

4.46

± 0

.30

0.94

82.

68–5

.31

3.89

± 0

.37

1.05

182.

36–5

.92

4.20

± 0

.24

1.00

FL10

3.34

–7.3

86.

10 ±

0.3

61.

148

3.77

–7.1

55.

34 ±

0.4

21.

2018

3.34

–7.3

85.

76 ±

0.2

81.

19FW

102.

41–4

.98

3.82

± 0

.23

0.73

82.

72–5

.06

3.63

± 0

.28

0.78

182.

41–5

.06

3.74

± 0

.17

0.74

HL

1010

.15–

22.1

517

.76

± 1.

003.

178

11.2

5–21

.82

17.1

5 ±

1.41

3.98

1810

.15–

22.1

517

.49

± 0.

813.

45H

W10

4.95

–10.

568.

61 ±

0.5

71.

808

5.31

–10.

067.

70 ±

0.7

32.

0618

4.95

–10.

568.

21 ±

0.4

51.

92BL

1020

0.20

–710

.00

557.

47 ±

44.

1713

9.68

828

0.00

–690

.00

532.

81 ±

58.

9316

6.67

1820

0.20

–710

.00

546.

51 ±

34.

9014

8.08

TL10

50.3

0–16

0–80

126.

27 ±

10.

0331

.70

870

.95–

160.

0011

6.97

± 1

1.33

32.0

518

50.3

0–16

0.80

122.

14 ±

7.3

731

.27

RW/R

H10

1.34

–2.0

21.

65 ±

0.0

80.

268

1.34

–1.7

41.

55 ±

0.0

50.

1318

1.34

–2.0

21.

60 ±

0.0

50.

21FW

/FL

100.

57–0

.72

0.63

± 0

.02

0.06

80.

65–0

.72

0.68

± 0

.01

0.03

180.

57–0

.72

0.65

± 0

.01

0.05

HW

/HL

100.

40–0

.56

0.49

–0.0

20.

068

0.35

–0.5

20.

45 ±

0.0

20.

0518

0.35

–0.5

60.

47 ±

0.0

10.

06TL

/BL

100.

20–0

.29

0.23

± 0

.01

0.03

80.

14–0

.29

0.23

± 0

.02

0.04

180.

14–0

.29

0.23

± 0

.01

0.04


376

Kar

amuk

L.

Cha

ract

ers

Fem

ales

Mal

esBo

th se

xes

nEx

t.M

± S

ESD

nEx

t.M

± S

ESD

nEx

t.M

± S

ESD

RH

62.

11–3

.06

2.76

± 0

.15

0.38

43.

10–3

.40

3.25

± 0

.08

0.15

102.

11–3

.40

2.96

± 0

.12

0.39

RW6

3.21

–4.7

63.

96 ±

0.2

30.

574

4.93

–6.0

65.

72 ±

0.2

60.

5310

3.21

–6.0

64.

66 ±

0.3

31.

05FL

64.

37–6

.75

5.56

± 0

.31

0.76

45.

94–7

.29

6.36

± 0

.31

0.63

104.

37–7

.29

5.88

± 0

.25

0.79

FW6

3.45

–3.9

63.

62 ±

0.0

80.

204

3.55

–4.2

63.

74 ±

0.1

70.

3510

3.45

–4.2

63.

67 ±

0.0

80.

26H

L6

12.8

4–19

.55

17.9

9 ±

1.08

2.65

416

.97–

21.2

319

.70

± 0.

941.

8710

12.8

4–21

.23

18.6

8 ±

0.76

2.42

HW

66.

14–1

0.25

9.24

± 0

.67

1.65

49.

72–1

1.17

10.4

4 ±

0.41

0.82

106.

14–1

1.17

9.72

± 0

.46

1.45

BL6

370.

1–64

0.1

553.

37 ±

40.

0298

.03

462

0.5–

630.

062

3.2

± 2.

284.

5510

370.

1–64

0.1

581.

30 ±

5.7

881

.52

TL6

90.5

0–14

0.20

120.

50 ±

8.4

920

.79

412

0.0–

130.

012

2.63

± 2

.46

4.92

1090

.5 –

140

.212

1.35

± 4

.99

15.7

9RW

/RH

61.

34–1

.56

1.43

± 0

.03

0.08

41.

47–1

.90

1.76

± 0

.10

0.21

101.

34–1

.90

1.57

± 0

.07

0.22

FW/F

L6

0.59

–0.8

30.

66 ±

0.0

40.

094

0.58

–0.6

00.

59 ±

0.0

00.

0110

0.58

–0.8

30.

63 ±

0.0

20.

08H

W/H

L6

0.48

–0.5

30.

51 ±

0.0

10.

024

0.48

–0.6

60.

54 ±

0.0

40.

0810

0.48

–0.6

60.

52 ±

0.0

20.

05TL

/BL

60.

19–0

.24

0.22

± 0

.01

0.02

40.

19–0

.21

0.20

± 0

.00

0.01

100.

19–0

.24

0.21

± 0

.01

0.02

Ulu

abat

L.

Cha

ract

ers

Fem

ales

Mal

esBo

th se

xes

nEx

t.M

± S

ESD

nEx

t.M

± S

ESD

nEx

t.M

± S

ESD

RH

71.

88–2

.87

2.32

± 0

.14

0.36

101.

34–3

.24

1.97

± 0

.17

0.53

171.

34–3

.24

2.11

± 0

.12

0.49

RW7

2.64

–4.5

93.

47 ±

0.2

50.

6510

2.31

–4.4

32.

95 ±

0.1

90.

5917

2.31

–4.5

93.

16 ±

0.1

60.

65FL

74.

34–7

.59

5.37

± 0

.43

1.15

104.

18–6

.06

4.82

± 0

.17

0.54

174.

18–7

.59

5.05

± 0

.21

0.86

FW7

2.68

–4.4

73.

41 ±

0.2

30.

6210

2.61

–3.6

82.

97 ±

0.0

90.

3017

2.61

–4.4

73.

15 ±

0.1

20.

49H

L7

12.9

9–20

.83

15.8

4 ±

1.07

2.83

1012

.63–

18.3

714

.13

± 0.

561.

7917

12.6

3–20

.83

14.8

3 ±

0.57

2.36

HW

76.

38–9

.92

7.57

± 0

.49

1.29

106.

12–8

.84

7.06

± 0

.30

0.93

176.

12–9

.92

7.27

± 0

.26

1.09

BL7

360–

730.

5049

1.70

± 5

0.70

134.

3510

330.

50–5

6040

2.32

± 2

0.64

65.2

817

330.

50–7

30.5

043

9.12

± 2

5,67

68.1

6TL

710

0.70

–170

.20

127.

51 ±

10.

3927

.50

1080

.70–

140.

2010

6.33

± 5

.56

17.5

817

8.70

–170

.20

115.

85 ±

5.8

123

.94

RW/R

H7

1.33

–1.9

51.

50 ±

0.0

80.

2210

1.26

–2.0

11.

53 ±

0.0

70.

2317

1.26

–2.0

11.

52 ±

0.0

50.

22FW

/FL

70.

58–0

.83

0.64

± 0

.04

0.09

100.

54–0

.73

0.62

± 0

.02

0.05

170.

54–0

.83

0.63

± 0

.02

0.07

HW

/HL

70.

46–0

.50

0.48

± 0

.01

0.01

100.

47–0

.53

0.50

± 0

.01

0.02

170.

46–0

.53

0.49

± 0

.00

0.02

TL/B

L7

0.10

–0.3

10.

22 ±

0.0

40.

1010

0.24

–0.3

20.

26 ±

0.0

10.

0217

0.10

–0.3

20.

25 ±

0.0

20.

07


377

the extent of geographic variation in subcaudals for dice snakes from Turkey with following mean values from the Black Sea coast (70 for males and ~59 for females), the Northeast of Turkey (70 for males and ~61 for fe-males), and southeastern Turkey (~73 for males, ~58 for females). Similarly, sexually dimorphic mean differenc-es for subcaudals were found in dice snakes from west-ern Europe (Lenz & Gruschwitz 1993, Mebert 1993, Zimmerman & Fachbach 1996), but also eastern Eu-rope (refs. in Mebert 1993, Gruschwitz et al. 1999). Finally, only further research will show, whether sexual-dimorphism of ventral and subcaudal scale counts in N. tessellata from western Turkey exhibits a variation com-parable to that in other areas of the country. The sig-nificance of sexual dimorphism in pholidotic characters is well documented in natricinae and is ubiquitous (e.g. Mebert 2010).

No specimens with 17 dorsally arranged scales at mid body (mid point between snout and vent) were encoun-tered in this study and the number of dorsal scale rows in all specimens was 19 rows. Mebert (1993) investigat-ed the scale row reduction pattern in N. tessellata across a wide area. However, he did not take the snake’s body length (SVL) as a reference, but the number of ventrals instead, counting from the head caudad. Yet, the bilat-eral reduction of scale rows from 19 rows to 17 rows in Swiss and Italian dice snakes still occurred posterior the mid point of the ventral scale number (posterior ~52% -56% of the number of ventrals). That means, convert-ing to the traditional mid point measurement using the entire SVL (with the ~3% head length added), the dorsal scale row reduction from 19 to 17 rows in western Eu-ropean dice snakes would occur posterior 55% to 58% body length, respectively 5% to 8% posterior mid body. Only a few (5%) dice snakes from western Europe ex-hibited a scale row reduction to 17 scale a long stretch before the mid point of the body, thus, resulting in a tra-ditionally applied mid body scale count of 17 rows (Me-bert 1993). Compared to western European dice snakes, the scale row reduction to 17 rows in Greek individuals occurs even ~10% and ~7% farther caudad than in indi-viduals from Northeast Turkey (Mebert 1993), hence, it is not surprising that dice snakes from western Tur-key yield 19 rather than 17 scale rows at mid body (this study).

Measurement and definitions of body proportions and associated ratio values of investigated populations are presented in Table 4. To identify sexual dimorphism of body proportions, an independent t-test was per-formed on raw data for each population separately with no differences found between the genders. This too is in contrast to results of explicit sexual dimorphic body proportions found in dice snakes from Switzerland and Italy (for ratios for the tail length, head width and length, and frontal shield, see Mebert 1993, 1996). Sex-ualdimorphic tail length were also found in Germany (Lenz & Gruschwitz 1993), Austria (Zimmermann & Fachbach 1996), as well as western Balkan and Greece (Mebert 1993). A further investigation on sex alloca-

tion could possibly clarify the inconsistent pattern de-scribed here.

Across all populations averaged, the head ratios (head width/head length) for dice snakes from western Turkey is 0.50, which is higher than the average of 0.43 for measurements taken from all over Turkey (Baran 1976), resulting in relatively wider head for animals in this study. Comparing maximum lengths of body pro-portions between the populations, the longest absolute rostral height and width in females were measured in the Akşehir population, the largest frontal length in the Uluabat population, but the largest frontal width, head length, head width, body length and tail length in the Beyşehir population; in males however, the largest ros-tral height was measured in the Akşehir population, whereas the longest frontal width, frontal length and head width were measured in the Karamuk population, and the longest frontal width, head length, body length and tail length were found in the Beyşehir population. Concerning relative values to compensate for different size classes, the heighest rostral ratio (widest relative rostral width) of 1.34 and tail ratio of 0.15 (relative lon-gest tail) was measured on a specimen from the Akşehir population, the heighest frontal ratio of 0.59 (relative widest frontal shield) was found in the Karamuk popu-lation, and the heighest head ratio of 0.42 (relative wid-est head) in the Beyşehir population. The Tukey dis-persion test revealed a significant difference concerning head ratios (HW/HL) (p < 0.05) between populations from Beyşehir and Karamuk.

Color-Pattern Analysis

Two different color-pattern types were identified among the investigated populations. Color-pattern type fre-quencies distributed among the populations are shown in Table 5. Unicolored specimens (Type B) were par-ticularly common in the Beyşehir population (n = 21, 58.34%) and in the Uluabat population (n = 8, 44.44%), as such local concentrations of this color form were not found in the samples evaluated by Baran (1976) from different locations of Turkey. However, the occurrence of distinct local frequencies of unicolored and also mel-anistic dice snakes are known from sites in southern Switzerland to China and, as far is known, do not fol-low a certain geographic pattern (Mebert 1993). How-ever, a higher frequency of melanistic specimens has been noted locally from various populations (see refs.

LOCALITIES A Type B/C Type21 (%58.34)008 (%44.44)

Beyşehir Lake 15 (%41.66)Akşehir–Eber Lake 29 (%100)Karamuk Lake 10 (%100)Uluabat Lake 10 (%55.56)

Tab. 5. Color-pattern types and ratios of Natrix tessellata from the inspected populations in western Turkey.


378

Fig. 2. Color Pattern of Natrix tessellata from western Turkey: Dorsal and ventral view of spotted Type A with (a) from Kara-muk Çay, Afyon, and (b) from, Gölkaşı village, Isparta, at the border with Afyon; (c) dorsal and ventral view of Type B from Beyşehir Lake, Isparta; (d) melanistic specimen from Beyşehir Lake, Type C (see Text for Type description).


a

a

b

b

c

c

d

379

in Gruschwitz et al. 1999, Litvinov et al. 2011, Liu et al. 2011, Tuniyev et al. 2011). It was even used to sup-port the former subspecific status of Natrix tessellata heinrothi (Hecht 1930), but this character was refuted due to similar occurrence of melanistic dice snakes in other populations (e.g. Mertens 1969, Gruschwitz et al. 1999).

Type A: These are dice snakes with typically black spots dorsally and laterally over an olive green to gray brown background on the neck and dorsum (Figs. 2a, b). While black spots usually form four rows, some specimens yield also whitish spots to vertical lines between the black spots along frontal and lateral sides of the body. In some individuals black spots on the dorsum begin as four rows, fuse to three rows and split into four rows farther caudad or vice versa. The venter is dirty white or yellowish with black spots on the anterior part of the body, which increasingly expand caudad until they form the principal background color. There may be yellow-ish-white scattered spots over this background.

Type B: This is a unicolored, spotless morph (Fig. 2c). The dorsum is gray to olive green. There may be a black stripe bilaterally over the back of the head, which ex-pandes from the neck and fades caudad but sometimes becomes prominent again posteriorly. The venter is pinkish to white in the front with a black stripe that in-creasingly widens posteriorly up onto the tail, equiva-lent to Type A.

Type C: These are melanistic dice snakes or abundistic specimens (generally darkening skin, albeit not black) as can be seen in Fig. 2d.

Electrophoretic Analysis of Blood-Serum Proteins

Sexually mature specimens were used for the electro-phoretic analysis of blood-serum proteins. Since there were no qualitative differences between genders, males and females were evaluated together.

The electrophoretic figures of blood-serum pro-teins were similar among Akşehir-Eber, Karamuk and Lake Uluabat populations, and they were subsequently lumped together and compared with dice snakes from the Beyşehir population. Gel photographs directly com-paring the electrophoretic separations of blood-serum proteins between a dice snake from Beyşehir Lake and one from the Uluabat population, representing the group with specimens from the Akşehir-Eber, Karamuk and Uluabat lakes, are shown in Figure 3. In addition, a gel photograph of blood-serum proteins with densitom-etry curves is shown for an individual from the Beyşehir population (Fig. 4) and another one from the Uluabat population (Fig. 5). As seen in Figure 3, dice snakes from the Beyşehir population produced rates of fractions in the albumin region that migrated faster than those from snakes from the Uluabat population (and thus equally

for the remaining populations). Qualitatively, there are 12 fractions in the blood-serum protein samples in the specimen from Beyşehir and Uluabat, 2 in the albumin region and 10 in the globulin region. Small differences are visible between the corresponding fractions in the globulin region (Figs. 4 and 5). Quantitatively, in the Beyşehir specimen the density of the albumin fraction

Fig. 3. Blood-serum protein electropherograms of representa-tive specimens from two different populations of Natrix tessel-lata. A: Uluabat, B: Beyşehir. The albumins are the bands on the left end, and the globulins are those adjacent to the left.

Fig. 4. Gel photograph and densitometric tracing curve showing the electrophoretic separation of the blood-serum proteins obtained from a Natrix tessellata of Lake Beyşehir, Turkey. OD: Optical density, S: Start (junction between the stacking and separation of gels).

Fig. 5. Gel photograph and densitometric tracing curve show-ing the electrophoretic separation of the blood-serum pro-teins obtained from a Natrix tessellata of Lake Uluabat, Turkey OD: Optical density, S: Start (junction between the stacking and separation of gels).


380

is 24.62% and the albumin/globulin (A/G) ratio is 0.327. In the specimen from the Uluabat population, these val-ues are 18.31% and 0.224 respectively. Hence, the albu-min fractions and A/G ratio in the Beyşehir population are higher than in the Uluabat population.

Many researchers dealing with electrophoretic sepa-rations of blood-serum proteins of different amphibian and reptile species declared the taxonomic importance of number, speed and density of protein fractions (Des-sauer & Fox 1956, Chen 1967, Ferguson 1980, Arikan et al. 1999). Ferguson (1980) suggested that factors such as genetic variation, age, physiological and environmen-tal conditions affect protein structure. He suggested that among these factors, while some genetic variations may cause qualitative differences, others cause quantitative differences.

In this study, electrophoretic analysis of blood-serum proteins showed 1) faster movement of fractions with-in the albumin region in dice snakes from the Beyşehir population, 2) their higher percentage of albumin frac-tions, and 3) some small differences at the level of cor-responding fractions especially in the globulin region, which serves to differentiate this population from the other studied populations. However, it is not clear to which biological functions these differences are asso-ciated, or whether the differences may just show geo-graphic variation by chance without any pertinent bio-logical relevance, but yet be a part of a co-adapted gene complex.

Natrix tessellata could not be found at Lake Eğirdir despite various field trips. The reason for this might be the introduction of the pikeperch, Sander (Stizostedion) lucioperca, into the lake, beginning in 1955 and reaching a peak in the 1970s (Campbell 1992, Türkiye Çevre Vakfi 1993, İzci & Kuşat 2006, Kesici & Kesici 2006, Bâlik et al. 2007). After the vaccination of the pike-perch, which was ignorantly introduced into the habi-tat of N. tessellata, a rapid change occurred in the fau-na of Eğirdir Lake (Çetinkaya 2006) which resulted in the extinction of the 8 endemic fish species (Campbell 1992, Küçük & İkiz 2004). The new fish species, known to be an invasive predator, became in a short period the dominant species and caused significant changes in the general fishing regime of the lake (Çetinkaya 2006). This change in the general fauna presumably has affect-ed the feeding habits of N. tessellata, either by direct pre-dation on young dice snakes or by competitively con-suming on the prey of dice snakes. However, a newer literature record shows that the dice snakes still survived at Eğirdir Lake and also nearby Kovada Lake (Franzen et al. 2008, M. Franzen pers. comm.).

In summary, we found that the Beyşehir population was different from the other inspected populations re-garding a few properties of pholidosis (number of pre-ocular and supralabial scales), head ratios, color-pattern and electrophoretic pattern of blood-serum proteins. However, it is surprising that dice snakes from the pop-ulation of Beyşehir Lake is distinct from regionally close (approx. 70 km) populations of the lakes Akşehir-Eber,

Karamuk, and possibly Eğirdir, which resemble more the far distant (approx. 270 km) dice snakes from Ul-uabat Lake. Only future research including a larger and wider sampling scheme, a closer look at the landscape situation including topography and water sheds, and a more detailed morphological and molecular analysis may resolve these questions.

References

Arikan, H., Atatür, M.K., Çevik, I.E. & Y. Kumlutaş (1999): A serological investigation of Lacerta viridis (Laurenti, 1768) (Sauria: Lacertidae) populations in Turkey. – Turkish Journal of Zoology 23: 227–230.

Bâlik, İ., Çubuk, H. & R. Özkök (2007): Spatial distributions of economic fish populations in Lake Eğirdir. – Journal of Fisher-ies Science.com 1(2): 88–96.

Baran, I. (1976): Türkiye Yılanlarının Taksonomik Revizyonu ve Coğrafi Dağılışları. – TBTAK Yayınlar, Turkey.

Baran, I & M.K. Atatür (1988): Türkiye Herpetofaunası (Kurbağa ve Sürüngenler). – T.C. Çevre Bakanlığı, Turkey.

Başoğlu, M. & I. Baran (1980): Türkiye Sürüngenleri, Kısım II Yılanlar. – Ege Üniversitesi Yayınları.

Bedriaga, J. (1879): Verzeichnis der Reptilien und Amphibien Vorder-Asiens. – Bulletin Soc. Nat. Moscow 74(3): 453–568.

Bodenheimer, F.S. (1944): Introduction into the knowledge of the Amphibia and Reptilia of Turkey. – Rev. Faculty Science, University of Istanbul Series, Turkey.

Boettger, O. (1888): Verzeichnis der von Hrn. E. von Oertzen aus Griechenland und aus Kleinasien mitgebrachten Batra-chier und Reptilen. – Sitzungsberichte der Königlich Preussi-schen Akademie der Wissenschaften zu Berlin 5: 139–186.

Boettger, O. (1890): Batrachier und Reptilen aus Kleinasien. – Bericht der Senckenbergischen Naturforschenden Gesell-schaft in Frankfurt am Main: 293–295.

Campbell, R.N.B. (1992): Food of an introduced population of pike-perch, Stizostedion lucioperca L., in Lake Eğirdir, Turkey. – Aquaculture and Fisheries Management 23: 71–85.

Çetinkaya, O. (2006): Türkiye sularına aşılanan veya stoklanan egzotik ve yerli balık türleri, bunların yetiştiricilik, balıkçılık, doğal populasyonlar ve sucul ekosistemler üzerindeki etkileri: Veri tabanı için bir ön çalışma. – I. Balıklandırma Ve Rezervu-ar Yonetimi Sempozyumu, Antalya, Turkey: 7–9.

Chen, P.S. (1967): Separation of serum proteins in different am-phibian species by polyacrylamide gel electrophoresis. – Expe-rientia 23: 483–485.

Davis, B.J. (1964): Disc electrophoresis-II. Method and applica-tion to human serum proteins. – Ann. N. Y. Acad. Sci. 121: 404–427.

Dessauer, H.C. & W. Fox (1956): Characteristic electrophoret-ic patterns of orders of amphibia and reptilia. – Science 124: 225–226.

Dürigen, B. (1897): Deutschlands Amphibien und Reptilien. – Madgeburg, Germany.

Ferguson, A. (1980): Biochemical Systematics and Evolution. – Blackie and Son, Glasgow and London.

Franzen, M., Bussmann, M., Kordges, T. & B. Thiesmeier (1980): Die Amphibien und Reptilien der Südwest-Türkei. – Laurenti Verlag, Bielefeld, Germany.

Fuhn, I.E. & S. Vancea (1961): Fauna Republici Romine. – Fauna Romine Bucurest, Romania 14(2).


381

Göçmen, B. & W. Böhme (2002): New evidence of the occurence of the dice snake, Natrix tessellata (Laurenti, 1768) on Cyprus. – Zoology in the Midle East 27: 29–34.

Gruschwitz, M., Lenz, S., Mebert, K. & V. Lanka (1999): Na-trix tessellata (Laurenti, 1768) – Würfelnatter. – In: Böhme, W. (Ed.): Handbuch der Reptilien und Amphibien Europas, Vol. 3/Schlangen II. – AULA Verlag,Wiesbaden, Germany: 581–644.

Guicking, D., Joger, U. & M. Wink (2009): Cryptic diversity in a Eurasian water snake (Natrix tessellata): Evidence from mi-tochondrial sequence data and nuclear ISSR-PCR fingerprint-ing. – Organisms, Diversity and Evolution 9(3): 201–214.

Guicking, D. & U. Joger (2011): A range-wide molecular phylo-geography of Natrix tessellata. – Mertensiella 18: 1–10.

Hecht, G. (1930): Systematik, Ausbreitungsgeschichte und Öko-logie der europaeischen Arten der Gattung Tropidonotus (Kuhl). H. Boie. – Mitt. Zool. Mus. Berlin 16: 244–393.

İzci, L.& M. Kuşat (2006): Some population parameters of pi-keperch (Sander lucioperca (L., 1758)) in Lake Eğirdir. – SDU, Fen Bilim. Enst. Derg. 10–2: 167–172.

Kesici, E. & C. Kesici (2006): The effects of interferences in the natural structure of Lake Egirdir (Isparta) to the ecological disposition of the Lake. EU. – Journal of Fisheres & Aquatic Sciences 23(1/1): 99–103.

Kramer, E. & H. Schnurrenberger (1963): Systematik, Ver-breitung und Ökologie der Lybischen Schlangen. – Revue Suisse Zool. Genf. 70: 453–568.

Küçük, F. & R. İkiz (2004): Antalya Körfezi’ne dökülen akarsuların balık faunası. EU. – Journal of Fisheres & Aquatic Sciences 21(3/4): 287–294.

Lanka, V. (1978): Variabilitat und Biologie der Würfelnatter (Na-trix tessellata). – Acta Universitatis Carolinae Biologica 1975–1976: 167–207.

Lenz, S. & M. Gruschwitz (1993): Zur Merkmalsdifferenzierung und –variation der Würfelnatter, Natrix tessellata (Laurenti 1768) in Deutschland. – Mertensiella 3: 269–300.

Litvinov, N., Bakiev, A. & K. Mebert (2011): Thermobiology and microclimatic of the dice snake at its northern range limit in Russia. – Mertensiella 18: 330–336.

Liu, Y., Mebert, K. & L. Shi (2011): Notes on Distribution and Morphology of the dice Snake (Natrix tessellata) in China. – Mertensiella 18: 430–436.

Maclean, G.S., Lee, A.K. & K. J. Wilson (1973): A simple meth-od of obtaining blood from lizards. – Copeia 2: 338–339.

Mebert, K. (1993): Untersuchung zur Morphologie und Taxono-mie der Würfelnatter Natrix tessellata (Laurenti 1768) in der Schweiz und im südlichen Alpenraum. – M.S. thesis, Zoolo-gical Museum, University of Zürich, Switzerland.

Mebert, K. (1996): Comparaison morphologique entre des po-pulations introduites et indigenes de Natrix tessellata de I’Arc Alpin. – Bull. Soc. Herp. France 80: 15–25.

Mebert, K. (2010): Massive Hybridization and Species Concepts, Insights from Watersnakes. – VDM Verlag, Saarbrücken, Ger-many.

Mebert, K. (2011): Geographic variation of morphological chara-cters in the dice snake Natrix tessellata (Laurenti 1768). – Mer-tensiella 18: 11–19.

Mertens, R. (1969): Zur Synonymie und Variabilitat der Würfel-natter (Natrix tessellata). – Senckenbergiana Biologica Band 50(3/4): 125–131.

Mertens, R. & H. Wermuth (1960): Die Amphibien und Repti-lien Europas (Dritte Liste nach dem Stand vom 1. Januar 1960). – Verlag Waldemar Kramer, Frankfurt am Main, Germany.

Özeti, N. & M.K. Atatür (1979): A preliminary survey of the se-rum-proteins of a population of Mertensiella luschani finiken-sis Başoğlu & Atatür from Finike in Southwestern Anatolia. – İstanbul Üniversitesi Fen Fakültesi Mecmuası 44(B): 23–29.

Pallas, P.S. (1771): Reise durch verschiedene Provinzen des Rus-sischen Reiches I. – Peterburg, Russia.

Schreiber, E. (1912): Herpetologia europaea (2. Auflage). – Fi-scher, Jena, Germany.

Sindaco, R., Venchi, A., Carpaneto, G.M. & M. Bologno (2000): The reptiles of Anatolia: a checklist and zoogeographi-cal analysis. – Biogeographia 21: 441–554.

Strauch, A. (1873): Die Schlangen des Russischen Reiches. – Memories de’ Academie Imperiale des Sciences de St.-Peters-bourg, VII serie, Tome XXI (4).

Tuniyev, B., Tuniyev, S., Kirschey, T. & K. Mebert (2011): Notes on the dice snake, Natrix tessellata, from the Caucasian Isth-mus. – Mertensiella 18: 343–356.

Türkiye Çevre Vakfi (1993): Türkiye’nin Sulak Alanları. – TÇV Yayınları, Önder Matbaa.

Venzmer, G. (1919): Zur Schlangenfauna Süd-Kleinasiens, speziell des cilicischen Tauris. – Archiv für Naturgeschichte 83(A)(II): 95–122.

Werner, F. (1902): Die Reptilien-und Amphibienfauna von Klei-nasien. – SB. Akad. Wiss. Wien, Math.-Naturw. KI. I, III: 1057–1121.

Werner, F. (1903): Über Reptilien und Batrachier aus Westasien (Anatolien und Persien). – Zool. Jb. Syst. 19: 329–346.

Werner, F. (1919): Reptilien und Amphibien aus dem Amanus-Gebirge. – Archiv für Naturgeschichte 85(A)(8): 130–141.

Zimmermann P. & G. Fachbach (1996): Verbreitung und Bi-ologie der Würfelnatter, Natrix tessellata tessellata (Laurenti, 1768), in der Steiermark (Österreich). – Herpetozoa 8(3/4): 99–124.


382

Appendix

Specimens (n = 93): The data are given as follows: collec-tions code and number, number and sex (m./f.) of spec-imens, locality, date of collection and name of collec-tor: ZDEU.65/1968. 1–4 m., 5–6 f., Uluabat Lake, Bursa, 12.05.1968, leg. Z. Eren, ZDEU. 55/1976. 1–2 m., Beyşehir Lake, Konya, 23.04.1976, leg. M. Başoğlu, S. Sezer, ZDEU. 18/1987. 1–1 m., 2–10 juv., Akşehir Lake,Afyon, 07.06.1987, leg. F. Atagün, ZDEU. 48/1988. 1–2 m., 3–3 f., 4–6 juv., Beyşehir Lake, Konya, 06.06.1988, leg. F. Atagün, ZDEU. 19/2003. 1–3 m., 4–7 f., Eber Lake, Afyon, 02.07.2003, leg. Y.E. Dinçaslan, D. Ayaz, ZDEU.

Authors Yunus Emre Dinçaslan, Environmental Protection Agency for Special Areas, 35680 Eskifoça/İzmir, Turkey, e-mail: [email protected]; Hüseyin Arikan, Ege University, Science Faculty, Department of Biology, Bornova, İzmir, Turkey; İsmail Hakki Uğurtaş, Uludağ University, Science and Art Faculty, Department of Biology, Nilüfer, Bursa, Turkey; Konrad Mebert, Siebeneichenstrasse 31, 5634 Merenschwand, Switzerland.

21/2003. 1–2 m., 3–4 f., Karamuk Lake, Çay, Afyon, 30.06.2003, leg. Y. E. Dinçaslan, ZDEU. 23/2003. 1–4 m., 5–10 f., 11–12 juv., Akşehir Lake, Afyon, 03.07.2003, leg. Y. E. Dinçaslan, D. Ayaz, ZDEU. 26/2003. 1–6 m., 7–8 f., Beyşehir Lake, Konya, 04.07.2003, leg. Y. E. Dinçaslan, D. Ayaz, ZDEU. 27/2003. 1–2 f., Karamuk Lake, Afyon, 02.07.2003, leg, Y. E. Dinçaslan, D. Ayaz, ZDEU. 24/2004. 1–2 m., 3–4 f., Karamuk Lake, Afyon, 06.08.2004, leg. Y. E. Dinçaslan, ZDEU. 264/2005. 1–8 m., 9–20 f., Beyşehir Lake, Konya, 19.05.2005, leg. Y. E. Dinçaslan, ZDEU. 265/2005. 1–6 m., 7–11 f., 12–12 juv., Uluabat Lake, Bursa, 09.07.2005, leg. İ. H. Uğurtaş.


Morphology and blood proteins of Dice snakes from western Turkey.

Documents