Wednesday, May 29, 2019

[Herpetology • 2019] Elaphe urartica • The Biogeography of Elaphe sauromates (Pallas, 1814), with A Description of A New Rat Snake Species

Elaphe urartica Jablonski, Kukushkin, Avcı, Bunyatova, Ilgaz, Tuniyev et Jandzik

Jablonski​, Kukushkin, Avcı, Bunyatova, Kumlutaş, et al., 2019. 

The rat snake genus Elaphe once comprised several dozens of species distributed in temperate through tropical zones of the New and Old World. Based on molecular-genetic analyses in early 2000s, the genus was split into several separate genera, leaving only 15 Palearctic and Oriental species as its members. One of the three species also occurring in Europe is Elaphe sauromates, a robust snake from the Balkans, Anatolia, Caucasus, Ponto-Caspian steppes, and Levant that has been suspected to be composed of two or more genetically diverse populations. Here, we studied the genetic structure and morphological variation of E. sauromates, aiming to better understand its inter-population relationships and biogeography, and subsequently revise its taxonomy.

We reconstructed the phylogeography and analyzed the genetic structure of E. sauromates populations originating from most of its geographic range using both mitochondrial (COI, ND4) and nuclear (C-MOS, MC1R, PRLR, RAG1) DNA gene fragments. We employed Maximum likelihood and Bayesian inference methods for the phylogenetic tree reconstructions, supplemented with species delimitation methods, analysis of haplotype networks, and calculation of uncorrected p-distances. Morphological variation in 15 metric and 18 meristic characters was studied using parametric univariate tests as well as multivariate general linearized models. In total, we analyzed sequences originating from 63 specimens and morphological data from 95 specimens of E. sauromates sensu lato.

The molecular phylogeny identified two clearly divergent sister lineages within E. sauromates, with both forming a lineage sister to E. quatuorlineata. The genetic distance between them (5.80–8.24% in mtDNA) is similar to the distances among several other species of the genus Elaphe. Both lineages are also moderately morphologically differentiated and, while none of the characters are exclusively diagnostic, their combination can be used for confident lineage identification. Here, following the criteria of genetic and evolutionary species concepts, we describe the lineage from eastern Anatolia and parts of the Lesser and Great Caucasus as a new species Elaphe urartica sp. nov.

Elaphe urartica sp. nov. represents a cryptic species whose ancestors presumably diverged from their common ancestor with E. sauromates around the Miocene-Pliocene boundary. The intraspecific genetic structure indicates that the recent diversity of both species has been predominantly shaped by Pleistocene climatic oscillations, with glacial refugia mainly located in the Balkans, Crimea, and/or Anatolia in E. sauromates and Anatolia and/or the Caucasus in E. urartica sp. nov.

Figure 4: Holotype (ZDEU 26/2012) of Elaphe urartica sp. nov. from eastern Turkey. (A) Dorsal view, (B) ventral view, (C) dorsal view of the head, (D) lateral view, (E) ventral view (photos by Aziz Avcı), (F) the holotype while alive (photo by Çetin Ilgaz), (G) Sako B. Tuniyev with freshly caught holotype of E. urartica sp. nov. (photo by Boris Tuniyev).

Figure 6: Paratypes of Elaphe urartica sp. nov. from Armenia ((A and B) photo by Ilya Korshunov and Konstantin Shiryaev) and Azerbaijan ((C) photo by Sabina Bunyatova) showing the habitus and details of the head.

Family Colubridae

GenusElaphe Fitzinger in Wagler, 1833

Elaphe urartica Jablonski, Kukushkin, Avcı, Bunyatova, Ilgaz, Tuniyev et Jandzik sp. nov.

Diagnosis. A new species of western Palearctic genus Elaphe, very similar to E. sauromates (Pallas, 1814), characterized by the combination of the following characters: total length usually does not exceed 1,200 mm (796–1,205 mm), snout-vent (SVL) length usually less than 1,000 mm (650–970 mm), tail length less than 250 mm (146–245 mm) (see Tables 4 and 6). Tail forms about 25% of the SVL in males and about 21% in females. Head relatively large, distinguished from the body. Snout in prefrontal and internasal area is conspicuously convex which usually forms a hook-nosed head profile. Pileus length on average 1.8–1.9 times larger than its width. Frontal plate 1.2–1.3 times longer than wide. Anterior inframaxillar scute relatively large and wide, 1.2–1.3 times longer than the narrow posterior inframaxillar scute. One or two preocular scales, one loreal, two postoculars, two temporals, three or four posttemporals, eight labials, 10–11 sublabials on each side of the head. Eye in contact with fourth and fifth labials (Table 5; Table S3). Variation in head scale counts is relatively low (see Table S3). Usually two gulars located the anterior inframaxillars. The total number of gulars between inframaxillars and first preventral scale exceeds 12. Number of ventrals is 154–211 (154–206 in males, 194–211 in females), 60–74 subcaudal pairs (65–74 in males, 60–72 in females). 23–25 longitudinal rows of scales are around the midbody, with well-developed keels on 18–21 rows of body scales. The background of dorsal surfaces of the body and lateral surfaces of the head are yellowish or whitish, or seldomly bright yellow. The pattern of the dorsal surface of the body is composed of 50–65 rounded brown or black large ellipsoid spots, which may have whitish edges. Spots can be extended transversely in the posterior part of the body. Pileus is dark, often almost black, slightly lighter on the tip of the snout. Upper preoculars and temporals are dark forming a postocular stripe extending toward the mouth corner. This stripe blends with the dark dorsolateral head coloration anterior to the eye. Pale spots on the labials, only barely visible or lacking on sublabials. Ventral side of the body is whitish to pale yellow, sometimes with pinkish tint. There are marbled patterns of numerous small irregular dark brown and light gray spots with reddish contours that are more pronounced on the lateral sides of ventral plates. Throat is light, with numerous reddish-orange or brownish speckles on the lower jaws and anterior ventral plates. Iris is dark brown or almost black with a thin light rim around the pupil.


Figure 5: Habitat at the type locality (Kısıklı, Süphan Mts., Turkey) of Elaphe urartica sp. nov. in south-eastern Turkey (photo by Boris Tuniyev).

Figure 8: Color and pattern variation in Elaphe urartica sp. nov. (A–D) Kaputan, Armenia; (E) Didi Shiraki, Georgia; (F) Ersi, Dagestan, Russian Federation (photos by Boris Tuniyev).

Distribution and habitat.
The geographic range of E. urartica sp. nov. is bordered by the Armenian Plateau, south-eastern foothills of the Great Caucasus, Alazan Valley, Kur-Aras, Lenkoran Lowlands, and the area of Qobustan. The species is distributed in Turkey, Georgia, Armenia, Azerbaijan, Nagorno-Karabakh, Iran, and Russia. In Turkey, it can be found east of the Anatolian Diagonal with reliable records from Kars, Bitlis, Diyarbakır, and Van Provinces, presumably also in Erzurum, Iğdır, and Ağrı Provinces (Baran et al., 2012). In eastern Transcaucasia E. urartica sp. nov. is distributed from south-eastern Georgia to the Zalka Plateau or to Suramskyi Ridge in Southern Ossetia in the West, throughout most of the Armenian territory, Nagorno-Karabakh, and Azerbaijan with the exception of the Abşeron Peninsula. The eastern part of the range lies in northern Iran to the Golestan Province to the East, and Kermanshah and Semnan Provinces to the South (Alekperov & Loginov, 1953; Muskhelishvili, 1970; Flärdh, 1983; Schulz, 1996; Sindaco et al., 2000; Arakelyan et al., 2011; Bunyatova, Akhmedov & Dzhafarov, 2012; Bunyatova, 2013; Najafov, Hashimov & Isgenderov, 2013; Safaei-Mahroo et al., 2015). In the Russian Federation, E. urartica sp. nov. occurs in Samur-Devichi Lowlands of southern Dagestan and probably in the Dagestan Intermontane Region as well (Ananjeva et al., 2006; Mazanaeva & Askenderov, 2014). The species could also occur in the extreme northern regions of Iraq (Sindaco, Venchi & Grieco, 2013).

The snake occurs in a wide range of altitudes—from ca. 25 m below sea level in the Lenkoran foredeep to about 2,600 m a.s.l. in the Shirak Province in Armenia (Arakelyan et al., 2011). It is an eurytopic species inhabiting a wide variety of landscapes: mountain and lowland semi deserts, different types of the steppe, semi subtropical savannah-like forest-steppes with oreoxerophytes, sparse juniper forests, montane broad-leaved forests, and alpine meadows (Fig. 5). The climate within the E. urartica sp. nov. range varies from the subtropical in Lenkoran and piedmont area of eastern Transcaucasia to cold mountain climate in Armenia and north-eastern Anatolia. Humidity varies from highly arid (with annual precipitation of less than 200 mm) to moderately humid (1,400–1,600 mm per year; Clark & Clark, 1973; Arakelyan et al., 2011; Bunyatova, Akhmedov & Dzhafarov, 2012; Şensoy et al., 2016).

Elaphe urartica sp. nov. is sympatric with E. dione in Dagestan, central-eastern Azerbaijan, eastern Georgia, and presumably in north-eastern Turkey, southern Armenia, and northern Iran. All other species of the genus Elaphe have allopatric distribution relative to E. urartica sp. nov. Since the species occurs in a region of southern Russia (Dagestan), north of the Caucasus, that is geographically and politically considered a part of Europe (Sillero et al., 2014), E. urartica sp. nov. is considered another member of the European herpetofauna.

Etymology. The specific epithet is a feminine adjective derived from the name of the ancient kingdom of Urartu that flourished in the Armenian Highlands and around lake Van, an area of recent distribution of E. urartica sp. nov., in the 9th–6th century BCE (Asher & Asher, 2009). We are choosing this name out of respect for Peter Simon Pallas, who proposed the name for E. sauromates, now the sister species of E. urartica, which most likely refers to Sarmatians (Sauromatae; Σαυρομαται in Greek), a confederation of nomadic peoples inhabiting vast portions of the recent range of E. sauromates between the 5th century BCE and 4th century CE.

Proposal of common names. We propose the English name “Urartian Rat Snake” for E. urartica sp. nov. Along with the name “Blotched rat snake”, we also suggest using the name “Sarmatian Rat Snake” for E. sauromates, instead of the older “Eastern Four-lined Rat Snake” derived as a subspecific name from the common name of E. quatuorlineata. The newly proposed name would decrease confusion and also better reflects the scientific name of E. sauromates.

Daniel Jablonski​, Oleg V. Kukushkin, Aziz Avcı, Sabina Bunyatova, Yusuf Kumlutaş, Çetin Ilgaz, Ekaterina Polyakova, Konstantin Shiryaev, Boris Tuniyev and David Jandzik. 2019. The Biogeography of Elaphe sauromates (Pallas, 1814), with A Description of A New Rat Snake Species.   PeerJ. 7:e6944.  DOI: 10.7717/peerj.6944