A new subspecies, Lyciasalamandra atifi oezi n. ssp. (Urodela: Salamandridae) from Gazipaşa (Antalya, Turkey)

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1 ISSN (online) ISSN (print) The journal is available on line at Research Article A new subspecies, Lyciasalamandra atifi oezi n. ssp. (Urodela: Salamandridae) from Gazipaşa (Antalya, Turkey) CEMAL VAROL TOK 1*, MURAT AFSAR 2 & BATUHAN YAMAN YAKIN 1 1 Department of Biology, Faculty of Arts and Sciences, Çanakkale Onsekiz Mart University, 17100, Çanakkale, Turkey 2 Department of Biology, Faculty of Arts and Sciences, Celal Bayar University, Manisa, Turkey Corresponding Author: cvtok@comu.edu.tr Received: 23 September 2016 Accepted by V. Pešić: 15 November 2016 Published online: 17 November Abstract In this study, a new subspecies of the Lycian salamander, Lyciasalamandra atifi oezi n. ssp., was described from Gazipaşa (Antalya, Turkey). The Lyciasalamandra specimens collected in Doğanca (Gazipaşa, Antalya) are clearly distinguished from the known subspecies of L. atifi by the very small and few white flecks on the dorsal ground pattern or by the absence of the flecks in some specimens. The light coloration, which can be distinctly observed in front of, behind, and under the eye of L. atifi, is indistinct in the new subspecies, unlike the other subspecies. The body length was observed to be shorter than that of the nominate subspecies but close to that of L. a. bayrami. In juveniles, scattered black flecks are striking on the posterior parts of their parotoids and, unlike adults, denser small and white flecks are striking on top of the head as well as on the dorsum, the tail, and the extremities. In addition, scattered yellow flecks in different sizes and shapes are present on the dorsal tail. Key words: Salamandridae, new subspecies, Lyciasalamandra atifi oezi subsp. nov., taxonomy, Gazipaşa, Antalya, Turkey. Introduction It was previously known that eight subspecies [L. l. luschani (Steindachner, 1891), L. l. atifi (Başoğlu 1967), L. l. fazilae (Başoğlu & Atatür, 1974), L. l. finikensis (Başoğlu & Atatür, 1975), L. l. antalyana (Başoğlu & Baran, 1976), L. l. basoglui (Baran & Atatür, 1980), L. l. billae (Franzen & Klawen, 1980), and L. l. flavimembris (Mutz & Steinfartz, 1995)] of terrestrial salamanders (Mertensiella luschani) in genus Mertensiella inhabited Turkey (Baran & Üçüncü, 1994; Başoğlu et al., 1994; Öz et al., 2003). A molecular study by Weisrock et al. (2001) suggests that Turkish terrestrial salamanders in genus Mertensiella should be included in the genus Salamandra. In the same study, it was further pointed out that the forms flavimembris, fazilae, luschani, billae, antalyana and atifi, inhabiting southwestern Anatolia, could be considered at the species level (Salamandra flavimembris, S. fazilae, S. luschani, S. billae, S. antalyana, and S. atifi). Veith & Steinfartz (2004) state that a total of seven terrestrial salamander species with one polytypic and six monotypic inhabit south-western Anatolia and the islands in its close vicinity, providing the views of previous researchers (Weisrock et al., 2001) and their respective unpublished data. However, they included those species in genus Lyciasalamandra, which was introduced in the same study, instead of genus Salamandra. Therefore, terrestrial salamander species L. luschani Steindachner (1891), L. helverseni Ecol. Mont., 9, 2016, 38-45

2 TOK ET AL. Pieper (1963), L. atifi Başoğlu (1967), L. fazilae Başoğlu & Atatür (1974), L. finikensis Başoğlu & Atatür (1975), L. antalyana Başoğlu & Baran (1976), L. basoglui Baran & Atatür (1980), L. billae Franzen & Klawen (1980) and L. flavimembris Mutz & Steinfartz (1995) were announced to exist. Recognized as a subspecies of the Lycian salamander for years, Lyciasalamandra atifi was first described from Türbelinaz (Dereköy) in Alanya, eastern Antalya in 1967 by Başoğlu. Later on, the distributional range of the species was extended by new records from Fersin (Güçlüköy, Akseki), Çaltepe (Manavgat), Selge (Altınkaya, Manavgat), and Mount Cebireis (Alanya) in various studies (Başoğlu & Baran, 1976; Klewen et al., 1988; Gebhart, 1990; Baran & Üçüncü, 1994; Veith et al., 2001; Öz et al., 2004). Akman et al. (2011) and Göçmen et al. (2013) provided new data recorded between elevations of 232 and 1400 meters in five different localities around Mahmutlar Town in the southern section of the Dim Tributary and in three around Gazipaşa, respectively. Lyciasalamandra atifi has a relatively wider distributional range, which extends from Selge (Altınkaya, Manavgat) to Gazipaşa than the other sister species do. Within this relatively wider area, the examined specimens obtained in the Dim Cave in the east of the Dim Tributary were described as L. atifi bayrami by Yıldız & Akman (2015). The researchers stated that the form bayrami had a shorter body length than the nominate subspecies did, a relatively long rostrum, and dark grey coloration on the dorsal side and that the subspecies bayrami of different sexes exhibited pattern differences in comparison with the nominate subspecies. The present study aims to examine the Lyciasalamandra atifi specimens first recorded in the vicinity of the Doğanca Village, Gazipaşa (Antalya) by morphologically comparing them with the adult specimens collected in Türbelinaz (Dereköy) the type locality of the nominate subspecies as well as from the vicinity of nearby Taşatan and is intended to provide data on the taxonomical status of these specimens, which were first recorded from the Doğanca Village. Materials and Methods One male, four female and two juvenile specimens evaluated in the study were collected in the vicinity of the Doğanca Village in Gazipaşa (Antalya) within the scope of the project The Task of Inventory and Monitoring of the Biological Diversity of the Terrestrial and Inland Water Ecosystems in Antalya Province, which was funded by the 6 th Regional Directorate of the Ministry of Forestry and Water Affairs. Although one male specimen was evaluated in the study, the other two male specimens collected during the study died while they were being transferred to the laboratory from the field and were too impaired to be used for a morphological evaluation. Nevertheless, the color-pattern observation at the first moment of their capture resembled the holotype. Twenty-four specimens belonging to the three localities (Doğanca, Türbelinaz, and Taşatan) examined in the research were obtained during the fieldwork carried out in spring (March and April). Their color photographs were taken after their color-pattern characteristics had been determined. The new Lyciasalamandra atifi specimens collected in the Doğanca Village, Gazipaşa (Antalya) (1 male, 5 females, 2 juveniles; Leg. C.Varol TOK, Batuhan Y. YAKIN; Lat= , Long.= , 390 m a.s.l.) were compared with 16 (6 males, 4 females, 6 juveniles, Leg. C.Varol TOK, Batuhan Yaman YAKIN; Lat.= , Long.= ) additional specimens collected in Türbelinaz (Dereköy) the type locality of the nominate subspecies as well as from the vicinity of Taşatan nearby Türbelinaz. The collected specimens have been preserved in the Collection of the Molecular Zootaxonomy Laboratory of Çanakkale Onsekiz Mart University. The morphological measurements were performed considering the terminology provided by Peters (1964), Öz & Arıkan (1990), Mutz & Steinfartz (1995), Öz et al. (2004), and Çiçek et al. (2010) (Table 1). The researchers of this study carried out body measurements, namely total body length (TBL), head length (HL), snout-vent length 1 (SVL 1), snout-vent length 2 (SVL 2), tail length 1 (TL 1), tail length 2 (TL 2), the distance between the axillar and the inguinal (Ax-In), head width (HW), parotoid length (PL), parotoid width (PW), body length (BL), nostril-eye distance (NoED), the distance between nostrils (Ln), eye diameter (O), forelimb length (Pa), and hindlimb length (Pp). Furthermore, the ratios of HW/HL, TL/TBL, PW/PL and NoED/HL were measured on a caliper with a sensitivity of 0.01 mm. Ecol. Mont., 9, 2016,

3 NEW SUBSPECIES OF THE LYCIAN SALAMANDER FROM TURKEY Results Lyciasalamandra atifi oezi n. ssp. Holotype and type locality: One male, collected by C. Varol TOK and Batuhan Yaman YAKIN between the Hasdere and Doğanca Villages in Gazipaşa - Antalya, (Turkey) 390 m a.s.l. on March 5, 2016 (Figure 1A, B). Paratypes: Five females and two juveniles, collected by C.Varol TOK and Batuhan Yaman YAKIN between the Hasdere and Doğanca Villages in Gazipaşa - Antalya (Turkey) 390 m a.s.l. on March 6 and April 13, 2016 (Figure 1 C, D). Figure 1. A Dorsal aspects of the holotype; B Parotoids of holotype; C Dorsal aspects of the paratype female; D Dorsal aspects of the juvenile specimen from the Doğanca Village (Gazipaşa, Antalya). Diagnosis: This subspecies can be distinguished from the nominate subspecies and the subspecies bayrami by the following characteristics. The ground color of the dorsal side is dark brown unlike the subspecies bayrami but as in the nominate subspecies. However, unlike the nominate subspecies, much fewer irregularly scattered white flecks are distinguished on this ground color, whereas some specimens are almost fleckless (Figure 1 A). The white flecks, which are striking on the posterior edges of the parotid glands in the nominate subspecies, are on the dorsal side and much fewer and scattered in this new subspecies (Figure 1 B). The light coloration, distinctly visible in front of, behind, and under the eye in the other two subspecies, is indistinct in this subspecies. A row of white flecks found in the paravertebral area in the males of subspecies bayrami is absent in the males of this new form (Table 2). 40

4 TOK ET AL. Table 1. Morphometric measurements (in millimeters) and ratios of the Lyciasalamandra atifi oezi n. ssp. material from the Doğanca Village (Gazipaşa, Antalya) together with statistical data. HL: Head length, SVL1: Snout-vent length 1, SVL 2: Snout-vent length 2, TL 1: Tail length 1, TL 2: Tail length 2, Ax-In: the distance between the axillar and the inguinal, HW: Head width, PL: Parotoid length, PW: Parotoid width, BL: Body length, NoED: Distance between Nostril and Eye, Ln: Length between Nostrils, O: Eye length, Pa: Forelimb length, Pp: Hindlimb length, TBL: Total body length, HW/HL, TL/TBL, PW/PL, NoED/HL. Characters L. a. oezi n. ssp. male L. a. oezi n. ssp. Females L. a. oezi n. ssp. juv. N Mean N Mean SD SE Min Max. N Mean SD SE Min Max. HL SVL SVL TL TL Ax-In HW PL PW BL NoED Ln O Pa Pp TBL HW/HL TL/TBL PW/PL NoED/HL Description of holotype: Total body length (TBL) 144 mm, tail length mm, head flat, head length (HL) and head width (HW) and mm, respectively. Parotoids distinct, parotoid length (PL) 8.97 mm and parotoid width (PW) 2.41 mm. Hindlimb longer than forelimb, Pa mm, Pp mm. Nostril to eye distance (NoED) 3.79 mm, distance between nostrils (Ln) 5.47 mm, and the eye length (O) 4.62 mm. Ratios HW/HL, TL/TBL, PW/ PL and NoED/HL are 0.69, 0.47, 0.26, and 0.22, respectively (Table 1). The ground color of the dorsal side is dark brown, and very few scattered and irregular white flecks are striking as far as the tail on the posterior part of the head and on the dorsal side. The parotoids contain irregularly scattered black dots and a few white flecks. The black flecks continuing as far as the tip of the tail in the vertebral area are distinct. The upper parts of the extremities are brownish and partly flesh-colored. They contain few and sparse white flecks. The lateral sides of the body are off-white and easily distinguished from the dorsal side. The ventral side is flesh-colored, and white flecks can be seen towards the lateral sides. The projection on the base of the tail is visible to the naked eye (Figure 1 A, B) (Table 2). Description of paratype: The five female and two juvenile specimens collected from the vicinity of the Doğanca Village were determined as paratypes. In the females, the TBL 138 mm (range: ), HL and HW mm (range: ) and mm (range: ). Parotoids were distinct also in the females, PL 9.48 mm (range: ) and PW 2.59 mm (range: ). The NoED is 3.77 mm (range: ) and Ln is 5.06 mm (range: ) and O is 3.94 mm (range: ). Forelimb mm (range: ) and hindlimb mm (range: ). HW/HL, TL/TBL, PW/ PL and NoED/HL ratios were 0.75 (range: ), 0.47 (range: ), 0.20 (range: ), and 0.24 (range: ), respectively. Ecol. Mont., 9, 2016,

5 NEW SUBSPECIES OF THE LYCIAN SALAMANDER FROM TURKEY Table 2. Comparison of morphological features of the subspecies of L. atifi. Lyciasalamandra atifi atifi Lyciasalamandra atifi bayrami Lyciasalamandra atifi oezi n. ssp. Ground color of the dorsal side Irregularly scattered white flecks White flecks on the posterior edges of parotoids Light coloration in front of, behind and under the eye A row of white flecks in the paravertebral area Scattered yellow flecks on the tail Dark brown Dark grey, a few whitish flecks Dark brown A few A few Very few / fleckless White and yellow flecks White and yellow flecks Black dots, a few white flecks Present Present Imperceptible A few white flecks Present in males, a few white Absent flecks for females Present Present Only for juveniles The TBL is mm (range: 80-85), and HL and HW are mm (range: ) and 8.55 mm (range: ) for juveniles, respectively. PL is 6.55 mm (range: ) and PW is 1.86 mm (range: ). NoED is 2.72 mm (range: ) and Ln is 3.49 mm (range: ) and O is 3.09 mm (range: ). Forelimb mm (range: ) and hindlimb mm (range: ). HW/HL, TL/TBL, PW/ PL and NoED/HL ratios were 0.75 (range: ), 0.45 (range: ), 0.28 (range: ), and 0.24 (range: ), respectively (Table 1). Moreover, the coloration given for the holotype and the density of the irregularly scattered black dots and a few white flecks on the parotoids mostly resemble the females selected as the paratypes. The light coloration, distinctly observable in front of, behind, and under the eye in the other two subspecies, is indistinct. Moreover, whilst a relatively larger number of irregularly scattered white flecks are striking on the ground color of the dorsal side in some female specimens, the flecks concerned are absent in some. The black flecks continuing as far as the tip of the tail in the vertebral area are distinct in the females. The upper parts of the extremities are brownish and partly flesh-colored. They contain sparse white flecks. The lateral sides of the body are off-white and easily distinguishable on the dorsal side. The ventral side is flesh-colored, and white flecks can be seen towards the lateral sides (Figure 1 C) (Table 2). The ground color of the dorsum is dark brown, and, as in the adult specimens, scattered black flecks are striking on the posterior parts of the parotoids in the two juvenile specimens collected from the same region. However, unlike the adult specimens, denser small and white flecks are present on top of the head as well as on the dorsum, tail, and extremities. Additionally, scattered yellow flecks in different sizes and shapes are present on the tail (Figure 1 D) (Table 2). Habitat and Distribution: The specimens were collected from the open areas in the forest around the Doğanca Village, Gazipaşa (Figure 2). One, four and two juvenile specimens were obtained from beneath the karstic stones in the region during the first study ( ) carried out in these areas. In the other study, however, only one specimen was detected under a stone in an open forest area covered with needles of pine trees during the research performed in the same region. Derivatio nominis: The name of the newly described species here is derived from the surname of the Turkish herpetologist Prof. Dr. Mehmet Öz, who made valuable contributions to the Lycian salamander taxonomy. 42

6 TOK ET AL. Figure 2. Habitats of Lyciasalamandra atifi oezi n. ssp. from the Doğanca Village (Gazipaşa, Antalya). Discussion Lyciasalamandra atifi, endemic to southern Anatolia, was first described from Türbelinaz (Dereköy, Alanya, Antalya) in 1967 by Başoğlu and considered a monotypic species until recently. It has been recently stated that the species atifi is represented by more than one subspecies in its distributional range, and the population inhabiting the Dim Cave has been introduced as a new subspecies, L. a. bayrami. It has been discovered that the subspecies concerned has grayish dorsal coloration unlike the nominate subspecies (Yıldız & Akman, 2015). The specimens detected from the vicinity of the Doğanca Village (Gazipaşa, Antalya) in the present study are immediately distinguished from the subspecies bayrami by their dark brown dorsal ground color. Even though the ground color of the dorsal side was stated to be dark brown in the specimens from Türbelinaz (terra typica of the nominate subspecies) in the original definition made by Başoğlu (1967), it was reported that dense, thin and white flecks were visible in this ground color. The color-pattern status indicated for the nominate subspecies by Başoğlu (1967) was also found similar in the adult specimens of the nominate subspecies examined from Türbelinaz and Taşatan by us, and irregularly scattered thin and white flecks were detected on the dorsal ground color. Nevertheless, unlike the nominate subspecies and the subspecies bayrami, the white flecks are either very rarely encountered on the dark brown ground color on the dorsal side in the adult specimens we detected around the Doğanca Village or hardly visible as in some specimens. However, it was established that the white flecks concerned formed two longitudinal bands in the males of the subspecies bayrami, and this type of pattern was not encountered in the male specimens we detected from the vicinity of the Doğanca Village in the present study. In the study by Yıldız & Akman (2015), it was reported that the mean body length value of the adults of the subspecies bayrami [136 mm (range: mm)] was lower than that of the nominate subspecies [158 mm ( ) by Başoğlu (1967); mm (range: ) by Öz et al. (2004); 161 mm (range: ) by Baran & Üçüncü (1994); and 153 mm (range: ) by Yıldız & Akman (2015)]. The mean total length value in the adult specimens of the new subspecies we detected from the vicinity of the Doğanca Village was calculated to be 139 mm (range: ), and it was observed that this value was lower than the mean values given for the nominate subspecies in the literature but close to the value for the subspecies bayrami. Until recently, the distributional range of L. atifi, described from the Türbelinaz Village (Alanya, Antalya), has been known to cover a narrow zone (Baran & Üçüncü, 1994; Öz et al., 2004). Nevertheless, the distributional range of the species was relatively extended with the studies carried out in the following years (Akman et al., 2011; Göçmen et al., 2013; Yıldız & Akman, 2015). However, L. atifi is included in the EN category of the IUCN Red List, and it is stated that its population tend to decrease due to the degradation of their habitats (Cox et al., 2006). By determining, in the present study, that the specimens detected from the vicinity of the Doğanca Village (Gazipaşa, Antalya) a new locality showed morphological and morphometric differences from the other two subspecies acknowledged to inhabit the distributional range of L. atifi, it was revealed that a new subspecies inhabited the region and this new population was named L. atifi oezi n. ssp. As also emphasized before, there is a need for studies on the distributions, ecologies, and Ecol. Mont., 9, 2016,

7 NEW SUBSPECIES OF THE LYCIAN SALAMANDER FROM TURKEY taxonomies of taxa Lyciasalamandra in southern Anatolia. A taxonomical evaluation should be made by examining an adequate number of specimens from the other populations of L. atifi that inhabit its distributional range. Acknowledgements The specimens and data obtained in this study were reached within the scope of a project entitled The Task of Inventory and Monitoring of the Biological Diversity of the Terrestrial and Inland Water Ecosystems in Antalya Province, funded by the Directorate of Antalya Branch of the 6 th Regional Directorate of the Department of Nature Protection and National Parks of the Republic of Turkey, Ministry of Forestry and Water Affairs. We would like to thank the establishment concerned and Turunç Peyzaj Anonim Şirketi for the support to the study. References Akman, B., Göçmen, B., Yalçınkaya, D. & Karış, M. (2011) Range extension of Lyciasalamandra atifi (Başoğlu, 1967) (Amphibia: Urodela: Salamandridae). North-Western Journal of Zoology, 7(2), Baran, İ. & Üçüncü, S. (1994) The state of Mertesiella lushani in Turkey. Mertensiella, Bonn, 4, Başoğlu, M. (1967) On a third form of Mertensiella luschani (Steindacner) (Amphibia, Salamandridae). Ege Üniversitesi Fen Fakültesi İlmi raporlar Serisi, Bornova-İzmir, 44, Başoğlu, M. & Baran, İ. (1976) The Subspecific Status of the Population of Mertensiella luschani (Steindacner) in the Antalya Region of Southwestern Anatolia. Ege Üniversitesi Fen Fakültesi İlmi raporlar Serisi, Bornova-İzmir, 235, Başoğlu, M., Özeti, N. & Yılmaz, İ. (1994) Türkiye Amfibileri. Ege Üniv. Fen Fak. Kitaplar Ser. No. 151, Bornova, Cox, N., Chanson, J., Stuart, S., Compilers (2006) The Status and Distribution of Reptiles and Amphibians of the Mediterranean Basin. Gland, Switzerland and Cambridge, UK: IUCN. Çiçek, K., Ayaz, D., & Mutlu, H. S. (2010): Data on Morphology of Southern Crested Newt, Triturus karelinii (Strauch, 1870) (Caudata: Salamandridae) in Uludağ (Bursa, Turkey). Biharean Biologist, Oredea, 4 (2), Gebhart, M., Roder, A. & Schmidtler, J.F. (1990) Neue Fundpunkte von Mertensiella luschani atifi Başoglu, 1967 in der Türkei. Salamandra, 26(1), Göçmen, B., Veith, M., Akman, B., Godmann, O., İğci, N. & Oğuz, M.A. (2013) New Records of the Turkish Lycian Salamanders (Lyciasalamandra, Salamandridae). North-Estern Journal of Zoology, Oradea, 9 (2), Klewen, R., Winter, H.G., & Franzen, M. (1988) Die Unterarten des Lykischen Salamanders Mertensiella luschani (Steindachner, 1891) Teil 1. Herpetofauna [Weinstadt], 10, Mutz, T., & Steinfartz, S. (1995) Mertensiella luschani flavimembris ssp. n., eine neue Unterart des Lykischen Salamanders aus der Türkei (Caudata: Salamandridae). Salamandra, 31, Öz, M. & Arikan, H. (1990) Bitlis Çevresindeki Salamandra salamandra (Urodela: Salamandridae) Populasyonu Üzerinde Taksonomik Araştırmalar. Doğa Turkish Journal of Zoology, 14, Öz, M., Düşen, S., & Tunç, M., R. (2003) Antalya Bölgesinin Herpetofaunası. Kıyı Deniz ve İçsu Biyolojik Çeşitliliği Semineri. Türkiye Tabiatını Koruma Derneği, Mayıs 2003, Finike, Antalya. Öz, M., Düşen, S., Tunç, R., Kumlutaş, Y., Durmuş, H. & Kaska, Y. (2004) A Morphological and Taxonomical Study on the Subspecies of The Lycian Salamander, Mertensiella luschani, (Steindachner, 1891) (Urodela: Salamandridae). Turkish Journal of Zoology, 28, Peters, J. A. (1964) Dictionary of herpetology: a brief and meaningful definition of words and terms used in herpetology. Hafner Publishing Company, New York and London, pp. Veith, M., Baran, İ., Godmann, O., Kiefer, A., Öz, M. & Tunç, M.R. (2001) A Revision of Population Designation and Geographic Distribution of the Lycian Salamander Mertensiella luschani (Steindachner, 1891). Zoology in the Middle East, 22(1), Veith, M. & Steinfartz, S. (2004) When Non-Monophyly Results in Taxonomic Consequences The Case of Mertensiella Within the Salamandridae (Amphibia: Urodela). Salamandra, 40(1),

8 TOK ET AL. Weisrock, D. W., Macey, J.R., Uğurtaş, I.H., Larson, A. & Papenfuss, T.J. (2001) Molecular Phylogenetics and Historical Biogeography among Salamandrids of the True Salamander Clade: Rapid Branching of Numerous Highly Divergent Lineages in Mertensiella luschani Associated With the Rise of Anatolia. Molecular Phylogenetics and Evolution, 18(3), Yildiz, M.Z. & Akman, B. (2015) A New Subspecies of Atif's Lycian Salamander Lyciasalamandra atifi (BASOGLU, 1967), from Alanya (Antalya, Turkey). Herpetozoa, 28(1-2), Ecol. Mont., 9, 2016,