Zinenko_et_al_Vipera_anatolica_HErPEtoZoa.qxd 11.02.2016 17:00 seite 1

HErPEtoZoa 28 (3/4): 141 - 148 141 Wien, 30. Jänner 2016

rediscovered and critically endangered: anatolica EisElt & B aran , 1970, of the western taurus Mountains (), with remarks on its ecology (: serpentes: )

Wiederentdeckt und stark gefährdet: Vipera anatolica EisElt & B aran , 1970 aus dem westlichen taurus-gebirge (türkei), mit angaben zur Ökologie dieser art (squamata: serpentes: Viperidae)

olEKsandr ZinEnKo & a ZiZ aVci & F riEdEriKE sPitZEnBErgEr & a ndriy tuPiKoV & K onstantin sHiryaEV & E Min BoZKurt & Ç Etin ilgaZ & n iKolaus stüMPEl

KurZFassung

das Vorkommen von Vipera anatolica EisElt & B aran , 1970 im gebiet der terra typica (dem Zedernwald- reservat “Çığlıkara ormanɪ” im westlichen taurus-gebirge, südtürkei) wurde 29 Jahre nach der letzten Feststellung bestätigt. an drei, nur zwei Kilometer voneinander entfernten orten wurden 19 individuen gefunden. alle Fund plätze befanden sich in Karstdolinen oberhalb der Baumgrenze zwischen 1840 - 1950 m seehöhe. Beobachtungen aktiver schlangen erfolgten bei tag zu anfang Mai, Mitte Juli und in der zweiten septemberhälfte. Weibchen mit Körperlängen von 242-360 mm waren bereits geschlechtsreif; die trächtigkeit kann sich mindestens bis in die septembermitte erstrecken. das gleichzeitige Vorkommen trächtiger und nicht trächtiger Weibchen im sommer scheint darauf hinzuweisen, daß Weibchen sich nicht jedes Jahr fortpflanzen. außerhalb der terra typica wurden zwei potentiell geeignete Berge in der umgebung untersucht. neue Vorkommen wurden jedoch nicht gefunden. überweidung dürfte der wesentlichste gefährdungsfaktor für diese nur aus dem gebiet der terra typi - ca bekannte art sein, da alle Fundplätze in gering beweideten gebieten lagen.

aBstract

the occurrence of Vipera anatolica EisElt & B aran , 1970, in the territory of the type locality (cedar forest reserve “Çığlıkara ormanɪ” in the western taurus Mountains of southern turkey) was confirmed 29 years after the last observation. nineteen specimens were found in three localities, situated two kilometers from each other, and located in karst dolines above the tree line between 1,840 and 1,950 m a. s. l. active were observed during daytime in the beginning of May, mid July and the second half of september. Vipera anatolica is characterized by small maturation size in females (242-360 mm); gravid females were found until the middle of september. the simultaneous presence of pregnant and non-pregnant females in summer indicates that females may not give birth each year. two neighboring mountain massifs within the altitudinal range of V. anatolica were visited, but addi - tional populations were not found. overgrazing seems to be the main threat to the since the record locali - ties were associated with low grazing activity and contrasted with potentially suitable habitats where high grazing pressure was present. KEy Words reptilia: squamata: serpentes: Viperidae; Vipera anatolica , distribution, ecology, conservation; Kohu dağ, “Çığlıkara ormanɪ”, Elmalı, antalya, western taurus Mountains, turkey

introduction

Vipera anatolica EisElt & B aran , Baran 1970; B illing 1985; s igg 1987; nil - 1970, is the rarest and least known species son & a ndrén 2001 ), all found in one of small vipers of the subgenus Pelias MEr - locality, the Kohu dağ Massif in the western rEM , 1820 , with only five specimens de - taurus Mountains south of Elmalı, antalya, scribed in the scientific literature ( EisElt & southwest turkey. it is also listed in the Zinenko_et_al_Vipera_anatolica_HErPEtoZoa.qxd 11.02.2016 17:00 seite 2

142 o. Z inEnKo et al.

of threatened species as specimens were collected ( sPitZEnBErgEr critically Endangered ( toK et al. 2009). in EisElt & B aran 1970) and of localities in the species represents an old evolutionary which the species was observed ( Billing lineage that split off from the stem of the 1985; s igg 1987) as well as several attempts (BonaPartE , 1835), V. renar - to find it ( nilson , a ndrén & F lärdH 1988; di (cHristoPH , 1861) and the V. kaznakovi nilson & a ndrén 2001; M ario scHWEi- niKolsKy , 1909 complexes ( KalyaBina - gEr , pers. comm.), it was not found for almost HauF et al. 2004: stüMPEl 2012; ZinEnKo three decades until its recent rediscovery in et al. 2015). it is the relict representative of 2014 ( gÖÇMEn et al. 2014; ZinEnKo et al. the subgenus Pelias in southwest turkey, 2014). the aim of the present research was isolated from other species of the group by to confirm the presence of V. anatolica in several hundred kilometers. it is similar in the area of the type locality, search for addi - external morphology to V. ursinii and was tional populations in potential habitats with - initially described as V. u. anatolica and in the altitudinal range of V. anatolica and later treated as a member of the V. ursinii collect primary information about the ecol - complex ( nilson & a ndrén 2001). in spite ogy of this species, necessary for evaluating of the big interest in this species, the precise its current status and further development of description of the area in which the type conservation measures.

MatErials and MEtHods

Field work was conducted during four ferent habitats at altitudes between 1,550 periods (3-10 May, 11-17 July and 13-19 and 2,220 m a. s. l. time and circumstances september, 2013 and 14-20 september, 2014) of 19 observations were recorded, in the territory of the type locality of V. ana - including search effort (amount of fieldwork tolica , the cedar forest reserve “Çığlıkara in person-hours), sex, age, reproductive and ormanɪ” and adjacent parts of the Kohu dağ physiological status of the observed speci - Massif, as well as in adjacent alaca dağ and mens. Pres ence or absence and amount of Bey dağ Massifs (Fig. 1) in the western developing embryos and food objects in the taurus Mountains, south of Elmalı, antalya, stomachs were checked by palpation. turkey. in July, special attention was paid to grazing load was estimated indirectly by those places where the first specimen was the level of vegetation degradation and pro - observed during the fieldwork of one of the portion of poisonous ( Daphne sp. and Eu - authors (Fs) in 1969. in total, an area of phorbia sp.) and spiny shrubs ( Astragalus approximately 420 hectares was surveyed sp., Acantholimon sp . and Berberis sp.) ver - there, consisting of mountain sus grasses. the area was considered highly grazed by sheep and goats during the sum - grazed if poisonous and spiny vegetation, mer months, and near natural near and a large surface proportion of bare soil the upper tree line within the protected area prevailed. air temperatures in the shade of the forest reserve. were measured at 0.1 m above the ground. the authors searched for active snakes neither pictures nor coordinates of the on the surface, under stones and among veg - localities are provided here due to conserva - etation during daytime (searches were con - tion reasons. ducted between 07:00 and 20:00 h), in dif -

______

(*) – 6.9 (nine karst dolines within an area of 420 ha on the Kohu dağ); 7.64 (seven karst dolines within an area of 337 ha on the Bey dağ); 0.07 (one karst doline within an area of 190 ha on the alača dağ). (*) – 6.9 (neun Karst-dolinen innerhalb eines areals von 420 ha auf dem Kohu dağ); 7.64 (sieben Karst- dolinen innerhalb eines areals von 337 ha auf dem Bey dağ); 0.07 (eine Karst-doline innerhalb eines areals von 190 ha auf dem alača dağ). Zinenko_et_al_Vipera_anatolica_HErPEtoZoa.qxd 11.02.2016 17:00 seite 3

the rediscovered Vipera anatolica EisElt & B aran , 1970 143

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Fig. 1: Zones at altitudes between 1,840 and 2,265 m a. s. l. in the western taurus Mountains (Elmalı, antalya, turkey) , potentially habitable for Vipera anatolica EisElt & B aran , 1970 . the authors searched for the viper in the encircled areas east of the type locality (Kohu daǧ). the habitable area between 1,840 and 2,265 m is shown by black. abb. 1: die Höhenzone zwischen 1840 und 2265 m ü. M. im westliches taurus-gebirge (Elmalı, antalya, türkei ), potentieller lebensraum von Vipera antolica EisElt & B aran , 1970. umrandet sind die östlich der typuslokalität (Kohu daǧ) gelegenen untersuchungsgebiete der autoren. die ökologisch präferierte Zone zwischen 1840 und 2265 m ü nn ist schwarz dargestellt.

rEsults and discussion

Habitat.- Vipera anatolica individ - Billing (1985) and sigg (1987), except that uals were found in three localities situated at they are at higher altitudes and always asso- a distance of about two km from each other ciated with open mountain grasslands (table in the Kohu dağ Massif only. their charac - 1). gÖÇMEn et al. (2014) gave a very similar teristics, along with those of areas where description of the habitats but raised the snakes were not found, are given in table 1. upper border of the vertical distribution to all the observations were made either on 2,265 m a.s.l. in addition to the sympatric the bottom, on slopes or in close vicinity of and amphibians mentioned by sigg karst dolines, surrounded by drier hills, sep - (1987) and gÖÇMEn et al. (2014), Mon - arating populations in the dolines from one tivipera xanthina (gray , 1849) was observed another. the maximum distance between just a few tens of meters away from the first observed within localities did not V. anatolica locality, at the same elevation exceed 60 meters (locality 1) and 130 but on drier stony slopes. meters (locality 2), respectively. seasonal and diurnal activi - the three new localities match the ear - ty.- the observations of the snakes cov - lier descriptions by EisElt & B aran (1970), ered the period between May 8 and sep- Zinenko_et_al_Vipera_anatolica_HErPEtoZoa.qxd 11.02.2016 17:00 seite 5

the rediscovered Vipera anatolica EisElt & B aran , 1970 145

Fig. 2: dorsal view of an adult female (a) and an adult male (b) specimen of Vipera anatolica EisElt & B aran , 1970 , from Kohu-dağ and “Ç ığl ıkara ormanɪ”, Elmalı, antalya, turkey. abb. 2: dorsalansicht eines adulten Weibchens (a) und eines adulten Männchens (b) von Vipera anatolica EisElt & B aran , 1970 . Fundorte: Kohu-dağ und “Çığlıkara ormanɪ”, Elmalı, antalya, türkei.

tember 19, while previous published find - temperatures between 18-25 °c. an adult ings occurred in June-July ( EisElt & B aran female found on 13 July was in the last 1970; s igg 1987). according to gÖÇMEn et stages of shedding. night temperatures in al. (2014) snakes stay outside till the first July fell to 13 °c and even 5 °c near the week of october. in May, adult males and bottom of deep dolines. notably, the maxi - females (Fig. 2) and one juvenile male spec - mum observed activity of V. anatolica imen were found outside their shelters be - occurred at midsummer (table 1), coincid - tween 10:00 and 12:50 h at air temperatures ing with the highest density of the prey, of 21-23 °c. during nights, temperatures mainly different species of orthopterans, fell to 5.2 °c. adult males were freshly available at this time. shed, indicating that the snakes must have on the contrary, during the autumn emerged from hibernation places between observations of 2013, three of four snakes three to five weeks earlier, at the beginning (two adult males and two adult females) to middle of april and the spring molting of were found active in the second half of the males was already completed, as is typical day, at different days between 17:35 and for all small vipers ( nilson 1980; l icHt 17:40 h; only one male snake was found at 1984). active individuals were, however, 09:55 h. air temperatures at that time were never found in april ( gÖÇMEn et al. 2014). higher than in summer and fluctuated be- the authors of the present paper observed tween 22.4-29 °c. the lowest night tem - shedding males and found shed skins in the perature was 7.5 °c. all three males found habitat at the end of september, close to the in 2014 were observed outside their hiding beginning of hibernation. at the same time, places at midday between 13:00-15:00 h, it is difficult to believe that males of V. ana - probably due to lower ambient tempera - tolica could have developed an exceptional tures, not exceeding 15 ºc. shedding cycle in lacking an early spring thus, the mountain habitats of Kohu molt unlike all other small Eurasian vipers dağ and “Çığlıkara ormanɪ” provide to some (nilson 1980; K otEnKo 1989; s o KoloV extent temperate thermal regimes, which ex- 1989; P aVloV 2003 ). the subsequent mat - plains the existence of small viper species in ing activity or traces of recent copulations southwest turkey. the seasonal activity of were not observed. V. anatolica (see also gÖÇMEn et al. 2014) in July, basking and foraging snakes seems to be comparable to the activity pat - (adult females and subadult specimens of terns of other taxa of the subgenus Pelias , both sexes; seven snakes in total) were especially V. ursinii (B aron 1992; BEa et al. observed between 8 a. m. and 11 a. m., at air 1992; Baron et al. 1996) and the montane Zinenko_et_al_Vipera_anatolica_HErPEtoZoa.qxd 11.02.2016 17:00 seite 6

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species of steppe vipers, for example Vipera pregnant but well fed females indicates a eriwanensis (rEuss , 1933). reproductive cycle which lasts more than Feeding.- no prey was found in one year, which is usual in vipers ( saint the stomachs of the snakes in May, but four girons & K raMEr 1963; B aron 1992; out of seven snakes caught in July contained Baron et al . 1996; l ourdais et al. 2002). remnants of prey in their stomachs, presum - the reproductive period also seems to shift ably orthopterans, and remnants of grass- to the late season in high altitude habitats, hoppers were revealed in the faeces of two and as a result, parturition in V. anatolica can specimens in July and september. different take place as late as in the second half of species of orthoptera (caelifera: genera Cal- september, similar to V. ur sinii (Baron liptamus , Euchorthippus , Chorthippus , Do- 1992; BEa et al. 1992; Baron et al. 1996). ciostaurus , Stenobothrus ; Ensifera: genera conservation.- the highest ap- Poecilimon , Tettigonia , Paradrymadusa , parent abundance of V. anatolica (0.45 spec - Metriopera ) were very abundant in the sites imens per person-hour spent in the field – where snakes were observed in July. a table 1) is similar to other mountain popu - higher abundance of grasshoppers differen - lations of the V. ursinii complex (luisElli tiates habitats where snakes were found 2004), which seem to be ecologically very from neighboring territories where snakes similar to V. anatolica . despite extensive were not found. the authors believe that V. searching, no snakes were found in nine anatolica can specialize in eating represen - carefully investigated, more intensively tatives of the order orthoptera, like V. ursinii grazed neighboring valleys (table 1). over - (Baron 1992; BEa et al. 1992). the authors grazing is considered a strong threat to V. often encountered Ablepharus chernovi ursinii in and (luisElli 2004 ; darEVKsy , 1953, and more rarely Anato - FiliPPi & l uisElli 2004; Z aMFirEscu et al. lacerta oertzeni WErnEr , 1904, in the habi - 2011 ) but it is not mentioned as a threat in tat of V. anatolica . apparently, these lizards the iucn assessment of the species state by could be additional feeding objects for toK et al. 2009). sigg (1987) already drew vipers in spring and autumn when there are attention to the degradation of the natural very few insects. this would especially vegetation in the Kohu dağ area due to concern young individuals (see also sigg overgrazing. the authors of the present 1987). observations by gÖÇMEn et al. paper consider overgrazing, with conse - (2014) of V. anatolica feeding on A. cher - quent depletion of the insect fauna, to cause novi and Chorthippus and attempts of grasp - the absence of vipers in open slopes outside ing of A. oertzeni are in line with the above the protected areas and represent a main suggestions. threat for the species. restricting the live - reproduction.- Both adult fe - stock in the open grasslands in the area males found in May were well fed, but no could positively influence the population eggs could be palpated. one of three adult situation in the Kohu dağ Mountain. Both females in July, and one of two adult females potential areas visited (Bey dağ and alača in september, showed no signs of pregnan - dağ), although similar in altitude, geology cy, whereas three females found at the same and vegetation to the Kohu dağ record times had well developed eggs. the small - localities, lacked sites unaffected from graz - est pregnant females had total body lengths ing and thus, represented different stages of of 242 mm (19 september) and 256 mm (15 degradation of the natural vegetation with July) with three eggs each. another snake low density of potential prey and no vipers found on 17 July, with a body length of 295 found. it is not known if these sites were mm, contained six eggs. compared to other ever inhabited by the snake in the recent small vipers, females of V. anatolica enter (historical) past or at any time after the iso - maturity at remarkably small size. again, it lation of V. anatolica in south-west turkey resembles most closely the maturity size of about five Mya at the Miocene-Pliocene V. u. ursinii , and the number of embryos also boundary ( ZinEnKo et al. 2015) . today, the fits the range of the latter species (31.5 cm; deep valleys separating these mountain 1-7 embryos according to Baron et al. 1996 massifs are absolutely insurmountable for and Baron 1997). the occurrence of non- vipers which are strictly adapted to high Zinenko_et_al_Vipera_anatolica_HErPEtoZoa.qxd 11.02.2016 17:00 seite 7

the rediscovered Vipera anatolica EisElt & B aran , 1970 147

altitude environment, constraining them to 1987; n ilson , a ndrén & F lärdH 1988) persevere on sky islands. in the case of through the 1990s (goran nilson , pers. proper habitat management they could rep - comm.) until today. For the conservation of resent sites where mirror populations could this species it is therefore most important to be introduced. maintain the status quo of human influence nonetheless, the Kohu dağ population in the area of Çığlıkara and adjacent Kohu of V. anatolica still exists today in the area dağ mountains. Further search for addi - of the type locality where there are no sys - tional populations on adjacent mountain temic changes in habitat distribution or level massifs and consequent protection is very of human activity from the 1980s when the desirable for a long lasting perspective on V. discovery of the species occurred ( sigg anatolica conservation.

acKnoWlEdgMEnts

the Mohamed bin Zayed species conservation for consultations and oksana tishenko (tula) and Fund financially supported the project (Project no. Matthew Holding (columbus) for the help with editing. 12254979). the authors are grateful to u. Joger the authors are also thankful to Edmund Weiss (Wien), (Braunschweig) for long lasting research support, who participated in the field study and provided valu - Metehan Kır (aydın) for field assistance, taras Pushkar able information about the type specimens’ collection (Kyiv) for identification of orthoptera species, Mario sites. schweiger (obertrum) and göran nilson (göte borg)

rEFErEncEs

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saint girons , H. & K raMEr , E. (1963): le ZaMFirEscu , s. & s trugariu , a. & g HErgHEl , cycle sexuel chez Vipera berus (l.) en montagne.- i. & Z aMFirEscu , o. (2011): Human impact on habitats revue suisse de Zoologie, genève; 70 (9): 191-220. of the meadow viper ( Vipera ursinii ) in Eastern ro- sigg , H. (1987): nachforschungen über Vipera mania.- analele ştiinţifice ale universitaţii “alexandru ursinii anatolica EisElt und Baran , 1970 im west - ioan cuza” [= annals of the “alexandru ioan cuza” lichen taurus.- Herpetofauna, Weinstadt; 9: 25-34. university], iaşi; (sect. 2a, Biologie animala) 57: 43- soKoloV a. s. (1989): shedding of adult males 56. of the common adder in tambov region.- Voprosy ger- ZinEnKo , o. & a Vci , a. & s PitZEnBErgEr , F. & petologii. abstracts of the report at the 7th all-ussr tuPiKoV , a. & s HiryaEV , K. & B oZKurt , E. & i lgaZ , conference of Herpetology, Kyiv, pp. 112-113; nau- c. & s tüMPEl , n . (2014): our present knowledge about kova dumka. the anatolian Viper ( Vipera anatolica EisElt et Baran , stüMPEl , n . (2012): Phylogenie und Phylo- 1970) with remarks about species ecology and conser - geographie eurasischer unter besonderer Be- vation status. 4th conference on the Biology of the rücksichtigung der orientalischen Vipern der gattun- Vipers, october 10-13, 2014, athens, . Program gen Montivipera und . dissertation. tech- and abstracts p. 56. nische universität Braunschweig, pp. 244. WWW ZinEnKo , o. & s tüMPEl , n. & M aZanaEVa , l. document available at < http://digisrv-1.biblio.etc.tu- & B aKiEV , a. & s HiryaEV , K. & P aVloV , a. & K o- bs.de:8080/docportal/servlets/McrFilenodeservlet/ tEnKo , t. & K uKusHKin , o. & c HiKin , y. & d uisEBa- docPortal_derivate_00022753/genehmigte_Phd_2012 JEVa , t. & n ilson , g. & o rloV , n. l. & t uniyEV , s. _final.pdf;jsessionid=7BE66E5E1397cF07566E53 & a nanJEVa , n. B. & M urPHy , r. W. & J ogEr , u. B60EB1aB73 > (2015): Mitochondrial phylogeny shows multiple toK , V. & u ğurtas , İ. & s EVinÇ , M. & B ÖHME , independent ecological transitions and northern dis - W. & c rocHEt , P.-a. & J ogEr , u. & K asKa , y. & persion despite of Pleistocene glaciations in meadow KuMlutaş , y. & K aya , u. & a Vci , a. & ü ZüM , n. & and steppe vipers ( Vipera ursinii and ).- yEniyurt , c. & a Karsu , F. (200 9): Vipera anatolica . Mo lecular Phylogenetics and Evolution, Waltham; 84: in: iucn 2013. iucn red list of threatened species. 85-100 [http://dx.doi.org/10.1016/j.ympev.2014.12. Version 2013.2. . downloaded 005]. on 9 March 2014.

datE oF suBMission: July 7, 2014 corresponding editor: Heinz grillitsch

autHors: oleksandr ZinEnKo (corresponding author < [email protected] >) 1) , aziz aVci 2) , Friederike sPitZEnBErgEr 3) , andriy tuPiKoV 4) , Konstantin sHiryaEV 5) , Emin BoZKurt 6) , Çetin ilgaZ 7) & nikolaus stüMPEl 8) 1) the Museum of nature at V. n. Karazin Kharkiv national university, trinkler str. 8, Kharkiv, 61058, ukraine; dvorichansky national Park, Privokzalna str. 51, dvorichna, 62701 Kharkiv region, ukraine; < zinenkoa @yahoo.co m >; 2) adnan Menderes university, Faculty of art and science, department of Biology, aydın, 09010 aydın, turkey; < [email protected] >; 3) Batlife , c/o naturhistorisches Museum Wien, säugetier sammlung, Burgring 7 1010 Wien, austria; < [email protected] >; 4) dvorichansky national Park, Privokzalna str. 51, dvorichna, 62701 Kharkiv region, ukraine; < [email protected] >; 5) tula regional Exotarium, 300002, oktyabrʾskaya str. 26, tula, ; < [email protected] >; 6) adnan Menderes university, Faculty of art and science, department of Biology, aydın, turkey; < [email protected] >; 7) dokuz Eylül university, Faculty of science, department of Biology, Buca-İzmir, 35150 turkey ; < [email protected] >; 8) staatliches naturhistorisches Museum, gausstraße 22, d-38106 Braunschweig, ; < nikolaus. [email protected] >