Conservation Activities for Mountain Viper, Montivipera Albizona (Nilson, Andrén and Flärdh, 1990) in Anatolia, Turkey

ECOLOGIA BALKANICA 2018, Vol. 10, Issue 2 December 2018 pp. 27-40

Conservation Activities for Mountain Viper, Montivipera albizona (Nilson, Andrén and Flärdh, 1990) in Anatolia, Turkey

Kerim Çiçek1*, Murat Afsar2, Efkan Bağda3, Cemal Varol Tok4

1 - Ege University, Faculty of Science, Department of Biology, Zoology Section, 35100, Izmir, TURKEY 2 - Celal Bayar University, Faculty of Arts and Sciences, Department of Biology, Manisa, TURKEY 3 - Sivas Cumhuriyet University, Faculty of Science, Department of Molecular Biology and Genetics, Sivas, TURKEY 4 - Çanakkale Onsekiz Mart University, Faculty of Arts and Sciences, Department of Biology, 17100, Çanakkale, TURKEY * Corresponding author: [email protected] or [email protected]

Abstract. The Mountain viper, Montivipera albizona, is an endemic to Anatolia and distributes in Anatolian Diagonal, Anti-Taurus Mountains and Amanos Mountains. Unfortunately, the species faced serious threats within narrow distribution range. Here, we evaluated the present status and main threats of the Mountain viper by 60-days intensive fieldwork and interviews with locals. According to our data, the Mountain viper prefers the rocky and those mountainous and rugged areas covered with less vegetation and they are active from the beginning of April to end of November. In spring, it is possible to observe 1 to 5 individuals in the suitable habitats depending on its density. We prepared 5-year Action Plan for Turkish General Directorate of Nature Conservation and National Parks and planned the roadmap for sustainability of the species with participation of regional administration, NGOs, and locals. We found that agricultural activities, overgrazing, road constructions, quarries, pet trade, sportive hunting, deliberate or accidental killing, and climatic change are the main threats on the Mountain viper in Anatolia. The main conservation measures include: creating some protected habitats in the high viper density regions, long-term monitoring survey to obtain data on its ecology and population trends, education and awareness raising activities among locals to prevent illegal collection/killing of the vipers.

Key words: Mountain viper, biology, conservation, reptiles, research, Anatolia.

Introduction disease, unsustainable use, and global climate Reptiles contain more than 10,000 species change (ALFORD & RICHARDS, 1999; GIBBONS et (UETZ et al., 2018) and are an important part of al., 2000). Especially human-induced habitat natural ecosystems and as the indicator of loss and harvesting are the predominant threats environmental quality. The group is threatened to reptiles (BÖHM et al., 2013). by habitat loss and destruction, introduced Anatolia hosts approximately 15 viper invasive species, environmental pollution, species which belong to three genera (Vipera,

Macrovipera, Montivipera) (MALLOW et al., Kangal, Koyulhisar, Merkez, Suşehri, 2003; BARAN et al., 2012; UETZ et al., 2018). The Şarkışla, Ulaş, Yıldızeli, Zara). mountain viper genus Montivipera (NILSON et The climate is a dry-summer continental al., 1990) contains eight valid species climate (Köppen climate classification: Dsb), (Montivipera albizona, M. bornmuelleri, M. with warm and dry summers and cold and bulgardaghica, M. kuhrangica, M. latifii, M. snowy winters (PEEL et al., 2007). However, the raddei, M. wagneri, and M. xanthina, STÜMPEL north of the city (the districts of Suşehri, et al., 2016; UETZ et al., 2018) and adapted to Akıncılar, Gölova, Koyulhisar, Doğanşar, and in the high mountain ecosystems in Near and the northern part of Zara) is similar to Black Sea Middle East. The genus hosts some rare and and has oceanic climate with high and evenly narrow distributed species (M. albizona, M. distributed rainfall the year round (SK, 2018). raddei, M. wagneri, and M. xanthina) in Fieldwork. In order to obtain information Anatolia. regarding the distribution, habitat preference, Among them the mountain viper, behavior, life cycle and population condition Montivipera albizona (NILSON et al., 1990) was of the species in Sivas Province, we first described in Kulmaç Mountains which is conducted field work in May-September for formed by southeastern Sivas Province total 60 days by a 1 or 2 people teams. located in Tecer Mountains’ arc towards Location information (coordinates and north east through Sivas and Kangal (NILSON altitudes) of the places that species were et al., 1990). The species are only known from observed is recorded by using Garmin mountain ranges Anatolian Diagonal and GPSMAP 62s and a detailed distribution map cities of Sivas, Kayseri, Tunceli, Erzincan, is formed. We calculated relative density of Kahramanmaraş and Hatay, classified as M. albizona by using catch-per-unit-effort Endangered (EN) according to the IUCN Red (CPUE) indices (RODDA, 2012) [dividing the List, and its population tends to decrease number of the vipers captured by the effort (TOK et al., 2009) and listed in the Bern expended] in three locations [(1) Gürün, (1) Convention (Appendix III - Protected fauna Kangal, (1) Ulaş] and searched for the snakes species). In this study, we evaluated the on 20 m x 2 km length routes. Each route was distribution, population status, phenology sampled four times by a team of two people and potential threats of Mountain viper in between 09:00 and 18:00 hrs. in May - June province of Sivas (Anatolia, Turkey). 2017. We avoided indicating exact location Furthermore, during the field work due to illegal trade activities. The method interviews with locals were conducted in may overestimate true abundance and reduce order to learn their thoughts regarding the the capacity to detect both presence and species. In order to conserve the species severity of a population decline. However, population and its habitats, we prepared 5 the obtained data could provide a years conservation action plan according to preliminary basis for detecting relative trends literature data, field observations and in the Mountain viper. interviews with the locals. Ecological Niche Modelling. We compiled occurrence localities from available literature Material and Methods (NILSON et al., 1990; TYNIE, 1991; MULDER, Study Area. Sivas Province is 1994; 1995; GÖÇMEN et al., 2009; 2014, geographically located at the intersection of STÜMPEL et al., 2016) and our own field data. Central Anatolia, Eastern Anatolia and Black Many authors did not indicate an exact Sea regions. It has a total surface area of locality data in case of avoiding international 28.488 km² and divided into 17 districts pet trade. The locality information with no (Akıncılar, Altınyayla, Divriği, Doğanşar, coordinate data was obtained by using Gemerek, Gölova, Gürün, Hafik, İmranlı, Google Earth ver. 7.1.2 (Google Inc.).

28 Kerim Çiçek, Murat Afsar, Efkan Bağda, Cemal Varol Tok

All records were georeferenced into Precipitation of Driest Quarter, BIO19 - WGS-84 coordinate system and checked with Precipitation of Coldest Quarter] that ArcGIS (v10, ESRI). To minimize sampling underlay the current distribution model for bias which could otherwise result in the species. inaccurate projections and overestimated We modelled the geographic distribution predictive power (MEROW et al., 2013) and of the Mountain viper under present (1950- reduce spatial autocorrelation (BORIA et al., 2000) and future (2050, 2070) bioclimatic 2014; FOURCADE et al., 2014) we draw a 25 km conditions using maximum entropy buffer area each occurrence record and modelling with MAXENT 3.4.1 (PHILLIPS et thinned a total of 34 records to 22 localities for al., 2018). The MAXENT algorithm, which is ecological niche modelling. among the most effective methods of We used 19 bioclimatic variables as ecological niche modelling (ELITH et al., 2006), predictor variables for the current estimates the potential distributions of species distribution. The bioclimatic variables were from occurrence data by finding the obtained from the WorldClim data base probability distribution of the maximum (HIJMANS et al., 2005, worldclim.org) at the entropy (i.e. closest to uniform) subject to the spatial resolution of 30 arc seconds (approx. 1 constraint that the expected value of each of a km), which derived from monthly set of features (environmental variables or temperature and rainfall data as averages of functions thereof) under this estimated the period 1950–2000. The bioclimatic distribution closely matches its empirical variables for 2050 (average for 2041-2060) and average (PHILLIPS et al., 2006; PHILLIPS & 2070 (average for 2061-2080) at a spatial DUDÍK, 2008). resolution of 30 arc-seconds (WorldClim 1.4, We performed ENMeval (MUSCARELLA worldclim.org), which are projected et al., 2014) for optimizing model complexity according to intermediate (the representative to balance goodness-of-fit and predictive concentration pathways, RCP4.5) and the ability. We chose randomly selected worst (RCP8.5) emission scenario, used for background (pseudo-absences) approach predicting future distribution pattern of the (PHILLIPS et al., 2006), and k-1 jackknife species. The data set of “Hadley Global method when working with relatively small Environment Model 2 – Earth System”, data sets (PEARSON et al., 2007; developed within the scope of the 5th SHCHEGLOVITOVA & ANDERSON, 2013). We Coupled Model Intercomparison Project built models with regularization multiplier (CMIP5) by the Met Office Hadley Centre values ranging from 0.5 to 10 (increments of (UK, metoffice.gov.uk), is preferred. We 0.5) and with six different feature classes buffered the climatic variables by 0.5 degrees combinations (L, LQ, H, LQH, LQHP; where using minimum convex polygon representing L - linear, Q - quadratic, H - hinge, P - the study area. product and T - threshold) and this resulted To reduce the negative effect that might in 100 individual model runs. We applied the result from multicollinearity among the 10-percentile training presence logistic bioclimatic variables (HEIKKINEN et al., 2006; threshold approach as recommended by LIU DORMANN et al., 2013), we removed some et al. (2005), and the clog-log output was highly intercorrelated (r > 0.9 or < –0.9) transformed into a continuous map of the variables with a pairwise Pearson correlation presence-absence distribution. The clog-log and selected a subset of the bioclimatic outputs represent the habitat suitability variables based on the ecological between from 0 (unsuitable) to 1 (suitable). requirements of the species. We chose 4 Model accuracy was evaluated from four environmental variables [BIO1 - Annual evaluation metrics by ENMeval Mean Temperature, BIO15 - Precipitation (MUSCARELLA et al., 2014) in R vers. 3.5.2: the Seasonality (Coefficient of Variation), BIO17 - area under the curve of the receiver‐

29 Conservation Activities for Mountain viper, Montivipera albizona... operating characteristic plot for test localities and the grass and tragacanth on the valley

(AUCTEST) (HANLEY & MCNEIL, 1982; plains (Fig. 1). Possibly, vertical migrations PETERSON et al., 2011), the difference between into Astragalus sp. communities, rock piles training and testing AUC (AUCDIFF) and humid vegetations at lower altitudes

(WARREN & SEIFERT, 2011), OR10 (10% provides optimization of body temperature training omission rate) for test localities for long durations in the active period and (FIELDING & BELL, 1997; PETERSON et al., even helps survival in the harsh weather 2011) and the Akaike information criterion conditions. corrected for small sample sizes (AICc) During our field studies, it was noted (BURNHAM & ANDERSON, 2004; WARREN & that temperature changes throughout the day SEIFERT, 2011). We used Wallace v1.0.6.1 makes individual of species take advantage of modular platform (KASS et al., 2018) in R the shadows of tragacanths that are present in vers. 3.5.2 for preparing and analyzing of the rocky areas with high steppe vegetation species distributions. The results were and the grassy fields which is formed by the imported and visualized with ArcGIS v10.0. water accumulated in valley plains (Fig. 1A). Conservation Action Plan. Throughout our It was observed that grasshoppers, lizards fieldwork, we conducted interviews with (Ophisops elegans, Parvilacerta parva, hunters, shepherds, beekeepers, farmers and Trachylepis vittata) and small mammalian officers. We obtained knowledge (life cycle, species (Spermophilus xanthoprymnus, Microtus phenology) and opinions of locals about the sp.) also densely inhabit these areas. Also, species and we tried to confirm their validity Eirenis modestus, Dolichophis schmidti, during fieldwork. Fieldwork, interview with Macrovipera lebetina and Vipera transcaucasiana the locals and literature data on species were shares the same habitat. In the regions where used to form a draft of conservation action the species occurs, farming and husbandry plan (CAP). We followed Open Standards activities are present and also some predatory methodology (2013, cmp-openstandards.org), birds and wild animals might have some used threats classification (ver. 2.0) for threats influence on the mountain vipers in between and actions classification (ver. 2.0) keys. CAP rock piles and tragacanth communities. draft was finalized in a workshop at 27-28 Depending the climate conditions, the September 2017 after obtaining feedbacks mountain vipers are active from April to end from stakeholders. of November in Sivas Province. More active periods are mating period in spring and the Results end of hibernation. They are more frequently Field studies showed that species live in observed in mornings and the evenings, various habitats in seven districts of Sivas especially between July and September. Its Province: Divriği, Gemerek, Gürün, Kangal, relative abundance ranged 1-5 snakes in Ulaş, Yıldızeli and Zara (Fig. 1). Interview suitable habitats. with the locals also indicated the presence of The niche model indicates the primary species in Altınyayla, İmranlı and Şarkışla. factors affecting the distribution of the species The mountain vipers were observed are annual mean temperature (BIO1, 35.3%), especially in areas with lesser vegetation and precipitation of coldest quarter (BIO19, rocky hillsides with higher sun penetration. 27.2%), precipitation seasonality (BIO15, The species mostly prefer sloped valleys at 23%), precipitation of driest quarter (BIO17, higher altitude and its vertical distribution 14.5%). In the future projected models for ranges between 1300 – 2200 m a.s.l. In the 2050 and 2070, the suitable habitats of the regions that species were observed (Fig. 1B, vipers in the distributional range will C, D), specimens mostly found in dry decrease and that there will be a decrease in rugged hillsides that also inhabits thorny the southern and eastern distributional Astragalus sp. communities and pile of rocks boundaries in particular (Fig. 2).

30 Kerim Çiçek, Murat Afsar, Efkan Bağda, Cemal Varol Tok

Threats and conservation actions. Sheep shepherds kill 3-10 individuals in a year. and goat herds in the species’ habitat is are Furthermore, species’ habitat is destroyed highly frequent. The situation creates high and segregated because of the road levels of grazing pressure in the constructions and stone pit activities. environment. Hunting sports are practiced Construction activities affect the species frequently in Sivas Province. Hunters from directly by habitat loss and indirectly by neighboring districts come to Sivas Province habitat segregation. The species attracts for partridge, quail and rabbit hunting. herpers, pet traders and scientist since they Flashlight hunting in the nights puts all the have spellbinding patterns and are endemic animals in the habitat under stress. to Anatolia. Collecting the species from their Especially in the spring months, contact habitats also cause the individual loss in the between species and local people (farmers, population. beekeepers and shepherds) occurs in the The mountain viper is mainly threatened species’ habitat. Locals kill the species by agricultural activities, overgrazing, road intentionally or accidentally because they constructions and quarries, pet trade, sportive think species is poisonous or they are afraid. hunting, deliberate or accidental killing by During the interviews, it was found that locals, and climate change (Table 1, Fig. 3).

A B

C D

Fig. 1. The general view of habitat (A) and detected individuals (B,C,D) in Sivas Province.

31 Conservation Activities for Mountain viper, Montivipera albizona...

Fig. 2. Current and potential distribution of the Mountain viper (Montivipera albizona) in Anatolia. The current and future (2050, 2070) potential distribution model of the Mountain viper in Anatolia. Probability of presences increases from blue to red..

We planned some activities about prosecution, conservation designation and land/water protection, species management, planning, research and monitoring, education awareness raising, law enforcement and and training, and institutional development.

32 Kerim Çiçek, Murat Afsar, Efkan Bağda, Cemal Varol Tok

We determined that creating some protected and awareness raising activities among locals habitats in the high viper density regions, to prevent illegal collection/killing of the long-term monitoring survey to obtain data on vipers are main conservation measures for its ecology and population trends, education sustainability of the Mountain viper (Table 2).

A B

C D

Fig. 3. Some potential threats of the Mountain viper from Sivas. A: Overgrazing activities, B: Agricultural activities, C, D: Deliberate or accidental killed vipers.

33 Conservation Activities for Mountain viper, Montivipera albizona...

Table 1. The major threats for the Mountain viper (Montivipera albizona) in Sivas Province.

Major Threat Reasons Level Agriculture and Aquaculture Annual and Perennial Non-Timber Crops Intensive agricultural activities High Livestock Farming and Ranching Overgrazing High Energy Production and Mining Mining and Quarrying Road constructions, quarrying High Biological Resource Use Hunting and Collecting Terrestrial Animals Poaching for pet, and hobbyist, scientific High collection, Deliberate or accidental killing by locals Climate Change Changes in Temperature Regimes Changing phenology Unknown Changes in Precipitation and Hydrological Regimes Changing phenology Unknown

Table 2. The implementation of the conservation action plan for the Mountain viper (Montivipera albizona) in Sivas Province.

Responsible Agencies, Actions Priority Organizations and Individuals Land/water protection Site/area protection Forestry, Agricultural, Controlling some key viper habitats and not allowed grazing and Critical Governorship offices, law hunting activities in these areas. enforcers, mukhtars. Species Management Species Stewardship  The distribution maps of the species should be shared with the relevant governmental organizations for use in planning Forestry, Agricultural, in road, quarry and infrastructure works due to reducing High Water affairs, Governorship damage of the viper habitats. offices.  Taking to consider the viper conservation in other the wildlife management plans. Ex-Situ Conservation  Providing two couple of vipers to some national zoos that High Zoos, Universities. can provide the necessary conditions of the species Awareness Raising Outreach & Communications  Prevention of illegal agricultural land opening activities in the viper habitats. Forestry, Agricultural,  Carry out awareness studies on the use of incorrect High Governorship, Education pesticides and fertilizers. offices, schools.  Opening of exhibitions and stand at the festivals in Sivas Province. Law Enforcement and Prosecution Detection and Arrest Ministry of Foreign Affairs,  Reducing illegal collection of the vipers and boosting of Critical Customs Office, inspections for bio-smuggling. Governorship. Non-Criminal Legal Action High GDNCNP, Universities. • Unless the justification is well explained, the viper collection is not allowed in the natural environment for scientific purpose.

34 Kerim Çiçek, Murat Afsar, Efkan Bağda, Cemal Varol Tok

• Encouraging in-situ scientific studies in the ecology and biology of the species. Conservation Designation and Planning Protected Area Designation and/or Acquisition  Establishing protected areas in key habitats for the viper after High GDNCNP, Universities. evaluating the viper monitoring study results. Site Infrastructure  With the help of rangers, mukhtars, shepherds, beekeepers and expert personnel, the creation of inventory by recording the deaths of the vipers for the road or other reasons within Medium GDNCNP, Universities. the year.  With the help of rangers, mukhtars, NGOs and locals, the creation of information sharing network on the detection of points where species are observed. Research and Monitoring Basic Research and Status Monitoring  Conducting research or analysis on ecology and biology of the vipers. Critical GDNCNP, Universities.  Monitoring the population trend of the species over the years. Education and Training Formal Education  In order to promote the viper and to increase the awareness of protection; preparing educational material for primary GDNCNP, Forestry, and secondary schools in Sivas Province, providing Agricultural, Governorship. High information about the subject and raising awareness. Education offices,  Education and information about of officers, gendarmes, universities, schools. customshouse guards, forestry rangers against bio- smuggling. Training and Individual Capacity Development  Information the locals in the region, especially the mukhtars, the shepherds and the beekeepers on criminal penalties, prohibition of killing of species. High GDNCNP, Universities.  Providing information about the importance of the species to the locals and carrying out information activities against bio- smuggling (posters, brochures, one-to-one training etc.). Institutional Development Internal Organizational Management and Administration  Kayseri, Tunceli, Erzincan, Kahramanmaraş and Hatay where species are distributed should be informed and High GDNCNP encouraged to implement the plan activities  Organizing a workshop with all stakeholders in 2022 for the revision of the conservation action plan

Discussion November in suitable weather conditions. The Mountain viper, Montivipera Researchers that study the species detect it in albizona, is distributed in suitable habitats of various region in the Anadolu diagonal mountain range in south east of Anatolian mountain chains in Sivas Province. diagonal and lives higher altitudes of north However, exact localities are not present in arm of the Middle Toros Mountains, Anti the literature in order to prevent harms that Toros Mountains, and Amanos Mountains in might be caused by snake collectors (NILSON the south (NILSON et al., 1990; TYNIE, 1991; et al., 1990; TYNIE, 1991; MULDER, 1994; 1995). MULDER, 1994; 1995; GÖÇMEN et al., 2009; It is already known that climate changes 2014). in glacial and inter glacial periods affected The species especially prefer rocky the geographical distribution of species. regions enclosed by grass and bushes and is Thus, like many species, mountain vipers active in Sivas Region from April to also experienced enlarging and narrowing of

35 Conservation Activities for Mountain viper, Montivipera albizona... suitable habitats for their ecological niche in There have been few efforts to conserve parallel with climate changes. It is highly endangered viper species worldwide possible that the species in the same group, (MARTIZ et al., 2016). Fortunately, Turkish Montivipera wagneri lived in northeastern National Parks have been prepared end of Anatolian diagonal, Montivipera conservation action plans for three bulgardaghica lived in southeast endangered viper species in Anatolia up to Mediterranean end and Montivipera albizona now: Vipera kaznakovi, V. anatolia, and M. lived in the region between Anti-Taurus albizona. The Mountain viper is suffering Mountains and northeastern Anatolia from habitat loss and destruction, Mountains. Then, increase in the persecution, international pet trade, and disadvantageous conditions might have climatic change. The creating some protected narrowed down their habitat areas to the habitats in the high viper density regions, distribution areas of today. Some of the main long-term monitoring survey to obtain data threats against the mountain vipers are on its ecology and population trends, collection for scientific purposes and education and awareness raising activities intentional/unintentional killing by the local among locals to prevent illegal population (TOK et al., 2009) collection/killing of the vipers are main Vipers are among snakes the most possible mitigation measures for misunderstood and persecuted groups, sustainability of the vipers. while they are threatened by extinction due to their low fecundity and slow growth rate Acknowledgements (MARTIZ et al., 2016). The most important This study is part of a project “The threats for vipers are habitat loss, species conservation plan of Sivas degradation, and fragmentation (GIBBONS et viper/White-banded Mountain Viper al., 2000; DIRZO & RAVEN, 2003; WALDRON et (Montivipera albizona) in Sivas”, funded by al., 2006; FISCHER & LINDENMAYER, 2007; the Directorate of Sivas Branch of the 15th TUNIEV & TUNIEV, 2009; MADSEN & UJVARI, Regional Directorate of the Department of 2011; MARTIZ et al., 2016). Nature Protection and National Parks of the International trade of viper species is a Republic of Turkey, Ministry of Forestry and global phenomenon and its effects on the Water Affairs and AK-TEL Ltd.Sti. We are wild population still not known (IUCN, grateful to these organizations for their 2015; MARTIZ et al., 2016). Furthermore, generous financial support. We also thank to climate changes cause some viper species John Mulder for sharing field experience under extinction risk (MARTIZ et al., 2016). with us and Çağdaş Yaşar for GIS mapping. Change in the climate might affect immune system functionality (KOBOLKUTI et al., 2012), References alter life-history traits (e.g. ALTWEGG et al., ALFORD R.A., S.J. RICHARDS. 1999. Global 2005), trigger phenological changes amphibian declines: a problem in (RUGIERO et al., 2013), negatively impact the applied ecology. - Annual Review of populations (BRITO et al., 2011; LE GALLIARD Ecology and Systematics, 30(1): 133-165. et al., 2012), and narrow their geographical [DOI]. ranges (e.g., BOMBI et al., 2011; DAVIS et al., ALTWEGG R., S. DUMMERMUTH, B.R. ANHOLT, 2015). The distribution of the Mountain viper T. FLATT. 2005. Winter weather affects could be narrowed from southern direction asp viper Vipera aspis population in particular. Besides, its life-history traits, dynamics through susceptible phenology and population structure and juveniles. - Oikos, 110(1): 55-66. [DOI]. fluctuation might be dependent on climate BARAN İ., Ç. ILGAZ, A. AVCI, Y. KUMLUTAŞ, changes. K. OLGUN. 2012. Türkiye Amfibi ve

36 Kerim Çiçek, Murat Afsar, Efkan Bağda, Cemal Varol Tok

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