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BIHAREAN BIOLOGIST 10 (2): 104-108 ©Biharean Biologist, Oradea, Romania, 2016 Article No.: e161302 http://biozoojournals.ro/bihbiol/index.html

Predicting the current and future potential distributions of Anatolia , strauchii (Steindachner, 1887), with a new record from Elazığ (Eastern Anatolia, Turkey)

Cemal Varol TOK1, Mustafa KOYUN2 and Kerim ÇIÇEK3,*

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, Bingöl University, 12000, Bingöl, Turkey. 3. Zoology Section, Department of Biology, Faculty of Science, Ege University, 35100, Izmir, Turkey. *Corresponding author, K. Çiçek, E-mail: [email protected] / [email protected]

Received: 26. Sepember 2015 / Accepted: 05. February 2016 / Available online: 31. October 2016 / Printed: December 2016

Abstract. Here, the current and future distributions of was predicted by using the maximum entropy ecological niche modeling. The most important factors which shaped the present distribution of the are isothermality and precipitation of driest month. The species is particularly distributed on the Euphrates Valley and in the west and south of Lake Van. According to the future model scenarios, it is predicted that depending on the climate change, there will be some loss in the habitats suitable for the species to inhabit and that its distribution will particularly tend to narrow from its western and eastern boundaries. Accordingly, the pressure of climate change and the other factors on the species is also discussed. In addition, the record of N. strauchii from a new locality in Elazığ (Eastern Anatolia) is first provided in this study.

Key words: Anatolia Newt, Neurergus strauchii, global climate change, ecological niche modeling, Eastern Anatolia.

Introduction Stuart et al. 2004, AmphibiaWeb 2015). Climate changes are hypothesized to be one of the most important factors to di- The genus Neurergus comprises of four valid species [Neur- rectly and indirectly trigger this decline (Pounds et al. 1999, ergus strauchii (Steindachner 1887), N. crocatus Cope, 1862, N. Blaustein et al. 2001, Kiesecker et al. 2001, Carey & Alexan- kaiseri Schmidt, 1952, and N. microspilotus (Nesterov 1916)] der 2003). This study aims to determine the environmental distributed in the Middle East (Anatolia, Iran, and Iraq) factors affecting the distribution of Anatolia Newt, Neurergus (Levinton et al. 1992, Schmidtler 1994, Papenfuss et al. 2009). strauchii, to describe the current ecological niche of the spe- Anatolia Newt, N. strauchii, is currently known from central cies and to forecast the potential distribution pattern in the Turkey and the western area of Lake Van in eastern Turkey future periods (2050 and 2070). (Schmidtler & Schmidtler 1970, Öz 1994). The species is listed as vulnerable in the IUCN Red List of Threatened Spe- cies due to its occupancy area, which is less than 2,000 km2, Material and Methods its fragmented distribution, and (Papen- In our fieldwork in 2013, six individuals of Neurergus strauchii at dif- fuss et al. 2009). Neurergus s. strauchii has a wider distribu- ferent larval stages are detected in one of the tributaries of River Ti- tion and is found in the east from River Euphrates up onto gris in the 163rd km of the Elazığ-Maden highway [Lat: 38.458, long.: the Lake Van area, and subspecies N. s. barani Öz, 1994 is 39.623, 1378 m a.s.l.]. Therefore, by thinking that the distribution of found only in the mountains located in the south-east of the species is not known exactly and that distributional boundaries Malatya (Pasmans et al. 2006). Anatolia Newt inhabits the might be wider, the potential distribution of the species is predicted small and cool mountain streams and overwinters on land by using its existing records. There are 36 records of the species (Ba- under stones and in burrows (Schmidtler & Schmidtler 1970, şoğlu et al. 1994, Baran & Öz 1986, Öz 1994, Steinfartz et al. 2002, Bogaerts et al. 2006, Pasmans et al. 2006, Özdemir et al. 2009, Schnei- Başoğlu et al. 1994). der & Schneider 2010, Coşkun et al. 2013, Koyun et al. 2013). To cor- The analysis of the relationship between species and en- rect for sampling bias and to reduce spatial autocorrelation (see Gür vironment has continually been one of the basic issues of 2013, Perktaş et al. 2015), 9 of the existing records, which are quite ecology (Guisan & Zimmermann 2000). The prediction of the close, are excluded and 27 records are included in model. The local- distributions of species has an essential place in the applica- ity information with no coordinate data is obtained by using Google tions concerning ecology, evolution, and conservation biol- Earth vers. 7.1.2 (Google Inc.). All records are georeferenced into ogy (Elith et al. 2006), and ecological niche modeling is a WGS-84 coordinate system and checked with ArcGIS vers.10.0 (ESRI). valid means of determining the potential distributions of Nineteen climatic variables are obtained from WorldClim ver.1.4 species (Guisan & Thuiller 2005, Elith et al. 2006). For the last data set (Hijmans et al., 2005, http://www.worldclim.org) at a spa- 20 years, many methods of finding out the distributions of tial resolution of 30 arc-seconds (approx. 1 km in the equator), which species (e.g. generalized additive models, GARP, BIOCLIM, represent monthly temperature and rainfall data as averages of the and MAXENT) are developed, and the most important dif- period 1950–2000. The bioclimatic variables for 2050 (average for ference among these methods is the type of data they use 2041-2060) and 2070 (average for 2061-2080) at a spatial resolution of (Elith et al. 2010). MAXENT’s predictive performance is con- 30 arc-seconds (WorldClim 1.4, sistently competitive with the highest performing methods http://www.worldclim.org/cmip5_30s), which are projected ac- cording to intermediate emission scenario the representative concen- (Elith et al. 2006, Graham & Hijmans 2006, Hijmans & Gra- tration pathways (RCP) 4.5, used for determining future distribution ham 2006, Elith et al. 2010, 2011), particularly in cases, in pattern of the species. The RCP 4.5 represents stabilization without which the sample size is low (Elith et al. 2006, Hernandez et overshoot in the amount of global radiative forcing expected by the al. 2006). end of the 21st century stated in the Fifth Assessment Report by the Global declining of is expressed by many re- IPCC. The data set of “Hadley Global Environment Model 2 - Earth searchers (e.g. Alford & Richards 1999, Houlahan et al. 2000, System”, developed within the scope of the 5th Coupled Model In- Predicting the current and future potential distributions of Anatolia Newt 105 tercomparison Project (CMIP5) by the Met Office Hadley Centre (UK, http://www.metoffice.gov.uk/), is preferred. The climatic variables are masked between 37o to 45o E and 36o to 40oN represent- ing the study area (the mask or M area; see Perktaş et al. 2015). To reduce the negative effect that might result from multicollin- earity among the environmental variables (Heikkinen et al. 2006), we selected a subset of the bioclimatic variables based on the ecological requirements of the species and pairwise Pearson correlations (r < 0.75). We chose 8 environmental variables [bio1 = annual mean tem- perature, bio2= mean diurnal range (mean of monthly (max temp - min temp)), bio3 = isothermality (bio2 / bio7) (* 100), bio7 = annual temperature range (bio5 - bio6), bio8 = mean temperature of wettest quarter, bio12= annual precipitation, bio14 = precipitation of driest month, and bio15 = precipitation seasonality (coefficient of varia- A.) tion)]. MAXENT vers. 3.3.3k (Phillips et al. 2006, 2008, 2009) program is used to model the potential distribution of the species. The MAX- ENT algorithm estimates the potential distributions of species from locality point data by finding the probability distribution of the maximum entropy (i.e. closest to uniform) subject to the constraint that the expected value of each of a set of features (environmental variables or functions thereof) under this estimated distribution closely matches its empirical average (Phillips et al. 2006, 2008). MAXENT logistic outputs represent the habitat suitability ranging from 0 (unsuitable) to 1 (suitable). The program set with the default settings. We used 10-fold cross-validation with 5000 number of itera- tions. We applied the 10 percentile training presence logistic thresh- B.) old approach as recommended by Liu et al. (2005), and the logistic output is transformed into a map of the presence-absence distribu- Figure 1. A general view of the stream (Elazığ) where the speci- tion. Model accuracy is evaluated from area under the receiver- mens are found (a) and three N.strauchii larvae (b). operator curve (AUC), and the averages of all models are imported and visualized with ArcGIS vers.10.0. that there will be a decrease in the western (Malatya) and eastern (Siirt) distributional boundaries in particular (Figs 3, Results 4).

During our fieldwork on November 23, 2013, 6 larvae of Neurergus strauchii at different stages are caught in one of the Discussion tributaries nourishing the river in Karataş district of River Tigris (Figs 1a, b). The average total length of the larvae is Anatolia Newt, Neurergus strauchii, is in the vulnerable cate- 50.5 mm (SD = 2.77 mm, range = 43.3 - 59.1 mm). The water gory in the IUCN (Papenfuss et al. 2009) red list as it only temperature in the slowly moving brook where the speci- inhabits the East Anatolian Region (Turkey) and has a nar- mens are caught is measured as 10oC and the air tempera- row range. According to the coordinate data, the species in- ture as 16oC. Both sides of the streambed in this section are habits mountain waters at altitudes between 946m and steep, and plants are presented by oriental plane, willow, 2,695m. It is reported that the water temperature in the and poplar, along with shrubs and grass. Since this section breeding period varies between 10oC and 17.3oC (Schmidtler of the river is highly sloping, the current is quite fast. Exces- & Schmidtler 1970, Pasmans et al. 2006). Bogaerts et al. sive deteriorations of the streambeds are seen due to the (2010) reported that breeding continued even in waters intercity roadwork in the region. The larvae are kept in an where the water temperature fell as low as 6oC. The breeding aquarium (L x D x H, 50 x 30 x 20 cm) under captivity condi- period is in April through June. The new locality we de- tions for a while for photographing, measurement, and ob- tected in Elazığ is on the western border of subspecies Neur- servation, and it is observed that a 58.3-mm-long specimen ergus s. strauchii (Fig. 1). At the same time, the larvae ob- reached a length of 130mm in about 80 days and completed served in November show that the breeding period also con- its metamorphosis. tinues after June according to the geographical region. No The mean AUC value of the current distribution consen- adult individual is encountered in our sampling. This is sus model (Fig. 2) is quite high (0.970). According to the probably related to the fact that they made a transition to the model, the primary factors affecting the distribution of the terrestrial form in this season. On the other hand, it is ob- species are isothermalitly (53.3%) and precipitation of driest served that the larvae could not complete metamorphosis month (32.9%). The contributions of the other variables are due to unfavorable conditions and would probably overwin- in the range 0.1 - 4.4%. The distribution model of the species ter in larval form. Fleck (1982) and Pasmans et al. (2006) pre- quite resembles its known distributional range. Neurergus viously observed overwintering of the N. strauchii larvae. strauchii is particularly distributed on the Euphrates Valley The overwintering behavior in larvae is also observed in and in the west and south of Lake Van (Fig. 2). In the future other species (e.g. Boone et al. 2004, Kishida & projected models of the species, it is observed that the suit- Tezuka 2013). able habitats in the distributional range will decrease and The prediction of the distributions of species has an im-

106 C.V. Tok et al.

Figure 2. The current potential distribution model of N.strauchii in Turkey. The visible area in maps is between 37o to 45o E and 36o to 40oN representing our study area. Probability of presences increases from blue to red. The circles denote the known literature records, whereas the star denotes the new locality. The shaded area is the IUCN distribution map.

Figure 3. The future (2050) pre- diction of the geographic distri- bution of N.strauchii in Turkey.

Figure 4. The future (2070) pre- diction of the geographic distri- bution of N.strauchii in Turkey.

Predicting the current and future potential distributions of Anatolia Newt 107

portant place in the applications about ecology, evolution, elements (Bogaerts et al. 2006, Pasmans et al. 2006, Schneider and conservation biology, and ecological niche modeling is a & Schneider 2010). Moreover, another important factor is its serviceable means of finding out the potential distributions collection for pet trade (Pasmans et al. 2006, Bogaerts et al. of species (Guisan & Thuiller 2005, Elith et al. 2006). The po- 2012). Unfortunately, the species is still being kidnapped tential distribution modeling performance of N. strauchii is at abroad by foreigners or studies are being conducted without quite good values, and it is determined that its distribution permission. Besides, the salamander species in our country depended mainly on temperature oscillation. The distribu- such as Lissotiton vulgaris, karelinii, and tions of the Syrian Salamandra infraimmaculata and Ommato- ophryticus are illegally sold in pet shops particularly in big triton vittatus are shaped almost entirely by precipitation cities such as İstanbul, Ankara, and İzmir. Another threaten- (Bogaerts et al. 2013). ing factor is the wrong beliefs of the local people due to their During the past glacial periods, European amphibians ignorance such as that the species is venomous and harmful. and reptiles are stuck in Central and Northern Europe, while Thus, these harmless are killed for such reasons as range expansion is observed in the inter-glacial periods that they contaminate and poison the water resource where (Gasc et al. 1997, Araújo et al. 2006). Thus, the effect of the animals are found. Hence, the greatest contribution likely to global climate change on herptiles can occur in two different be made to the sustainability of populations is to raise ways. Some groups enter a process of extinction (e.g. Stuart awareness by carrying out training and informative activi- et al. 2004), whereas the others may expand their distribu- ties for the local people. Our results suggest that Anatolia tion (e.g. Gasc et al. 1997, Araújo et al. 2006). Newt urgently needs an action plan and a long-term moni- Some European amphibians and reptiles expand their toring program for the sustainability of its population in the distribution if they have dispersal potential (Araújo et al. near future. 2006). If the species have low dispersal ability, they will lose their ranges. Araújo et al. (2006) claim that the climatic warming in the cooler northern ranges of Europe will create an opportunity to expand for the colonization of the species Acknowledgments. The distribution map of the species is used with the permission by the IUCN Red List of Threatened Species and that the species inhabiting south-western Europe (in- (http://www.iucnredlist.org/). cluding the Iberian Peninsula) will lose their ranges. It is predicted that especially amphibians will tend to become ex- tinct depending on a decrease in precipitation but an in- crease in temperature (e.g. Pounds et al. 1999, Araújo et al. References

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