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 Newt, Neurergus 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: kerim.cicek@hotmail.com / kerim.cicek@ege.edu.tr

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

Abstract. Here, the current and future distributions of Neurergus strauchii was predicted by using the maximum entropy ecological niche modeling. The most important factors which shaped the present distribution of the species 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 The genus Neurergus comprises of four valid species [Neur-ergus strauchii (Steindachner 1887), N. crocatus Cope, 1862, N. kaiseri Schmidt, 1952, and N. microspilotus (Nesterov 1916)] distributed in the Middle East (Anatolia, Iran, and Iraq) (Levinton et al. 1992, Schmidtler 1994, Papenfuss et al. 2009). Anatolia Newt, N. strauchii, is currently known from central Turkey and the western area of Lake Van in eastern Turkey (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, its fragmented distribution, and habitat destruction (Papen-fuss et al. 2009). Neurergus s. strauchii has a wider distribu-tion and is found in the east from River Euphrates up onto the Lake Van area, and subspecies N. s. barani Öz, 1994 is found only in the mountains located in the south-east of Malatya (Pasmans et al. 2006). Anatolia Newt inhabits the small and cool mountain streams and overwinters on land under stones and in burrows (Schmidtler & Schmidtler 1970, Başoğlu et al. 1994).

The analysis of the relationship between species and en-vironment has continually been one of the basic issues of ecology (Guisan & Zimmermann 2000). The prediction of the distributions of species has an essential place in the applica-tions concerning ecology, evolution, and conservation biol-ogy (Elith et al. 2006), and ecological niche modeling is a valid means of determining the potential distributions of species (Guisan & Thuiller 2005, Elith et al. 2006). For the last 20 years, many methods of finding out the distributions of species (e.g. generalized additive models, GARP, BIOCLIM, and MAXENT) are developed, and the most important dif-ference among these methods is the type of data they use (Elith et al. 2010). MAXENT’s predictive performance is con-sistently competitive with the highest performing methods (Elith et al. 2006, Graham & Hijmans 2006, Hijmans & Gra-ham 2006, Elith et al. 2010, 2011), particularly in cases, in which the sample size is low (Elith et al. 2006, Hernandez et al. 2006).

Global declining of amphibians is expressed by many re-searchers (e.g. Alford & Richards 1999, Houlahan et al. 2000,

Stuart et al. 2004, AmphibiaWeb 2015). Climate changes are hypothesized to be one of the most important factors to di-rectly and indirectly trigger this decline (Pounds et al. 1999, Blaustein et al. 2001, Kiesecker et al. 2001, Carey & Alexan-der 2003). This study aims to determine the environmental factors affecting the distribution of Anatolia Newt, Neurergus strauchii, to describe the current ecological niche of the spe-cies and to forecast the potential distribution pattern in the future periods (2050 and 2070). Material and Methods In our fieldwork in 2013, six individuals of Neurergus strauchii at dif-ferent larval stages are detected in one of the tributaries of River Ti-gris in the 163rd km of the Elazığ-Maden highway [Lat: 38.458, long.: 39.623, 1378 m a.s.l.]. Therefore, by thinking that the distribution of the species is not known exactly and that distributional boundaries might be wider, the potential distribution of the species is predicted by using its existing records. There are 36 records of the species (Ba-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-der & Schneider 2010, Coşkun et al. 2013, Koyun et al. 2013). To cor-rect for sampling bias and to reduce spatial autocorrelation (see Gür 2013, Perktaş et al. 2015), 9 of the existing records, which are quite close, are excluded and 27 records are included in model. The local-ity information with no coordinate data is obtained by using Google Earth vers. 7.1.2 (Google Inc.). All records are georeferenced into WGS-84 coordinate system and checked with ArcGIS vers.10.0 (ESRI).

Nineteen climatic variables are obtained from WorldClim ver.1.4 data set (Hijmans et al., 2005, http://www.worldclim.org) at a spa-tial resolution of 30 arc-seconds (approx. 1 km in the equator), which represent monthly temperature and rainfall data as averages of the period 1950–2000. The bioclimatic variables for 2050 (average for 2041-2060) and 2070 (average for 2061-2080) at a spatial resolution of 30 arc-seconds (WorldClim 1.4, http://www.worldclim.org/cmip5_30s), which are projected ac-cording to intermediate emission scenario the representative concen-tration pathways (RCP) 4.5, used for determining future distribution pattern of the species. The RCP 4.5 represents stabilization without overshoot in the amount of global radiative forcing expected by the end of the 21st century stated in the Fifth Assessment Report by the IPCC. The data set of “Hadley Global Environment Model 2 - Earth System”, developed within the scope of the 5th Coupled Model In-

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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-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-old approach as recommended by Liu et al. (2005), and the logistic output is transformed into a map of the presence-absence distribu-tion. Model accuracy is evaluated from area under the receiver-operator curve (AUC), and the averages of all models are imported and visualized with ArcGIS vers.10.0. Results During our fieldwork on November 23, 2013, 6 larvae of Neurergus strauchii at different stages are caught in one of the tributaries nourishing the river in Karataş district of River Tigris (Figs 1a, b). The average total length of the larvae is 50.5 mm (SD = 2.77 mm, range = 43.3 - 59.1 mm). The water temperature in the slowly moving brook where the speci-mens are caught is measured as 10oC and the air tempera-ture as 16oC. Both sides of the streambed in this section are steep, and plants are presented by oriental plane, willow, and poplar, along with shrubs and grass. Since this section of the river is highly sloping, the current is quite fast. Exces-sive deteriorations of the streambeds are seen due to the intercity roadwork in the region. The larvae are kept in an aquarium (L x D x H, 50 x 30 x 20 cm) under captivity condi-tions for a while for photographing, measurement, and ob-servation, and it is observed that a 58.3-mm-long specimen reached a length of 130mm in about 80 days and completed its metamorphosis.

The mean AUC value of the current distribution consen-sus model (Fig. 2) is quite high (0.970). According to the model, the primary factors affecting the distribution of the species are isothermalitly (53.3%) and precipitation of driest month (32.9%). The contributions of the other variables are in the range 0.1 - 4.4%. The distribution model of the species quite resembles its known distributional range. Neurergus strauchii is particularly distributed on the Euphrates Valley and in the west and south of Lake Van (Fig. 2). In the future projected models of the species, it is observed that the suit-able habitats in the distributional range will decrease and

A.)

B.)

Figure 1. A general view of the stream (Elazığ) where the speci-mens are found (a) and three N.strauchii larvae (b).

that there will be a decrease in the western (Malatya) and eastern (Siirt) distributional boundaries in particular (Figs 3, 4). Discussion Anatolia Newt, Neurergus strauchii, is in the vulnerable cate-gory in the IUCN (Papenfuss et al. 2009) red list as it only inhabits the East Anatolian Region (Turkey) and has a nar-row range. According to the coordinate data, the species in-habits mountain waters at altitudes between 946m and 2,695m. It is reported that the water temperature in the breeding period varies between 10oC and 17.3oC (Schmidtler & Schmidtler 1970, Pasmans et al. 2006). Bogaerts et al. (2010) reported that breeding continued even in waters where the water temperature fell as low as 6oC. The breeding period is in April through June. The new locality we de-tected in Elazığ is on the western border of subspecies Neur-ergus s. strauchii (Fig. 1). At the same time, the larvae ob-served in November show that the breeding period also con-tinues after June according to the geographical region. No adult individual is encountered in our sampling. This is probably related to the fact that they made a transition to the terrestrial form in this season. On the other hand, it is ob-served that the larvae could not complete metamorphosis due to unfavorable conditions and would probably overwin-ter in larval form. Fleck (1982) and Pasmans et al. (2006) pre-viously observed overwintering of the N. strauchii larvae. The overwintering behavior in larvae is also observed in other salamander species (e.g. Boone et al. 2004, Kishida & Tezuka 2013).

The prediction of the distributions of species has an im-

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

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

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.

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portant place in the applications about ecology, evolution, and conservation biology, and ecological niche modeling is a serviceable means of finding out the potential distributions of species (Guisan & Thuiller 2005, Elith et al. 2006). The po-tential distribution modeling performance of N. strauchii is at quite good values, and it is determined that its distribution depended mainly on temperature oscillation. The distribu-tions of the Syrian Salamandra infraimmaculata and Ommato-triton vittatus are shaped almost entirely by precipitation (Bogaerts et al. 2013).

During the past glacial periods, European amphibians and reptiles are stuck in Central and Northern Europe, while range expansion is observed in the inter-glacial periods (Gasc et al. 1997, Araújo et al. 2006). Thus, the effect of the global climate change on herptiles can occur in two different ways. Some groups enter a process of extinction (e.g. Stuart et al. 2004), whereas the others may expand their distribu-tion (e.g. Gasc et al. 1997, Araújo et al. 2006).

Some European amphibians and reptiles expand their distribution if they have dispersal potential (Araújo et al. 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 and that the species inhabiting south-western Europe (in-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. 2006). The amphibian breeding phenology is affected largely by environmental cues such as temperature and moisture (Carey & Alexander 2003). Hence, their breeding phenology may be affected directly by global warming (Blaustein et al. 2001, AmphibiaWeb 2015). Pasmans et al. (2006) observed that the streams inhabited by Anatolia newts are slightly al-kaline and indicated that this could result from heavy rain or the prolonged drought period. Bogaerts et al. (2006) stated that the breeding streams of the species are 0.5 to 2 meters wide and fed by melting snow and rain. Therefore, the re-productive behavior of N. strauchii will most probably be af-fected by climate change in future periods.

The aridity index, precipitations of driest month and coldest quarter are strongly shaped to distribution of all Neurergus species (Barabanov & Litvinchuk, 2015). Neurergus strauchii is particularly distributed on the Euphrates Valley and in the west and south of Lake Van in Eastern Anatolia. In our modeling results, the distribution of the species is shaped by temperature and precipitation. The results of the future model scenarios predict that the habitats suitable for the species to inhabit will be lost and that its distribution will particularly tend to narrow from its western and eastern boundaries. It is estimated that the populations of the spe-cies, particularly the population of N.s.barani, will substan-tially be influenced by the global climate change. Moreover, our findings support the hypothesis that salamanders are more defenseless against climate changes (Araújo et al. 2006). The Anatolia newt is stated to be quite sensitive to habitat destruction and disintegration and global climate change (Bogaerts et al. 2012). Especially overgrazing, the contamination of the breeding water depending on domestic wastes, and the cutting of trees are the primary threatening

elements (Bogaerts et al. 2006, Pasmans et al. 2006, Schneider & Schneider 2010). Moreover, another important factor is its collection for pet trade (Pasmans et al. 2006, Bogaerts et al. 2012). Unfortunately, the species is still being kidnapped abroad by foreigners or studies are being conducted without permission. Besides, the salamander species in our country such as Lissotiton vulgaris, Triturus karelinii, and Ommatotriton ophryticus are illegally sold in pet shops particularly in big cities such as İstanbul, Ankara, and İzmir. Another threaten-ing factor is the wrong beliefs of the local people due to their ignorance such as that the species is venomous and harmful. Thus, these harmless animals are killed for such reasons as that they contaminate and poison the water resource where animals are found. Hence, the greatest contribution likely to be made to the sustainability of populations is to raise awareness by carrying out training and informative activi-ties for the local people. Our results suggest that Anatolia Newt urgently needs an action plan and a long-term moni-toring program for the sustainability of its population in the near future. Acknowledgments. The distribution map of the species is used with the permission by the IUCN Red List of Threatened Species (http://www.iucnredlist.org/). References Alford, R.A., Richards, S.J. (1999): Global amphibian declines: A problem in

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