Distribution and Environmental Suitability of the Smallscaled Rock Agama, Paralaudakia microlepis (Sauria: Agamidae) in the Iranian Plateau

Natalia B. ANANJEVA, Evgeny A. GOLYNSKY, Seyyed Saeed HOSSEINIAN YOUSEFKHANI, and Rafaqat MASROOR

1Department of Herpetology, Zoological Institute, Russian Academy of Sciences 199034, St. Petersburg, Russia

2Department of Biology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, Iran

3Zoological Sciences Division, Pakistan Museum of Natural History, Garden Avenue, Shakarparian, Islamabad 44000, Pakistan

Distribution and Environmental Suitability of the Smallscaled Rock Agama, Paralaudakia microlepis (Sauria: Agamidae) in the Iranian Plateau

Natalia B. ANANJEVA1*, Evgeny A. GOLYNSKY1, Seyyed Saeed HOSSEINIAN YOUSEFKHANI2, and Rafaqat MASROOR3

1Department of Herpetology, Zoological Institute, Russian Academy of Sciences 199034, St. Petersburg, Russia

2Department of Biology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, Iran

3Zoological Sciences Division, Pakistan Museum of Natural History, Garden Avenue, Shakarparian, Islamabad 44000, Pakistan

Predictive potential distribution modeling is of increasing importance in modern herpetological studies and determination of environmental and conservation priorities. In this article we provided results of analysis and forecasts of the potential distribution of smallscaled rock agama Paralaudakia microlepis (Blanford, 1874) using the distribution models through Maxent (www.cs.princeton.edu/ ～ schapire / maxent). We made an attempt for comparison of input of bioclimatic factors and characteristics of biotope distribution for three species of genus Paralaudakia. constructed model identified dissemination of Paralaudakia microlepis enough performance (AUc = 0.972 with dispersion 0.003). According to the map constructed, the most suitable habitats of smallscaled rock agama Paralaudakia microlepis are located in southern and eastern Iran, the west of central Pakistan and southeastern Afghanistan.

Iranian Plateau, Agamidae, Potential species distribution modeling, Paralaudakia microlepis, Maxent modeling

1. Introduction

Species distribution modeling is a powerful tool to investigate important biological questions. It can allow predicting of lost biodiversity, identify areas with highest risk of biological invasions and thereby its conservation and identification of suitable areas for threatened species (Thuiller et al., 2005; Ficetola et al., 2010; Reshetnikov and Ficetola, 2011; Bernardes et al., 2013). Predictive potential distribution modeling is of increasing importance in modern herpetologicalstudies and determination of environmental priorities (Litvinchuk et al., 2010; Doronin, 2012; Bernardes et al., 2013; Ananjeva and Golynsky, 2013; Ficetola et al., 2013; Hosseinian Yousefkhani et al., 2013). It was shown that bioclimatic models are useful in predicting amphibians and reptile’s distribution due to their ectothermy (Buckley et al., 2012).

Using Maxent as the modeling technique and Asian rock agamas (genus Paralaudakia Baig, Wagner, Ananjeva and Böhme, 2012) as a model system we construct a bioclimatic model for the poorly known narrow spread species Paralaudakia microlepis (Blanford, 1874) and made an attempt to compare input of bioclimatic factors to distribution of different species (P. caucasia, P. lehmanni, P. microlepis) (Ananjeva and Golynsky, 2013; Hosseinian Yousefkhani et al., 2013).

We expect to provide an additional estimation of these agamas ecological niche, which can be used to predict its potential geographical distribution.

Recently, Baig et al. (2012) revision recognized within the genus Laudakia three genera: Laudakia Gray, 1845; Stellagama Baig, Wagner, Ananjeva and Böhme, 2012; and Paralaudakia Baig, Wagner, Ananjeva and Böhme, 2012. The latter is an agamid genus inhabiting the mountain rock landscapes. Its distribution ranges from Greece and the Nile River delta on the west, through the Middle East and central Asia, to Gobi Altai on the northeast and Brahmaputra River on the east (Ananjeva and Tuniyev, 1994; Rastegar-Pouyani and Nilson, 2002; Ananjeva et al., 2006). P. microlepis is poorly studied species of Asian rock agamids of P. caucasia complex with limited distribution within the Iranian Plateau (Anderson, 1968). We gathered all available data on the distribution of P. microlepis to describe its distribution range and use MAXENT model to identify suitable habitats in Iran, Afghanistan and Pakistan; its range was never been mapped and analyzed. The results of model will be of value for understanding of the biogeography of Asian rock agamas and determination of their conservation status.

In this study, we use maximum entropy modeling to study the distribution of Paralaudakia microlepis in the Middle East based on geographic distributional data and environmental predictor variables, with the following objectives: 1) to determine which environmental factors are correlated with the distribution of this species and another earlier studied species of this genus and 2) to compare potential areas by applying models based on those factors of rock agamas of the genus Paralaudakia.

2. Materials and Methods

We combined literature records, localities data on museum specimens from Iran, Afghanistan and Pakistan stored in Sabzevar University Herpetological collection (SUHc), california Academy of Sciences (cAS), Pakistan Museum of Natural History (PMNH), Zoological Institute, Russian Academy of Sciences (ZISP), Zoological Museum, Moscow State University (ZMMGU), and data of the field surveys of authors and colleagues to describe the distribution of Paralaudakia microlepis through its entire range. We also used all the available literature records in Iran and Pakistan (Anderson, 1999; Macey et al., 1998, 2000; Nazarov, Melnikov, pers. communications). The data (Table 1) were used to prepare a new updated distribution map for P. microlepis, and served as baseline to build a correlative species distribution model identifying the most suitable areas.

Maximum Entropy modeling (MAXENT) was used to assess the potential distribution of Paralaudakia microlepis in the Middle East and to made an attempt of comparison of characteristics of biotope distribution of three species of rock agamas of Paralaudakia (Ananjeva and Golynsky, 2013; Hosseinian Yousefkhani et al., 2013). In the present work the records from 33 localities in Iran, Pakistan and Afghanistan were analyzed.

Maximum Entropy modeling (MAXENT) was used to assess the potential distribution of Paralaudakia microlepis in the Iranian Plateau. MAXENT combines distribution data with environmental factors and assesses the probability of presence of one species in a given cell on the basis of environmental features in that cell. This method is considered as one of the most important in modern herpetological studies and determination of environmental priorities. The model was fitted using linear, quadratic and hinge features.

We used data from 19 bioclimatic variables (Bio 1–19), the parameters obtained from the Worldclim database (http://www.worldclim.org/ current) and cliMond database (www.climond.org) with resolution of geospatial layers 10 acrsec, as well as the geographic coordinates of 33 known locations records collected in different periods. We considered seven bioclimatic variables that are normally expected to be important for metabolism and thermoregulation of reptiles, as well as their water availability. These variables included: 1) precipitation of warmest quarter (mm); 2) precipitation of coldest quarter (mm); 3) highest weekly radiation (W m²); 4) temperature seasonality (c of V); 5) precipitation of driest week (mm); 6) radiation of driest quarter (W m²); and 7) mean diurnal temperature range (mean.period max-min) (ºc). We follow some author’s conclusions and did not include altitude because it is strongly correlated to temperature (Harris et al., 2013; Hosseinian Yousefkhani et al., 2013). In the model, we used accessibility (Nelson, 2008; Uchida and Nelson, 2010) as a measure of sampling bias and a logistic output, with MAXENT suitability ranging from zero (no suitability) to one (maximum suitability).

3. Results

We obtained records of Paralaudakia microlepis from 33 localities in the Iranian Plateau (Figure 1, Table 2). The distribution of P. microlepis includes the region in the southern, central and eastern parts of the Iranian Plateau within the territory of Iran; in the mountain regions of

southwestern Afghanistan and in Balochistan Province, northwestern Pakistan. The constructed MAXENT model described precisely the distribution data as the average AUc for test data was 0.972 demonstrating very good performance (with dispersion 0.003).

Figure 1 Potential distribution modeling of Paralaudakia microlepis within the Iranian Plateau. Different colors in the map indicate different suitability values. White: 55%–37% suitability; Light-gray: 72%–55% suitability; Dark-gray: 100%–72% suitability. The distribution range of Paralaudakia caucasia is shown by white line.

Table 1 Bioclimatic variables used in Maxent modeling.

Summer and winter precipitation as well as the highest weekly radiation were the variables with the highest contribution to the model (Table 3). The model indicated that central and eastern regions of Zagros Mountains within territories of Fars, Kerman and western Isfahan provinces in Iran as well as in southern Khorasan Province are the most suitable regions for P. microlepis in Iran. The model also showed fragmented distribution range for this species; another cluster of the most suitable regions of P. microlepis is revealed in the bordering mountain areas of Afghanistan and Pakistan. According to the predictive map, more northern regions of Iran, Afghanistan and adjacent regions of Turkmenistan and Tajikistan are unsuitable for P. microlepis (Figure 1). The variables with highest values include: 1) precipitation of warmest quarter (mm); 2) precipitation of coldest quarter (mm); 3) highest weekly radiation (W m²); 4) temperature seasonality (c of V); 5) precipitation of driest week (mm); 6) radiation of driest quarter (W m²); 7) mean diurnal temperature range (mean.period max-min) (ºc) (Table 3).

4. Discussion

Paralaudakia microlepis was one of the most poorly studied species of Paralaudakia genus in the past. Itwas described in 1874 by Blanford from southern Iran, north of Shiraz. The model results confirm the known distribution pattern of this species. According to the model the suitability is highest in central and eastern regions of Zagros Mountains within territories of Fars and Kerman provinces as well as in southern Khorasan Province in Iran and in the bordering mountain area of Afghanistan and Pakistan. Thus the distribution of P. microlepis in Iran is practically limited by the mountains of the Iranian Plateau. Most of the northern mountains of Iran and the area between Iran and Afghanistan seem to be unsuitable for P. microlepis. The model however identified potentially suitable regions outside the known range of P. microlepis in the north-west of Iran and much expanded distribution range within Afghanistan where only one reliable record is registered before.

Table 2 All coordinate data for Paralaudakia microlepis for its entire distribution used in this study.

Table 3 Relative importance of variables included in the best model.

According to Anderson (1968, 1999) the habitat of this species is similar to that of P. caucasia but niche differences between them are still not determined. Anderson was the first who considered the problem of sympatry of mountain rock agamids in Iran. The map of potential distribution of both related species P. microlepis and P. caucasia with zones of sympatry in the north of Iran was constructed on the base of MAXENT model in this paper. It confirmed that within the Iranian Plateau

P. microlepis extends across its entire northern border to Afghanistan. P. microlepis distribution range overlaps with that of P. caucasia except in the mountains of northern extremes of its range (Anderson, 1968). The potential suitable region of sympatry is shown in the Figure 1.

We made an attempt to apply models based on those factors for several species of Asian rock agamas of genus Paralaudakia (P. caucasia, P. microlepis, P. lehmanni) for estimation of bioclimatic variables role in their distribution (Table 4). The water availability is shown as one of the most important variable for all three studied species of the genus Paralaudakia (Table 4). Winter precipitation is the variable with the highest contribution to the model for P. caucasia and P. lehmanni as they showed the highest average percent contribution; this variable has a second high value for P. microlepis. The water availability is associated with relative aridity which is of value for speciation trends of these Palearctic agamid lizards (Ananjeva and Tuniyev, 1994). We can also suppose the influence of the water availability to vegetation and its association to partial phytophagous mode of feeding. In general, the highest contribution to distribution modeling of all three studied species of genus Paralaudakia make the precipitation of warmest quarter, precipitation of coldest quarter, maximum temperature and solar radiation. The variables of lower contribution to distribution modeling are different in these species: radiation of driest quarter and mean diurnal temperature range for P. microlepis and P. lehmanni; minimum temperature for P. caucasia having more northern distribution.

For both species of P. caucasia-complex the relative importance of winter and summer precipitation is high as well as solar radiation. Temperature factors are also significant for these thermophilous rock agamas: for P. caucasia - maximal and minimal temperatures and for P. microlepis - temperature seasonality.

Data obtained are valuable in the light of consideration about phylogenetic relations of these both species. Baig (1992) has extended the range of P. microlepis by including some localities in western and several places together with P. caucasia, and south-western Turkmenistan. This conclusion was based on the statement (Baig, 1992; Baig et al., 2012) that populations from Turkmenistan described as P. caucasia triannulata (Ananjeva et Atayev, 1984) should be included in P. microlepis. We must remind however that study of phylogenetic relationships within the Paralaudakia caucasia species group on the Iranian Plateau (Macey et al., 1998, 2000) not only recognized P. microlepis and P. caucasia as different evolutionary lines but also placed P. c. triannulata within P. c. caucasia and demonstrated that only four nucleotide substitutions occur between P. c. triannulata (caspian Sea floodplain) and the nearest P. c. caucasia population (Temen Spring in the western Kopet-

Dagh). Thus MAXENT data (Figure 1) show that there is a narrow zone of range’s overlapping in the north of Iran. The problem of sympatry of related species from the same complex of Paraludakia is correlated with ideas on hybridization and hybridogeneous origin of some forms of mountain agamas. Panov et al. (1987) expressed interesting hypothesis for hybridogeneous origin of the western group of populations of P. caucasia in Turkmenistan. They supposed that this area may be considered as the zone of secondary intergradation and some populations are a product of secondary contact between P. caucasia and P. microlepis because they exhibit hybrid characteristics. Two hypotheses are discussed in this context: a) these populations are a result of L. caucasia and L. c. triannulata hybridization, or b) these populations and also “triannulata” form are a result of hybridization of L. caucasia and L. microlepis. The future nuclear genome molecular study of these agamas will allow clarifying if triannulata populations are of hybridogeneous origin or not. The data on distribution of both species show a real and potential zone of secondary intergradation of L. caucasia and L. microlepis.

Table 4 Relative importance of variables used in Maxent model for 3 species of Paralaudakia genus.

AcknowledgementsThe study was partially supported by grants from the Russian Foundation for Basic Research to NBA (Project 12-04-00057) and the Scientific School Support Program (NSh- 2990.2014). NBA and EAG are deeply thankful to Gentile Francesco FIcETOLA, Igor DORONIN, Roman NAZAROV and Daniel MELNIKOV for valuable help in preparation of earlier version of this manuscript.

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*corresponding author: Prof. Natalia B. ANANJEVA, from the Zoological Institute, Russian Academy of Sciences, with her research mainly focusing on taxonomy, phylogeny and biogeography of widely distributed Eurasian amphibians and reptiles.

E-mail: natalia.ananjeva@zin.ru

Received: 5 July 2014 Accepted: 9 September 2014