Journal of Arid Environments xxx (xxxx) xxx–xxx

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Journal of Arid Environments

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Patterns of alpha diversity among Tunisian ()

∗ Daniel Escorizaa,b, a Institut Català de la Salut, Gran Via de les Corts Catalanes, 587−589, 08007, Barcelona, Spain b Laboratory of Ecology, Biodiversity and Environment, University Abdelmalek Essaâdi, Avenue Khenifra, 93000, Tétouan,

ARTICLE INFO ABSTRACT

Keywords: are a successful group in subtropical arid regions. However, little is known about the drivers that Environmental filtering influence the diversity of arid communities. One approach is to investigate the variation in phylogenetic Lizards structure of the communities along a broad environmental gradient. In this study, I investigated these patterns in Phylogenetic clustering the communities of lacertids at the periphery of the Sahara Desert in Tunisia. The effect of the environment was Sahara desert assessed based on a set of variables describing the climate, topography, substrate and cover of perennial ve- getation. The phylogenetic alpha diversity was described using the mean pairwise distance (MPD) and the mean nearest taxon distance (NTD) metrics. The analyses showed that the lacertid could be clustered into three main ecological groups: mesic (Podarcis vaucheri, algirus, Psammodromus blanci, Timon pater), xeric (Acanthodactylus blanci, Acanthodactylus boskianus, Acanthodactylus maculatus, Mesalina olivieri, Ophisops occidentalis), and hyperxeric (Acanthodactylus dumerilii, Acanthodactylus longipes, Acanthodactylus scutellatus, Mesalina guttulata). The analyses also indicated that environment had a weak influence on species richness (15.7% of explained variance), but a strong effect on the phylogenetic (76.5% NTD, 89.5% MPD) structure. The lacertid communities tended to be phylogenetically clustered on sandy substrates under arid climate conditions, and overdispersed under more humid climatic conditions.

1. Introduction et al., 2002). In contrast, under harsh climatic conditions and in habi- tats of low productivity the communities are species-poor, and include Deserts occupy vast areas of the land surface (19.1%; United related taxa that share similar functional traits (Escoriza and Ruhí, Nations Environment Program, 1997). Desert are characterized 2014). by erratic rainfall patterns and low primary productivity, which is Deserts and their peripheral ecoregions are appropriate places to usually limited to one or two annual pulses (Hereford et al., 2006). evaluate hypotheses about the spatial turnover of community structure, These extreme conditions have a negative effect on vertebrate diversity, because they show contrasting gradients in diversity and structure of particularly in those taxa that have high metabolic requirements or are vegetation (Búrquez et al., 1999). In addition, communities in limited by environmental moisture (Lannoo, 2005; Ding et al., 2006). warm deserts tend to be relatively rich (i.e., can include 11–40 sym- Despite this, some groups (including lizards) have diversified in warm patric species), with species separated along gradients of topography, desert regions, and show species-rich communities that are richer than substrate, and vegetation density (e.g., the Gibson/Great Victoria de- those occurring in areas of higher productivity (Morton et al., 2011). serts in Australia, the Sonoran Desert in North America, the Kalahari This suggests that diversity in lizard communities may be subject to Desert in South Africa, and the Sahara Desert in north Africa; Pianka, different drivers than are other vertebrate groups. 1973; Schleich et al., 1996). The spatial patterns of biotic communities can be studied based on In this study I investigated the patterns of alpha diversity among differences in species composition and richness, but also by the phy- lacertid lizard communities on the margin of the Sahara Desert in logenetic affinities of the species involved (Webb et al., 2002). The Tunisia. This region has a narrow humid belt in the north, but the patterns are especially evident when marked environmental contrasts conditions become progressively more arid to the south, and hyperarid also occur, as these imply variations in the productivity and complexity conditions occur in the southern third of the country (Peel et al., 2007). of the habitats (Jetz and Rahbek, 2002). This is the case because het- The arid and hyperarid regions of Tunisia are characterized by high − erogeneous and productive environments show a wide range of mi- interannual fluctuations in rainfall (36–532 mm y 1; Floret et al., − − crohabitats that favour phylogenetically diverse communities (Webb 1982) and low net primary productivity (14–120 g C m 2 y 1), which

∗ Institut Català de la Salut, Gran Via de les Corts Catalanes, 587−589, 08007, Barcelona, Spain. E-mail address: [email protected]. https://doi.org/10.1016/j.jaridenv.2017.11.012 Received 15 March 2017; Received in revised form 8 August 2017; Accepted 21 November 2017 0140-1963/ © 2017 Elsevier Ltd. All rights reserved.

Please cite this article as: Escoriza, D., Journal of Arid Environments (2017), https://doi.org/10.1016/j.jaridenv.2017.11.012 D. Escoriza Journal of Arid Environments xxx (xxxx) xxx–xxx occurs in one cold-season pulse (Floret et al., 1982; Cao and Woodward, 1998). The lacertid communities of the arid regions are relatively species-rich, and are composed of pan-Saharan species belonging to the genera Acanthodactylus and Mesalina (Sindaco and Jeremcenko, 2008). In contrast, the northern area has more stable hydrological conditions − − and higher net primary productivity (230 g C m 2 y 1; Cao and Woodward, 1998). The lacertid communities in this area are species- rich, and there is greater diversity at higher taxonomic levels than oc- curs among desert communities; in this area the lacertid genera include Ophisops, Podarcis, Psammodromus and Timon in addition to Acantho- dactylus and Mesalina (Schleich et al., 1996). Here I examined the effect of the environmental gradient on species identity and lacertid com- munity structure, expecting to find divergent species responses to cli- mate (hypothesis i) and decreasing phylogenetic dispersion in steppes and deserts (hypothesis ii).

2. Methods

2.1. Study area Fig. 2. Canonical Outlying Mean Index ordination plot of Tunisian Lacertidae occurrence sites, with the environmental variables fitted as vectors. Warmer colors of the circles The study region included Tunisia and some adjacent regions of indicate species clusters that occur in arid zones. A, Acanthodactylus;M,Mesalina; O, Algeria, comprising a surface area of 163,610 km2. The climate in the Ophisops;P,Podarcis (P. vaucheri) and Psammodromus (P. algirus/P. blanci); T, Timon. MAT, mean annual temperature (°C); ISO, isothermality; AIN, aridity index; PSE, precipitation northern part of the region is Mediterranean (Csa type, Köppen classi- seasonality; RUG, ruggedness index; SAN, sand (%); CLA, clay (%); FOR, forest (%); BUS, fi cation; Peel et al., 2007). Aridity rapidly increases along a latitudinal bush (%); CUL, cultivated land (%); BAR, barren land (%). (For interpretation of the axis of 790 km, giving rise to subtropical desert conditions (BWh type) references to colour in this figure legend, the reader is referred to the web version of this throughout most of the country (Peel et al., 2007). A total of 13 lacertid article.) species occur in the region, belonging to six genera: Acanthodactylus, Mesalina, Ophisops, Podarcis, Psammodromus and Timon (Schleich et al., were selected because they are known to influence the occurrence of fi 1996). Data were obtained during several eld surveys conducted be- lizards in subtropical regions (Anderson, 1999). The climate was – tween March and May 2012 2016 (Escoriza and Ben Hassine, 2017) characterized using an aridity index (mean annual precipitation/mean and from Nouira (1996), including 271 sites and 489 records (Fig. 1). annual potential evapotranspiration; Trabucco and Zomer, 2009), the mean annual temperature, isothermality (mean diurnal range/tem- 2.2. Geographic information system data perature annual range) and precipitation seasonality. Data for the cli- − matic parameters were obtained at a resolution of 1000 m pixel 1 from The environmental gradient was characterized based on climate, GIS databases (Hijmans et al., 2005; Trabucco and Zomer, 2009). The topography, soil and cover of perennial vegetation variables. These topography was characterized using a ruggedness index that is an evaluation of the average topographic variation among a series of ad- jacent points (Riley et al., 1999). The ruggedness index was calculated − from a digital elevation model having a resolution of 250 m pixel 1 (Jarvis et al., 2008). The soil features were based on a standard depth of − 0–5 cm at 250 m pixel 1 resolution (Hengl et al., 2014), and involved assessment of the sand (grain size = 50–2000 μm) and clay (grain size ≤ 2 μm) content. Vegetation cover was characterized at 1000 m − pixel 1 resolution using four vegetation categories: forest, bush, culti- vated vegetation and barren (Tuanmu and Jetz, 2014). The data were obtained using the package Quantum-GIS vs 2.18 (QGIS Development Team, 2017).

2.3. Community modelling

The alpha diversity was inferred from the modelled ranges of the various species (Peterson et al., 2016). The models were generated by comparing the environmental characteristics of the sites where species were present against a random background matrix (VanDerWal et al., 2009). This involved generation of a series of random points (ap- proximately 10 × n, where n is the number of species occurrences) for distance bands of 100, 200, 300 and 400 km. Bands of shorter or greater distance usually generate less reliable models (VanDerWal et al., 2009). Both datasets (species presence and background data) were classified using Random Forests. This classification method is not based on probabilistic assumptions, and has been shown to be superior to other Fig. 1. Map of Tunisia, showing sampling localities. The aridity gradient, based on an classification algorithms (Hastie et al., 2009). Classification perfor- aridity index, is included. Warm colors indicate higher aridity (0.021; hyperarid) than mance was evaluated based on the classification error rate, which was cold colors (0.574; subhumid). (For interpretation of the references to colour in this figure determined by selecting those bands that showed a rapid decrease in legend, the reader is referred to the web version of this article.) classification error (VanDerWal et al., 2009). Stratified sampling was

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