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Habitat Partitioning and Overlap by Large Lacertid Lizards in Southern Europe

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Habitat Partitioning and Overlap by Large Lacertid Lizards in Southern Europe diversity Article Habitat Partitioning and Overlap by Large Lacertid Lizards in Southern Europe Daniel Escoriza 1,* and Félix Amat 2 1 GRECO, Institute of Aquatic Ecology, Campus Montillivi s/n, University of Girona, 17071 Girona, Spain 2 Area d’Herpetologia, BiBIO, Museu de Granollers–Ciències Naturals, Palaudàries 102, 08402 Catalunya, Spain; [email protected] * Correspondence: [email protected] Abstract: South-western Europe has a rich diversity of lacertid lizards. In this study, we evaluated the occupancy patterns and niche segregation of five species of lacertids, focusing on large-bodied species (i.e., adults having >75 mm snout-vent length) that occur in south-western Europe (Italian to the Iberian Peninsula). We characterized the niches occupied by these species based on climate and vegetation cover properties. We expected some commonality among phylogenetically related species, but also patterns of habitat segregation mitigating competition between ecologically equivalent species. We used multivariate ordination and probabilistic methods to describe the occupancy patterns and evaluated niche evolution through phylogenetic analyses. Our results showed climate niche partitioning, but with a wide overlap in transitional zones, where segregation is maintained by species-specific responses to the vegetation cover. The analyses also showed that phylogenetically related species tend to share large parts of their habitat niches. The occurrence of independent evolutionary lineages contributed to the regional species richness favored by a long history of niche divergence. Citation: Escoriza, D.; Amat, F. Keywords: enhanced vegetation index; Lacerta; Mediterranean; niche partitioning; Sauria; Timon Habitat Partitioning and Overlap by Large Lacertid Lizards in Southern Europe. Diversity 2021, 13, 155. https://doi.org/10.3390/d13040155 1. Introduction Climate is a powerful environmental factor driving the process of niche diversifi- Academic Editor: Francisco cation in reptiles [1,2]. Tolerance to maximum temperatures in reptiles is evolutionarily Javier Zamora-Camacho constrained, possibly because of the importance of external heat sources in maintaining activity and for bodily water balance [3,4]. For these reasons, there is a significant associa- Received: 17 March 2021 tion between the composition of reptile assemblages and thermal latitudinal gradients [5]. Accepted: 2 April 2021 Published: 4 April 2021 However, the thermoregulation efficiency of reptiles is not only mediated by the overall climate conditions, but also by the temperature conditions in microhabitats [6]. Vegetation Publisher’s Note: MDPI stays neutral cover and structure regulate the patterns of reptile occurrence, but at a finer scale than the with regard to jurisdictional claims in climate [7,8]. published maps and institutional affil- South-western Europe encompasses a relatively rich reptile fauna, favored by its iations. topographic heterogeneity, insularity and mild climate conditions [9]. In this region, several groups of phylogenetically related species display complex patterns of overlap structured by environmental gradients or by interspecific interactions [10–12]. In this study we evaluated the niche occupancy patterns of five species of large lacertid lizard (i.e., adults having >75 mm snout-vent length) that occur in south-western Europe and comprise a Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. monophyletic group [13]. We focused on phylogenetically related species because stronger This article is an open access article competitive interactions among them can be expected [14]. The target species in this study distributed under the terms and included one species having a broad circumboreal distribution, Lacerta agilis (Linnaeus conditions of the Creative Commons 1758), two western Mediterranean endemics Lacerta bilineata (Daudin, 1802) and Timon Attribution (CC BY) license (https:// lepidus (Daudin, 1802), and two Iberian endemics Lacerta schreiberi (Bedriaga, 1878) and creativecommons.org/licenses/by/ Timon nevadensis (Buchholz, 1963). Given these substantial chorological differences, it was 4.0/). also expected that these species would diverge in their environmental associations. For Diversity 2021, 13, 155. https://doi.org/10.3390/d13040155 https://www.mdpi.com/journal/diversity Diversity 2021, 13, x FOR PEER REVIEW 2 of 11 Diversity 2021, 13, 155 2 of 11 chorological differences, it was also expected that these species would diverge in their environmentalexample, associations.T. nevadensis For example,mainly occupies T. nevadensis semi-arid mainly steppe-like occupies habitats, semi-aridL. agilis appears steppe-like habitats,to be confined L. agilis toappears sub-alpine to be confined meadows, to andsub-alpine the other meadows, species areand possiblythe other more habitat species are possiblygeneralists more [15 ha,16bitat]. generalists [15,16]. The purposeThe of this purpose study ofwas this to study investig wasate to the investigate patterns theof habitat patterns occupancy of habitat of occupancy of these five speciesthese of five large species lacertids of large and lacertids evaluateand them evaluate from an them evolutionary from an evolutionaryperspective. perspective. We hypothesizedWe hypothesized that the diversity that of the large diversity lacertid of lizards large lacertid in southern lizards Europe in southern would be Europe would favored by nichebe favored partitioning. by niche However, partitioning. this partitioning However, thiswill partitioningbe phylogenetically will be con- phylogenetically strained becauseconstrained related species because tend related to occupy species similar tend to or occupy equivalent similar niches or equivalent [17]. To test niches [17]. To these hypotheses,test these we used hypotheses, multivariate we used ordi multivariatenation and novel ordination probabilistic and novel methods probabilistic that methods enabled quantificationthat enabled of the quantification niche overla ofp thebetween niche overlapspecies, betweenand the niche species, breadth. and the niche breadth. 2. Materials and2. Materials Methods and Methods 2.1. Study Region2.1. Studyand Surveys Region and Surveys The study regionThe studyencompassed region encompassed most of south-western most of south-western Europe including Europe the including Iberian the Iberian Peninsula, southernPeninsula, France southern and the France Italian and Peninsula the Italian (Figure Peninsula 1). The (Figure region1). is The dominated region is dominated by Mediterraneanby Mediterranean climate types, climate ranging types, from ranging subtropical from subtropical warm desert warm to desert humid to humid sub- sub-MediterraneanMediterranean and oceanic, and oceanic,and temperate and temperate to tundra-like to tundra-like types typesin thein mountain the mountain ranges ranges (Pyrenees,(Pyrenees, Alps) Alps)[18]. This [18]. environmen This environmentaltal heterogeneity heterogeneity favors favors the concentration the concentration of high of high bioticbiotic diversity diversity in this in region, this region, including including species species having having xeric Mediterranean xeric Mediterranean and and meso- meso-temperatetemperate affinities affinities [19]. [19]. Figure 1. MapFigure of the 1. studyMap of region the study including region the including distribution the distribu of thetion species of the according species according to the IUCN to the (polygons) IUCN and the surveyed sites(polygons) (circles). The and polygons the surveyed with diagonalsites (circles). stripes The and po dotslygons indicate with diagonal the areas stripes of geographic and dots overlap indicate between two species or threethe species areas of (grid). geographic overlap between two species or three species (grid). Species recordsSpecies were records obtained were opportunisti obtainedcally, opportunistically, based on rand basedom habitat on random surveys habitat surveys conducted inconducted the region in from the regionspring fromto autumn, spring following to autumn, the following annual activity the annual periods. activity periods. The surveys Thewere surveys planned were to capture planned the to maxi capturemum the heterogeneity maximum heterogeneity of habitats within of habitats the within the distribution rangesdistribution of these ranges species, of these but with species, no buta priori with selection no a priori of the selection most suitable of the most suitable habitats (i.e., habitatsa random (i.e., sampling a random of samplingavailable habitats). of available In habitats).total, 823 sites In total, were 823 surveyed sites were surveyed throughout south-westernthroughout south-western Europe by 1–3 Europe observers; by 1–3 each observers; site was each visited site only was once. visited The only once. The occurrence ofoccurrence each species of each was speciesassessed was base assessedd on visual based surveys on visual an surveysd rock andflipping, rock flipping,be- because cause both techniquesboth techniques have been have used been to used build to buildinventories inventories of diurnal of diurnal lizards lizards [20]. [20The]. The surveys surveys werewere conducted conducted on sunny on sunny days daysbetween between 10:00 10:00 a.m. and a.m. 5:00 and p.m. 5:00 local p.m. time. local time.The The visual visual surveyssurveys were complemented were complemented with rock with fl rockipping flipping in cases in caseswhere where identification identification of the of the species species couldcould
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