CITE THIS ARTICLE AS “IN PRESS” Basic and Applied Herpetology 00 (0000) 00-00

Atlas of the and of northern : updated distribution and patterns of selection

Mohamed Mediani1,*, José Carlos Brito2,3, Soumia Fahd1

1 Laboratoire “Ecologie, Biodiversité et Environnement”, Faculté des Sciences de Tétouan, Université Abdel- malek Essaâdi, Tétouan, Morocco. 2 CIBIO/InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos da Universidade do Porto, Vairão, Portugal. 3 Departamento de Biologia da Faculdade de Ciências da Universidade do Porto, Porto, Portugal.

*Correspondence: Laboratoire “Ecologie, Biodiversité et Environnement”, Faculté des Sciences de Tétouan, Université Abdelmalek Essaâdi, M’Hannech, BP 2121, Tétouan, Morocco. Phone: +212672126805, E-mail: [email protected]

Received: 27 October 2014; returned for review: 3 December 2014; accepted: 21 July 2015.

Observational data collected from bibliography and during herpetological surveys in northern Morocco between 1989 and 2014 were plotted to generate updated distribution maps of amphibi- ans and reptiles using a UTM 5 x 5 km grid system. Eleven amphibians and 53 reptiles were ob- served, including three amphibians and nine reptiles endemic to Morocco. In both taxonomic groups, three distinct categories were identified in the area: widely distributed species, species restricted to particular environmental characteristics, and species with small and / or frag- mented distributions. For total species richness, 10 areas of high diversity were identified. These areas were common to all taxonomic groups and correspond roughly to Mediterranean-type habi- tats. Amphibians constitute a relatively homogeneous group according to their habitat selection patterns while reptiles can be grouped in three assemblages: 1) generalist species with broad distri- butions in northern Morocco; 2) species occupying Mediterranean environments, generally abun- dant in the north-western region; and 3) species that occupy arid , frequently found in the eastern region. The topographic complexity of northern Morocco apparently creates micro- environmental conditions for each group and is related to high levels of species diversity ob- served: 78% and 52% of the total number of amphibians and reptiles of Morocco, respectively. These findings strengthen the status of northern Morocco as a priority area for herpetofauna con- servation at the national level.

Key words: conservation; habitat selection; herpetofauna; priority area; species richness.

Atlas de los anfibios y reptiles del norte de Marruecos: actualización de la distribución y los patrones de selección de hábitat. Recopilamos datos observaciones obtenidos tanto de la litera- tura como de muestreos herpetológicos realizados en el norte de Marruecos entre 1989 y 2014 para generar mapas de distribución actualizados, empleando una cuadrícula UTM de 5 x 5 km, de las especies de anfibios y reptiles. Observamos 11 anfibios y 53 reptiles, incluyendo tres especies de anfibios y nueve de reptiles endémicos de Marruecos. Para ambos grupos taxonómicos identifica- mos tres tipos de especies en la zona: especies de amplia distribución, especies restringidas a unas condiciones ambientales particulares, y especies con áreas de distribución pequeñas y / o fragmen-

DOI: http://dx.doi.org/10.11160/bah.14009 MEDIANI ET AL. tadas. Para la riqueza total de especies identificamos 10 áreas de elevada diversidad, las cuales fueron comunes a todos los grupos taxonómicos y correspondieron generalmente a ambientes mediterráneos. Los anfibios constituyen un grupo homogéneo de acuerdo a la selección de su hábitat, mientras que los reptiles se pueden agrupar en tres tipos: 1) especies generalistas de am- plia distribución en Marruecos; 2) especies presentes en ambientes mediterráneos, generalmente abundantes en la región noroccidental; y 3) especies que ocupan ambientes áridos y que aparecen frecuentemente en la región oriental. La compleja topografía del norte de Marruecos parece crear condiciones micro-ambientales para cada grupo y está en relación con la elevada diversidad ob- servada, que abarca respectivamente el 78% y el 52% del número total de especies de anfibios y reptiles presentes en Marruecos. Estos hallazgos refuerzan la importancia del norte de Marruecos como un área prioritaria para la conservación de la herpetofauna a nivel nacional.

Key words: áreas prioritarias; conservación; herpetofauna; riqueza de especies; selección de hábi- tat.

Atlas des amphibiens et reptiles du nord du Maroc: actualisation de la distribution et les pa- trons de sélection de l’habitat. Les données d’observation recueillies de la bibliographie et lors de prospections herpétologiques réalisées dans le nord du Maroc entre 1989 et 2014, nous ont per- mis d’actualiser les cartes de distribution des amphibiens et des reptiles de cette région en utili- sant un système de grille UTM 5 x 5 km. Onze amphibiens et 53 reptiles ont été observés, dont trois et neuf endémiques marocains, respectivement. Pour les deux groupes taxonomiques, trois catégories distinctes ont été identifiées dans la région: les espèces largement répandues, les es- pèces inféodées à des caractéristiques environnementales particulières et celles à distribution ré- duite et / ou fragmentées. Concernant la richesse en espèces, 10 zones de grande diversité ont été identifiées. Ces zones sont communes à tous les groupes taxonomiques et correspondent en géné- ral aux habitats de type méditerranéen. Selon leurs modèles de sélection des habitats, les amphi- biens forment un groupe relativement homogène, tandis que les reptiles forment trois groupes distincts: 1) les espèces généralistes, présentant une ample répartition au nord du Maroc; 2) les espèces occupant les milieux méditerranéens; généralement abondantes dans les régions du nord- ouest, et 3) les espèces qui occupant les habitats arides, fréquents dans l’Oriental. La complexité orographique du nord marocain crée apparemment des conditions micro-environnementales pour chaque groupe et est liée à l’importante diversité spécifique observée: 78% et 52% du nombre total des amphibiens et des reptiles du Maroc, respectivement. Ces résultats renforcent le statut du nord du Maroc en tant que zone prioritaire pour la conservation de l’herpétofaune au niveau national.

Key words: conservation; herpétofaune; richesse spécifique; sélection d’habitat; zone prioritaire.

Northern Morocco is located in the ty in the Mediterranean Basin and am- Mediterranean Basin hotspot, one of 34 phibians and reptiles constitute a major global areas simultaneously gathering component of such diversity, especially in high biodiversity and high levels of threat the western Mediterranean and north Afri- (Myers et al., 2000; Mittermeier et al., ca (Bons Geniez, 1996; Schleich et al., 2004). Northern Morocco also concentrates 1996; Geniez et al., 2004). The region is also a large portion of the terrestrial biodiversi- characterised by a high proportion of en-

PrePrint 2 AMPHIBIANS AND REPTILES OF NORTHERN MOROCCO demic species (Schleich et al., 1996; Mar- survey designs, evaluating habitats occu- tínez-Freiría et al., 2013) and by the pres- pied by species and communities, and for ence of relict elements of Palearctic fauna ecological modelling of species distribu- (Bons Geniez, 1996). The high richness in tion (e.g. Anderson et al., 2002; Hirzel et northern Morocco has been associated al., 2002). The most frequently used system in with the presence of Rif and Atlas Moun- biodiversity distribution atlases in the tains, which divide the country into sever- Western Mediterranean is based on the al bioclimatic regions of Mediterranean UTM (Universal Transverse Mercator) co- type (Médail Quézel, 1999), character- ordinate system, and it has been used in ised by hot and dry summers and cold and many cases in the Iberian Peninsula (e.g. wet winters. The prevailing conditions Pleguezuelos et al., 2002; AyllÓn et al., allow for distinguishing at least three cli- 2002-2003; Sillero et al., 2005; Soares et al., matic regions: an Atlantic climate attenuat- 2005) and Morocco (e.g. Fahd Plegue- ed by moisture from the ocean in the west- zuelos, 1996, 2001; Belqat Adler, 2001; ern area, a mountain climate in the main Bennas et al., 2001; El Haissoufi et al., summits, and a continental climate, more 2010). or less arid, inland and in the Oriental re- A distribution atlas of the herpetofauna gion (Sobrino Raissouni, 2000). This ge- of Morocco was published in the mid- ographical diversity also allowed the allo- 1990s (Bons Geniez, 1996), and there patric speciation of several species (e.g. have also been some publications focusing Brown et al., 2002; Fritz et al., 2005; on partial regions of the country, such as Recuero et al., 2007). Moreover, phylogenetic the Rif’s mountains (Fahd Pleguezuelos, analyses over the past decade have identi- 1996, 2001) or the southern region (Geniez fied a large number of genetic lineages et al., 2004). However, there are still many within Moroccan herpetofauna, sometimes knowledge gaps in distribution patterns, leading to the description of several new especially in poorly sampled and inacces- species or species complexes (e.g. Harris sible regions, such as the Algerian- et al., 2003; Perera et al., 2007; Carranza et Moroccan frontier regions and the highest al., 2008; Pinho et al., 2008; Fonseca et al., Rif and Atlas Mountains. Furthermore, 2008, 2009; Velo-AntÓn et al., 2012). since the seminal work of Bons Geniez Atlases of species distribution are es- (1996), there have been profound changes sential sources of data to evaluate large- in the taxonomic status of multiple species scale patterns of species geographical (e.g. Wade, 2001; Carranza et al., 2004, ranges and changes in their distribution in 2006, 2008; Garcia-Porta et al., 2012; Met- space and time (Sillero et al., 2005). These allinou et al., 2012) and many works have atlases can also be used, among other sub- collected additional distribution data for jects, for clarifying the spatial distribution several species (e.g. in den Bosch, 2005; of species and determining the geography Harris et al., 2008, 2010; Barata et al., of population distribution, documenting 2011; de Pous et al., 2012; Beukema et al., and analysing changes in population size 2013). As such, the present work aims to: and range, providing framework data for 1) revise the taxonomic list of amphibians

PrePrint 3 MEDIANI ET AL. and reptiles present in northern Morocco; Lexhab and Jbel Lakraa). Sebou landscape 2) update the knowledge on the spatial is characterised by low altitude and mostly distribution of amphibians and reptiles in flat areas. Mountains of Beni Snassen have northern Morocco at the 5 x 5 km UTM rock formations of limestone and can grid scale; 3) identify areas of high am- reach an altitude of 1530 m. The north of phibian and species richness; and 4) Morocco is considered very rich and di- identify preliminary relationships between verse in vegetation cover (Benabid, 1982; species distribution and habitat variability. Valdés et al., 2002; Valdés, 2013). Major Ultimately, we expect to provide a frame- plant formations are generally of thermo- work basis for the definition of conserva- Mediterranean type (Sauvage, 1961), oc- tion strategies for these two taxonomic curring in the Tingitana peninsula, the groups in northern Morocco. western and central Rif, Jbel Tazekka, Deb- dou and Beni Snassen mountains, but have Materials and Methods been degraded in some areas and trans- formed into croplands and pastures in oth- Study area er places like the Gharb Basin and the east- The study area is located in northern ern Rif. Morocco and covers approximately 53 013 Taxonomic species list km2. It is bordered by the Mediterranean Sea to the north, Algeria to the east, the Since the publication of the lists devel- Atlantic Ocean to the west, and minimum oped by Bons (1972), Mellado Dakki latitude of N 33.389 degrees (datum WGS (1988), Bons Geniez (1996), Schleich et 1984) to the south (Fig. 1). The maximum al. (1996) and Geniez et al. (2004), changes in altitude is 2548 m at Jbel Tazekka. The cli- species status have not ceased to modify mate is mainly of Mediterranean type and the list and of amphibians and it is characterised by high levels of precipi- reptiles of Morocco. In this study, we used tation and drainage, with an average an- the most updated and most complete taxo- nual rainfall and soil drainage above 1100 nomic species data. For amphibians, we mm. The high plains of eastern Morocco adopted the work of Beukema et al. (2013), exhibit a hot and dry climate. Coastal are- except for Bufo spinosus (Garcia-Porta et as experience moderate rainfall levels and al., 2012; Recuero et al., 2012; Arntzen et temperature is milder in comparison with al., 2013) and for the inland areas that exhibit a continental-type (Vences et al., 2014), for which D. scovazzi climate. was separated from D. pictus. For reptiles, Limestone formations are relatively we took into account the following taxo- common in northern Tingitana Peninsula nomical considerations: we used Timon and east of the central Rif. To the east, the tangitanus ‒separated from Timon pater‒, terrain becomes high and steep, with Scelarcis perspicillata and Podarcis vaucheri climbs reaching elevations of 1700 m (Jbel based on the revision of the phylogeny of Tazaout), 1928 m (Jbel Kelti), 2050 m (Jbel Eurasian Lacerta by Arnold et al. (2007), Tissouka) and 2170 m (Jbel Bouhalla, Jbel discarded Acanthodactylus lineomacula-

PrePrint 4 AMPHIBIANS AND REPTILES OF NORTHERN MOROCCO

Figure 1: Location of the study area, altitudinal variation and identification of the main toponims cited in the text. tus, which was lumped into Acanthodactylus et al. (2006), and used Hemorrhois hippocrepis erythrurus following Fonseca et al. (2009), based on Nagy et al. (2004) and Daboia mau- used Agama impalearis after Brown et al. ritanica following Lenk et al. (2001). (2002), considered Trapelus boehmei Species observations based on Wagner et al. (2011), used Uro- mastyx nigriventris following the genetic anal- Published distributional data were yses of Harris et al. (2007) and Wilms et al. gathered from the following works: Bons (2007), considered Stenod actylus mauri- Geniez (1996), Fahd Pleguezuelos tanicus after Metallinou et al. (2012) and (1996, 2001), Brown et al. (2002), Donaire- Metallinou Crochet (2013), used Hy- Barosso Bogaerts (2003), in den Bosch alosaurus koellikeri based on Macey et al. (2005), Fahd et al. (2005, 2007), Pieh (2006), (1999), followed for Macroprotodon Fahd Mediani (2007), Guzmán et al. the works of Wade (2001) and Car- (2007), Harris et al. (2007, 2008, 2010), ranza et al. (2004), separating M. cucullatus Carranza et al. (2008), Fonseca et al. from M. brevis and M. abubakeri, consid- (2008), Mediani et al. (2009), Barnestein et ered Malpolon insignitus after Carranza al. (2010, 2012), El Hamoumi Himmi

PrePrint 5 MEDIANI ET AL.

(2010), Stoetzel et al. (2010), Barata et al. scale published by the French Institut (2011), de Pous et al. (2011a, 2012), Géographique National (IGN). Field obser- Donaire et al. (2011a,b), Escoriza et al. vations collected after 1996 were georefer- (2011), Geniez et al. (2011), Garcia-Porta enced with a global positioning system et al. (2012), Beukema et al. (2013), Damas- (GPS) on the WGS 84 coordinate system. Moreira et al. (2014) and Velo-AntÓn et al. Distribution atlas, species richness and (2014). relationships with land‐cover We also gathered data collected in the field since 1989 (amphibians), 1996 For each species present in our study (saurians and amphisbaenians) or 2001 area, distribution maps were produced (snakes) until 2014. Sampling was not uni- representing all published observations in form across the study area; we focus sam- the earlier documents and our new field- pling efforts in regions where previous work observations over a 5 x 5 km UTM knowledge about species distribution was grid cell size (3088 cells in total). Distribu- rather limited. Sampling was conducted tion maps combined species for which the monthly during the whole year and the distribution limits are not yet clear number of persons varied in each station (Discoglossus spp., Macroprotodon spp. and from two to six. The geographic coordi- Malpolon spp.), or species of the same genus nates of observations collected before 1996 for which the number of citations was low were gathered from maps with a 1:50 000 (Saurodactylus spp.). For rare species (≤ 13

Table 1: Land-cover categories and their availability in the study area, including number of pixels (N) and percentage (%) of occurrence (adapted from Bicheron et al., 2008).

Land-cover category Code N % Rain-fed croplands CROP 6690 7.12 Rain-fed shrub or tree crops SHRU 11 0.01 Mosaic of cropland (50-70%) and vegetation (20-50%) CRVG 20084 21.437 Mosaic of vegetation (50-70%) and cropland (20-50%) VGCR 21179 22.53 Closed (> 40%) broad-leaved deciduous forest (> 5 m) BRFO 658 0.7 Closed (> 40%) needle-leaved evergreen forest NEFO 379 0.4 Mosaic forest or shrub land / grassland FOSH 3689 3.93 Closed to open (> 15%) shrub land (< 5 m) BNSH 5875 6.325 Closed to open (> 15%) broad-leaved deciduous shrub land (< 5 m) BRSH 2470 2.63 Sparse (< 15%) vegetation VEGE 7304 7.877 Sparse (< 15%) grassland GRAS 7416 7.89 Artificial surfaces and associated areas (> 50%) URBA 628 0.67 Bare areas BARE 9396 10 Consolidated bare areas CONS 7744 8.24 Water bodies WATE 464 0.549

PrePrint 6 AMPHIBIANS AND REPTILES OF NORTHERN MOROCCO observations) in the study area and also in Tarentola mauritanica, Natrix maura, H. hip- Morocco, we provide the coordinates in 1 pocrepis and Malpolon monspessulanus; (2) x 1 km, whenever possible. These species species with limited and / or fragmented include ebneri, Chalcides mauri- distribution, such as Salam and ra algira, tanicus, Chalcides parallelus, Alytes maurus, B. spinosus, Bufotes bouleng- microdactylus, Psammodromus blanci, Ophi- eri, Pelobates varaldii, Pleurodeles waltl, sops occidentalis, T. pater and Eryx jaculus. Acanthodactylus boskianus, Acanthodactylus We exclude from this list those species maculatus, Blanus tingitanus, Chalcides considered rare in our study but abundant colosii, Chalcides minutus, , in their distribution areas in Morocco (see Chalcides pseudostriatus, Emys orbicularis, Bons Geniez, 1996). Maps were pro- Mesalina olivieri, P. blanci, S. fasciatus, duced using the Geographical Information Saurodactylus mauritanicus, S. perspicillata, System ArcGIS 10.0 (ESRI, Redlands, Cali- Stenodactylus mauritanicus, Trogonophis fornia, USA). wiegmanni, Spalerosophis dolichospilus, Na- Three types of synthetic maps (i.e. rich- trix natrix and D. mauritanica; (3) species that ness of amphibians, richness of reptiles may be considered rare in northern Mo- and total species richness) were generated rocco, but apparently common throughout by adding individual 5 x 5 km presence their distribution areas in Morocco, such observations of species using Spatial Ana- as Chalcides mionecton, Chalcides polylepis, lyst (ArcGIS). H. koellikeri, Mesalina guttulata, T. boehmei, The field observations georeferenced Lytorhynchus diadema, M. cucullatus and S. with a GPS were intersected with land- dolichospilus; and (4) rare species with less cover categories (Bicheron et al., 2008; 250 than 13 observations, such as P. microdac- m resolution; Table 1) to quantify prelimi- tylus, P. blanci, T. pater, O. occidentalis, C. nary patterns of habitat selection. Analyses ebneri, C. mauritanicus, C. parallelus and E. were conducted using Spatial Analyst tool jaculus. Concerning the latter group, C. mau- functions (ArcGIS). ritanicus was recorded in two locations, the Moulouya River mouth and Ras El Mae Results (WD 5986 and WD 5587, respectively), C. Overall, we identified and mapped dis- parallelus was observed in six new locations in tributions of 11 species of amphibians the Oriental Region (WD 5587, WD 2386, (1515 observations) and 53 of reptiles (3573 WD 1196, WD 1187, WD 2384 and WD observations) in the study area (Table 2, 7256), and both P. blanci and O. occiden- Appendix 1). talis were recorded in two new locations (WC Regarding species distribution 9993 and WD 9502, and WC 3665 and WC patterns, four groups of amphibians and 9993, respectively). reptiles were identified: (1) species with Several patterns of habitat selection widespread distribution, such as Amiet- were observed in the herpetofauna of ophrynus mauritanicus, D. scovazzi, P. sahari- northern Morocco (Table 2). All amphibi- cus, A. erythrurus, A. impalearis, Mauremys ans, Testudines and Scincidae were fre- leprosa, P. vaucheri, Psammodromus algirus, quently linked to mosaics with combina-

PrePrint 7 MEDIANI ET AL.

1.3 1.2 1.2 0.7 3.3 0.7 0.5 6.7 4.7 3.2 16.7 Wate

a occu- a

0.4 5.4 2.4 2.0 5.0 6.5 10.0 16.7 13.6 12.1 Cons

4.8 1.3 2.7 0.8 2.9 3.2 4.6 4.1 5.3 5.0 4.6 2.3 3.2 33.3 31.3 16.7 16.7 11.1 Bare

4 1.7 2.4 3.6 3.3 1.8 5.3 2.0 1.3 1.0 3.3 3.0 4.7 3.2 10.8 16.7 22.2 20.0 Urba

0.9 1.6 1.2 1.8 6.4 1.4 3.3 6.9 4.6 4.7 9.7 10.8 13.3 25.0 22.7 Gras

10 4.9 2.7 0.8 4.8 1.8 2.1 5.4 6.0 8.3 3.3 4.6 6.7 7.0 10.9 11.1 13.6 25.0 16.1 Vege

4 3.5 2.7 2.7 3.6 1.8 3.2 2.0 3.3 3.0 6.7 1.5 Brsh

2.7 9.5 5.0 9.1 8.2 3.3 9.1 3.0 9.3 3.2 12.1 16.7 12.0 24.4 20.2 17.7 11.7 15.2 10.9 10.0 11.1 20.0 11.1 25.0 Bnsh

4 9.5 1.7 1.7 3.6 2.4 1.8 3.2 4.8 3.3 3.3 4.2 3.5 6.7 4.6 4.6 6.7 7.0 11.1 Fosh

6.9 5.0 1.3 2.4 2.7 0.8 2.3 0.6 0.7 1.5 3.3 Nefo

3.2 4.6 2.0 1.0 6.7 5.17 1.67 2.22 12.2 4.03 4.76 0.59 16.7 Brfo

2.1 33.3 44.8 50.0 35.6 36.6 21.6 35.5 35.7 25.0 35.3 21.3 54.6 32.0 13.3 31.3 26.2 40.0 16.7 22.7 11.1 18.2 33.3 50.0 20.0 25.6 16.1 44.4 50.0 Vgcr

19 8.3 100 47.6 21.7 22.2 17.1 21.6 24.2 21.4 30.0 21.2 23.4 22.7 31.3 10.0 23.2 17.3 23.3 16.7 13.6 22.2 18.2 16.7 25.0 20.9 22.6 22.2 12.5 Crvg

2.33 Shru

4.8 5.2 3.3 7.6 4.9 1.6 9.4 4.6 5.4 5.3 4.2 7.4 3.3 4.6 4.6 16.2 11.9 36.7 17.0 33.3 11.1 16.7 13.3 11.6 16.1 11.1 12.5 Crop tegory (see Table 1 for land-cover category abbreviations). category abbreviations). land-cover 1 for (see Table tegory

% 1.5 2.8 1.5 8.5 1.6 2.1 5.4 3.9 2.0 8.0 4.9 0.9 5.5 1.2 5.6 2.0 7.7 1.5 0.1 0.3 0.8 0.4 3.1 0.5 0.2 0.7 2.2 1.4 0.4 0.4

3 (0) 7 (1) 6 (1) 42 (4) 43 (4) 45 (6) 55 (0) 25 (4) 22 (3) 11 (1) 13 (6) 20 (6) 40 (5) 11 (2) 11 (0) 80 (11) 56 (13) 34 (12) 55 (11) 43 (15) 90 (19) 60 (18) 242 (52) 150 (13) 111 (18) 225 (59) 137 (32) 152 (38) 182 (38) 216 (70) N UTM

3 9 7 N 46 79 75 56 75 31 54 71 54 24 13 94 13 23 66 41 15 12 110 344 209 127 394 147 230 215 255 obs

Taxa Pleurodeles waltl Salamandra algira Alytes maurus* Amietophrynus mauritanicus Bufo spinosus Bufotes boulengeri scovazzi*Discoglossus + D. pictus Hyla meridionalis Pelobates varaldii* saharicus Pelophylax Testudo graeca Emys orbicularis leprosa Mauremys Acanthodactylus boskianus Acanthodactylus erythrurus Acanthodactylus maculatus Agama impalearis Chalcides colosii* Chalcides ebneri* Chalcides mauritanicus Chalcides minutus* Chalcides mionecton* Chalcides ocellatus Chalcides parallelus Chalcides polylepis* Chalcides pseudostriatus* Chamaeleo chamaeleon Eumeces algeriensis Hemidactylus turcicus koellikeriHyalosaurus Taxonomic list of amphibians and reptiles observed in northern Morocco. Asterisks (*) indicate endemic species. N obs: number number obs: N species. endemic indicate (*) Asterisks Morocco. northern in observed reptiles and amphibians of list Taxonomic

Order / suborder Urodela Anura Chelonia Sauria pied, and percentage of observations in each land-cover ca land-cover in each of observations pied, and percentage Table 2: Table 2: of are percentage %: of news records), (number observed was species in which squares 5 km x of 5 number UTM: N of observations, PrePrint 8 AMPHIBIANS AND REPTILES OF NORTHERN MOROCCO

0.8 1.8 3.0 1.3 2.8 2.6 3.1 1.5 0.9 Wate

1.8 7.7 6.3 2.0 2.6 3.1 2.2 4.8 100 24.0 66.7 14.3 20.0 12.5 36.4 27.3 Cons

0.8 3.0 5.3 1.6 2.6 5.9 1.2 2.7 7.5 25.0 24.0 22.2 14.3 50.0 30.0 43.8 13.9 18.2 18.2 23.8 Bare

2 0.8 0.6 7.7 1.6 2.9 5.6 2.2 4.8 0.9 6.7 20.0 14.3 10.8 Urba

3 8.0 1.6 4.2 2.7 5.6 3.1 4.8 9.1 0.9 28.6 15.2 15.4 18.8 10.0 12.5 27.3 19.1 Gras

5.6 5.4 4.0 1.6 2.9 5.1 3.7 3.6 2.7 8.4 50.0 14.3 12.1 12.5 30.0 21.9 11.1 18.2 14.3 Vege

4.0 4.0 2.4 2.0 1.6 2.9 9.4 2.2 4.8 4.7 15.4 Brsh

20 4.0 7.7 0.3 2.8 9.1 5.4 9.1 9.5 19.1 15.1 30.8 12.1 11.3 12.5 14.7 20.5 18.8 11.1 16.9 10.3 Bnsh

50 4.0 3.6 7.7 6.1 6.3 4.0 4.7 5.1 3.1 5.9 3.6 8.1 9.1 9.1 8.4 4.8 14.3 14.3 Fosh

2.4 3.6 0.7 3.1 5.1 2.4 2.7 18.2 Nefo

5.6 1.8 2.7 2.9 1.2 2.7 1.9 6.7 Brfo

50 29 50 3.1 20.0 11.1 33.3 30.1 20.0 38.5 15.2 38.5 30.7 40.6 32.4 22.2 33.3 34.4 36.3 31.3 45.5 14.3 35.1 46.7 Vgcr

17 4.0 0.3 9.1 9.5 25.0 19.4 22.3 14.3 60.0 21.2 30.8 22.7 26.6 23.5 19.4 20.5 15.6 16.9 18.2 14.3 16.2 21.5 13.3 Crvg

1.2 10.0 Shru

50 2.4 4.2 6.3 8.7 6.3 0.3 6.3 2.6 9.4 8.9 7.2 9.1 9.1 5.6 6.7 12.0 15.2 17.7 16.7 42.9 13.5 14.3 Crop

% 0.1 1.3 0.4 6.1 8.8 0.3 0.2 0.6 1.6 0.9 1.1 7.9 3.7 0.1 0.4 1.3 1.7 2.1 2.2 0.1 1.6 5.7 4.5 0.7 0.4 2.1 0.4 0.4 4.6 1.2 0.2 0.7 0.04

3 (0) 8 (2) 6 (0) 3 (0) 3 (0) 1 (0) 6 (0) 35 (6) 12 (2) 18 (2) 25 (4) 33 (4) 11 (2) 36 (9) 16 (3) 10 (3) 11 (1) 11 (3) 33 (6) 19 (4) 44 (15) 51 (15) 59 (13) 62 (18) 44 (14) 59 (10) 174 (52) 247 (72) 227 (72) 100 (25) 157 (30) 129 (27) 130 (17) N UTM

4 8 6 3 3 1 6 N 34 11 18 65 29 31 12 37 53 64 74 47 21 10 59 12 14 33 24 270 351 291 120 193 143 150 obs

ulata

tt

Taxa Mesalina gu Mesalina olivieri occidentalis Ophisops vaucheri Podarcis Psammodromus algirus Psammodromus blanci Psammodromus microdactylus* Saurodactylus fasciatus* Saurodactylus mauritanicus Scelarcis perspicillata Stenodactylus mauritanicus Tarentola mauritanica Timon tangitanus Timon pater Trapelus boehmei nigriventris Uromastyx Blanus tingitanus* Trogonophis wiegmanni Coronella girondica Eryx jaculus Daboia mauritanica hippocrepis Hemorrhois Natrix maura Natrix natrix diadema Lytorhynchus Macroprotodon abubakeri Macroprotodon brevis Malpolon insignitus Malpolon monspessulanus schokari Psammophis Spalerosophis dolichospilus latasteiVipera

(cont.).

Order / suborder Sauria Amphisbaenia Serpentes Table 2 PrePrint 9 MEDIANI ET AL.

Figure 2: Representation in UTM 5 x 5 km grid of (A) species richness, (B) reptile spe- cies richness, and (C) total species richness in northern Morocco.

tions of vegetation and croplands, where brevis and M. abubakeri. Other species such as some species from the other taxonomic B. boulengeri, P. saharicus, A. erythrurus, A. groups were also frequently found, includ- impalearis, P. vaucheri, P. algirus, T. mauri- ing Chamaeleo chamaeleon, H. koellikeri, tanica, N. maura and M. monspessulanus ex- Eumeces algeriensis, P. microdactylus, S. fasci- hibited relatively general patterns of habi- atus, S. perspicillata, T. tangitanus, T. wieg- tat selection. Finally, there are few species manni, E. jaculus, Coronella girondica, D. associated with desert habitats, including mauritanica, N. natrix, S. dolichospilus, M. A. boskianus, A. maculatus, Saurodactylus

PrePrint 10 AMPHIBIANS AND REPTILES OF NORTHERN MOROCCO mauritanicus, O. occidentalis, P. blanci, U. by several authors as introduced in Moroc- nigriventris, L. diadema, M. cucullatus, M. co ( and Sidi Ifni; de Zulueta, 1909; insignitus and Psammophis schokari. Joleaud, 1934), while the presence of C. Areas of relatively high amphibian spe- cerastes in the plain of Tafrata near Debdou cies richness were highly fragmented and (Laurent, 1935) has been considered as located in the western Rif, Tingitana Pen- doubtful (Bons Geniez, 1996). insula, Mamoura Forest (Gharb Basin), Given that sampling effort was not uni- Jbel Tazekka, along the Atlantic coast, and form along space and time, interpretations in a narrow stripe in the north-east (Fig. of distribution maps of individual species 2a). A large number of reptile species were and species richness should be made with located in the Tingitana Peninsula, west- care. In particular, the frontier areas with ern Rif, Jbel Tazekka, Trois Fourches Cape, Algeria, some mountains of Beni Snassen, the mouth of Moulouya River and Jbel between Taourirt and Touissite and some Chekhar. Other relatively rich areas for oriental Rif mountains were not visited. reptiles are located along the high plains Future fieldwork sampling efforts should of the oriental and central Rif, pre-Rif and concentrate on those areas in order to up- Mamoura Forest (Fig. 2b). The distribution date distribution maps. of total species richness follows the same Species distribution maps were updat- patterns exhibited by the distribution of ed according to our field observations and reptile’s richness (Fig. 2c). literature. Some old observations were re- evaluated and in some cases they were Discussion considered as erroneous and excluded Northern Morocco hosts 11 species of from our study. These observations in- amphibians and 53 species of reptiles. cluded A. maurus in the Tingitana Penin- These 64 species represent 56% of the her- sula (see Bons Geniez, 1996) and three petofauna of Morocco, which is a relative- records of Vipera latastei at Trois Fourches ly high proportion in comparison to the Peninsula and Oued Kert (Yus Ramos relative surface of the study area (about Cabo Hernández, 1986). On the contrary, 7.5% of Morocco). About 31.6% and 34.7% the single observation of E. orbicularis in of the observations of amphibians and rep- the eastern Rif (Fahd Pleguezuelos, tiles, respectively, are new localities, while 1996) was considered in this work because the remaining fractions predominantly there are recent photographic evidences of come from published references for am- the species presence in this region. We also phibians (Bons Geniez, 1996; Beukema et gave veracity to the observation of P. waltl al., 2013) and reptiles (Bons Geniez, 1996; at Talamagaït (Mateo, 1991), despite our Fahd Pleguezuelos, 1996, 2001). All am- intense sampling in eastern Rif and in this phibians and reptiles of northern Morocco locality failed to find the species. Howev- were included in this study with the ex- er, there are some local guides confirming ception of sea turtles and two terrestrial its presence. Further research should be reptiles (Psammodromus hispanicus and conducted throughout the eastern region Cerastes cerastes). The former was considered to determine the specific status of P. waltl

PrePrint 11 MEDIANI ET AL. in this area. which can be attributed to increased sam- In comparison with the previous atlas- pling efforts in recent years by both pro- es of distribution of amphibians and rep- fessional and amateur herpetologists (e.g. tiles in Morocco (Bons Geniez, 1996; Pieh, 2006; Guzmán et al., 2007; Harris et Fahd Pleguezuelos, 1996, 2001; Beukema al., 2008, 2010; Barnestein et al., 2010, 2012; et al., 2013), new observations were record- Barata et al., 2011; Donaire et al., 2011a). ed outside the known distribution area for During our field expeditions in north- one amphibian and three reptile species. ern Morocco, contact zones between The amphibian, B. boulengeri, was record- parapatric Discoglossus species were sam- ed in several localities of the western Rif pled. According to phylogenetic and mor- (UE 0404, TD 9891, UD 1188 and UD 0185), phological reviews of the genus, D. sco- as well as in the watershed of Oued Laou vazzi clearly differs from its congener D. pic- (western Rif) by Fahd Mediani (2007). tus by the absence of tympanum (Fromhage et This species had been considered absent al., 2004; Martínez-Solano et al., 2004; from this region by previous works Zangari et al., 2006; Pabijan et al., 2012). (Donaire et al., 2011b; Beukema et al., The former species has a wide distribu- 2013), probably because of lack of prospec- tion, from the Atlantic Coast to the west of tion in the localities mentioned above. Re- Moulouya Basin, while the latter species garding reptiles, C. pseudostriatus was occurs on the eastern side of Moulouya observed (May 2002) in a wetland of the River (Beukema et al., 2013; Vences et al., Moulouya River (WD 5453), an area prob- 2014). In eastern Morocco, all sampled ably inhabited also by C. minutus, as the populations examined east of the Mou- two species are known to occur in sympat- louya River were clearly assignable to D. ry in the Middle Atlas Mountains (Geniez pictus. This species was also found along the Soto, 1994). This species was recorded in Mediterranean Coast west of Moulouya southern Debdou (VC9758, Damas- River, in the cities of Nador and Melilla, Moreira et al., 2014), also outside its previ- suggesting that the potential barrier to the ously known distribution range. These distribution of these corresponds to two observations merit more attention in the wide and arid river valley and not to future genetic analyses, because the identi- the river itself (Vences et al., 2014). During fication of these two specimens was based our field expeditions, sampling of locali- on morphological analyses only. Finally, S. ties north of the Moulouya Valley was un- perspicillata was recorded at the Beni Snassen able to detect sympatry between D. sco- Mountain in 2010 and 2014 (WD 7256). vazzi and D. pictus, which further supports Taken in combination, these new observa- the genetic revisions of Vences et al. (2014). tions extended significantly the known Three species of Macroprotodon snakes distribution areas of these three species in are known to occur in Morocco (M. abu- northern Morocco. Additionally, the rec- bakeri, M. cucullatus and M. brevis) according ords that we have compiled in the present to the latest revision on the genus (Wade, work also contributed to extend the 2001; Carranza et al., 2004). During our known ranges of P. varaldii and N. natrix, field expeditions in the Trois Fourches

PrePrint 12 AMPHIBIANS AND REPTILES OF NORTHERN MOROCCO

Peninsula, no specimens of M. abubakeri tween these two species. Further detailed were found west of Moulouya Valley. studies on genetic and phenotypic diversi- Nevertheless, Wade (2001) attributed to M. ty in contact zones are needed to under- abubakeri the specimens found in two localities stand population dynamics. west of the Moulouya Valley (Ras El Mae), The distribution maps of many species which shows that the Moulouya River show a trend for more or less contiguous does not act as a geographic barrier for the observations, suggesting that their areas of species. Therefore, the exact distribution distribution are fairly well documented. limits between M. brevis and M. abubakeri These species include A. mauritanicus, P. remain unknown and the occurrence of saharicus, D. scovazzi, A. erythrurus, A. im- contact zones is highly probable (Wade, palearis, C. ocellatus, H. hippocrepis, M. mon- 2001; Carranza et al., 2004). The same prob- spessulanus, M. leprosa, N. maura, P. algirus lem was found with M. cucullatus and M. and T. mauritanica, and particularly those brevis because their distribution limits were species that have been subject of previous apparently not related with geographical detailed studies, such as A. maurus, S. al- barriers. Because of these difficulties in gira, Discoglossus spp., P. varaldii and Macro- determining the limits of their distribution protodon spp.. On the contrary, some species areas, the three species were combined reported previously in northern Morocco, into a single map (Appendix 1). Both eco- such as C. cerastes and P. hispanicus, re- logical and genetic studies are needed in quire more detailed studies to confirm order to better understand the habitat se- their presence in the region. The lection patterns of these species and how Acanthodactylus savignyi, Acanthodactylus genetic diversity is spatially structured. dumerili and P. vaucheri have been document- According to our study, the north- ed in the western regions of Algeria western limit between the snakes of the (Salvador, 1982; Arnold, 1983, Bons genus Malpolon (M. insignitus and M. mon- Geniez, 1996), suggesting their likely pres- spessulanus) is not very clear, but apparently ence in eastern Morocco as well. Recently, the Moulouya Valley might be acting as a A. maurus was recorded in the neighbouring barrier between these two species to the Tlemcen province in Algeria (Loukkas, southeast. Malpolon insignitus, once con- 2006), and its presence suggested in north- sidered a subspecies of M. monspes- eastern Morocco, particularly in the sulanus, was elevated to the rank of species by wettest environments of the highlands of the phylogenetic study of Carranza et al. Debdou and Meseta-Oran, as shown by (2006), and most citations of this species ecological modelling (de Pous et al., 2013). are found in the valley of Moulouya, at the To clarify the status of these species in eastern high plateau (Bons Geniez, north-eastern Morocco, further sampling is 1996). An intermediate form between M. required. For other species, such as C. eb- monspessulanus and M. insignitus, based on neri, E. jaculus, T. pater, S. dolichospilus, P. morphological characteristics, was discov- microdactylus, P. varaldii, M. guttulata and ered at Saïdia (Geniez et al., 2006) suggest- H. koellikeri, no new records were made, sug- ing the possibility of hybridization be- gesting also that further sampling is need-

PrePrint 13 MEDIANI ET AL. ed in particular areas of northern Morocco. cies according to their habitat selection The majority of new data collected in patterns: 1) species occupying the arid re- our study comes from the Tingitana Penin- gions of the eastern plains dominated by sula and western Rif, while the central and bare soil or with some vegetation cover, 2) eastern Rif, the Gharb, the Middle Atlas, generalist species usually exhibiting wide and eastern Morocco (highlands of Deb- distributions across northern Morocco, dou, Beni Snassen Mountain, and regions and 3) species occupying Mediterranean in the border with Algeria) remain poorly environments that are usually abundant in studied. The interpretations of distribution north-western regions. maps should take into account such geo- The distribution patterns of observed graphical sampling bias. Still, important richness of amphibians, reptiles and her- observations were made in those regions. petofauna in general were almost similar. For instance, C. pseudostriatus and S. per- The highest species richness was observed spicillata were recorded for the first time in the along a large area of the central and west- eastern region of northern Morocco, and P. ern Rif. These regions correspond to the waltl was observed in the eastern Rif, far from most humid bioclimatic zone of Morocco the previously known range of the species. (Emberger, 1962; Benabid, 1982, 2000) and Concerning patterns of habitat selec- support also rich and diversified forest tion, the main results are supported by communities, including Abies marocana, previous works on the subject (e.g. Bons Cedrus atlantica, Quercus suber, Quercus ilex, Geniez, 1996; Real et al., 1997; Fahd Ple- Quercus canariensis and Quercus fructicosa guezuelos, 2001). All amphibians appar- (Valdés et al., 2002). For the herpetofauna, ently occur outside the semi-desert areas, these regions tend to harbour species of in habitats with important primary pro- different biogeographical origins, which duction (mosaics of cropland and natural originates a high species richness. These vegetation). These habitats are found species include those of Palaearctic affini- mainly in north-western Morocco, in areas ty, resulting from faunal exchange be- with high levels of precipitation. Eastern tween Africa and Europe during geologi- Morocco is much drier and the majority of cal times (Steininger et al., 1985), and those habitats found in the south-east corre- of sub-Saharan origin which tend to follow spond to bare areas, which results in re- the arid corridor of the Moulouya River duced species richness. One of the most Valley (Fahd Pleguezuelos, 1996; Real et obvious and direct effects of reduced rain- al., 1997). fall on the herpetofauna is the scarcity of The distribution maps presented here breeding sites for amphibians. According constitute framework tools for future es- to our data, croplands would constitute a tablishment of new potential protected breeding habitat for most amphibians in areas or enlargement of the current ones. northern Morocco, which is consistent Acknowledgement with other observations (de Pous et al., 2011b; Beukema et al., 2013). For reptiles, We would like to thank Haut Commis- there are apparently three groups of spe- sariat aux Eaux et Forêts et à la Lutte Con-

PrePrint 14 AMPHIBIANS AND REPTILES OF NORTHERN MOROCCO tre la Désertification (HCEFLCD) for all provincia de Ciudad Real (Castilla-La Man- permits and assistance in the fieldworks cha, España). Zoologica Baetica 13/14: 155- during all years. Part of this study was 202. funded by Convention cooperative Barata, M.; Perera, A.; Harris, D.J.; Van Der Meijden, A.; Carranza, S.; Ceacero, F.; CNRST / FCT (GRICES. Portugal), 889- García-MuÑoz, E.; Gonçalves, D.; Henri- 08/09. José Carlos Brito is supported by a ques, S.; Jorge, F.; Marshall, J.C.; Pedrajas, FCT contract (IF/00459/2013). Study sup- L. Sousa, P. (2011). New observations of ported by project “Biodiversity patterns in amphibians and reptiles in Morocco, with a amphibians and reptiles of North Afri- special emphasis on the eastern region. Her- ca” (Proc. 4.1.5 CNRST/Morocco). We petological Bulletin 116: 4-14. would like to thank the editors Ana Perera Barnestein, J.A.M.; González de la Vega, J.P.; and Manuel Ortiz-Santaliestra as well as Jiménez-Cazalla, F. Gabari-Boa, V. two anonymous reviewers for their help- (2010). Contribución al atlas de la herpeto- fauna de Marruecos. Boletín de la Asocia- ful comments that improved the manu- ción Herpetológica Española 21: 76-82. script. Barnestein, J.A.M.; Donaire-Barroso, D.; References González de la Vega, J.P.; ValdeÓn, A. El Mouden, E.H. (2012). Contribución al Anderson, R.P.; GÓmez-Laverde, M. Peter- conocimiento de la herpetofauna de Ma- son, A.T. (2002). Geographical distributions rruecos: Nuevos datos corológicos (octubre of spiny pocket mice in South America: 2003). Butlletí de la Societat Catalana d’Her- insights from predictive models. Global petologia 20: 57-71. Ecology and Biogeography 11: 131-141. Belqat, B. Adler, P.H. (2001). Distribution du Arnold, E.N. (1983). Osteology, genitalia and genre Prosimulium Roubaud (Diptera, Si- the relationships of Acanthodactylus muliidae) dans le Rif (Nord du Maroc). (Reptilia: ). Bulletin of the British Zoologica Baetica 12 : 119-134. Museum of Natural History () 44: 291- Benabid, A. (1982). Etudes Phytoécologique, Bio- 339. géographique et Dynamique des Associations et Arnold, E.N.; Arribas, O. Carranza, S. Séries Sylvatiques du Rif Occidental (Maroc): (2007). Systematics of the Palaearctic and Problèmes Posés par la Reforestation et l’Amé- Oriental tribe Lacertini (: nagement des Peuplements Forestiers Actuels. Lacertidae: Lacertinae), with descriptions of Ph.D. Dissertation, Université Paul Cé- eight new genera. Zootaxa 1430: 1-86. zanne, Aix-en-Provence - Marseille, France. Arntzen, J.W.; McAtear, J.; Recuero, E.; Zier- Benabid, A. (2000). Flore et Écosystèmes du Ma- mann, J.M.; Ohler, A.; van Alphen, J. roc. Evaluation et Préservation de la Biodiversi- Martínez-Solano, I. (2013). Morphological té. Ibis Press, Paris, France. and genetic differentiation of Bufo toads: Bennas, N.; Sáinz-Cantero, C.E. Ouarour, two cryptic species in Western Europe A. (2001). Nouvelles données sur les coléop- (Anura, Bufonidae). Contributions to Zoolo- tères aquatiques du Maroc: les Hydraenidae gy 82: 147-169. Mulsant, 1844 (Coleoptera) du Rif. Zoologi- AyllÓn, E.; Bustamante, P.; Cabrera, F.; Flox, ca Baetica 12: 135-168. L.; Galindo, A.J.; Gosálvez, R.U.; Hernán- Beukema, W.; de Pous, P.; Donaire-Barroso, dez, J.M.; Morales, M.; Torralvo, C. Za- D.; Bogaerts, S.; Garcia-Porta, J.; Escori- mora, F. (2002-2003). Atlas provisional de za, D.; Arribas, O.J.; El Mouden, E.H. distribución de los anfibios y reptiles de la Carranza, S. (2013). Review of the system-

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Colubridae) in Algeria with a description of mastyx Merrem, 1820 (Reptilia: Squamata: a new species. Bulletin of the Natural Histo- Agamidae: Uromastycinae) – Resurrection ry Museum, Zoology Series 67: 85-107. of the genus Saara Gray, 1845. Bonner Zool- Wagner, P.; Melville, J.; Wilms, T.M. ogische Beiträge 56: 55-99. Schmitz, A. (2011). Opening a box of cryptic Yus Ramos, R. Cabo Hernández, J.M. (1986). taxa – the first review of the North African Guía de la Naturaleza de la Región de Melilla. desert lizards in the Trapelus mutabilis Ayuntamiento de Melilla, Melilla, Spain. Merrem, 1820 complex (Squamata: Zangari, F.; Cimmaruta, R. Nascetti, G. Agamidae) with descriptions of new taxa. (2006). Genetic relationships of the western Zoological Journal of the Linnean Society 163: Mediterranean painted frogs based on al- 884-912. lozymes and mitochondrial markers: evolu- Wilms, T.M.; BÖhme, W.; Wagner, P.; Lutz- tionary and taxonomic inferences mann, N. Schmitz, A. (2007). On the phy- (Amphibia, Anura, Discoglossidae). Biolog- logeny and taxonomy of the genus Uro- ical Journal of the Linnean Society 87: 515-536.

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Appendix 1

Distribution maps of the amphibian and reptiles species in northern Morocco. Solid black marks represent records from bibliographical sources. Grey marks with a central dot represent records from our own field observations.

Pleurodeles waltl Salamandra algira

Discoglossus scovazzi Alytes maurus

Amietophrynus mauritanicus Bufo spinosus

Bufotes boulengeri Hyla meridionalis

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Pelobates varaldii Pelophylax saharicus

Testudo graeca Emys orbicularis

Mauremys leprosa Tarentola mauritanica

Hemidactylus turcicus Stenodactylus mauritanicus

Saurodactylus fasciatus Saurodactyluls mauritanicus Chamaeleo chamaeleon

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Agama impalearis Trapelus boehmei

Timon tangitanus Uromastyx nigriventris Timon pater

Scelarcis perspicillata Podarcis vaucheri

Psammodromus algirus Psammodromus blanci

Psammodromus microdactylus Ophisops occidentalis

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Mesalina olivieri Mesalina guttulata

Acanthodactylus erythrurus Acanthodactylus maculatus

Acanthodactylus boskianus Chalcides ocellatus

Chalcides colosii Chalcides ebneri

Chalcides parallelus Chalcides polylepis

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Chalcides mionecton Chalcides pseudostriatus

Chalcides minutus Chalcides mauritanicus

Eumeces algeriensis Hyalosaurus koellikeri

Blanus tingitanus Trogonophis wiegmanni

Eryx jaculus Hemorrhois hippocrepis

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Spalerosophis dolichospilus Coronella girondica

Macroprotodon brevis Macroprotodon abubakeri Lytorhynchus diadema Macroprotodon cucullatus

Natrix natrix Natrix maura

Malpolon monspessulanus Malpolon insignitus Psammophis schokari

Vipera latastei Daboia mauritanica

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