Atlas of the amphibians and reptiles of northern Morocco: updated distribution and patterns of habitat selection
Mohamed Mediani1,*, José Carlos Brito2,3, Soumia Fahd1
1 Laboratoire Ecologie, Biodiversité et Environnement, Faculté des Sciences de Tétouan, Université Abdel- malek Essaâdi, MHannech, BP 2121, Tétouan, Morocco. 2 CIBIO/InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos da Universidade do Porto, Campus Agrário de Vairão, R. Padre Armando Quintas, 4485-661 Vairão, Portugal. 3 Departamento de Biologia da Faculdade de Ciências da Universidade do Porto, Rua Campo Alegre, 4169- 007 Porto, Portugal.
*Correspondence: Laboratoire Ecologie, Biodiversité et Environnement, Faculté des Sciences de Tétouan, Université Abdelmalek Essaâdi, MHannech, 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 plo ed 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 species categories were identied 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 identied. 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 pa erns 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 habitats, 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 ndings 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 anbios 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 anbios y reptiles. Observamos 11 anbios y 53 reptiles, incluyendo tres especies de anbios y nueve de reptiles endémicos de Marruecos. Para ambos grupos taxonómicos identica- mos tres tipos de especies en la zona: especies de amplia distribución, especies restringidas a unas
DOI: http://dx.doi.org/10.11160/bah.14009 MEDIANI ET AL.
condiciones ambientales particulares, y especies con áreas de distribución pequeñas y / o frag- mentadas. Para la riquea total de especies identicamos 10 áreas de elevada diversidad, las cua- les fueron comunes a todos los grupos taxonómicos y correspondieron generalmente a ambientes mediterráneos. Los anbios 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 anbios y reptiles presentes en Marruecos. Estos hallagos refueran 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; riquea 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 lhabitat. Les données dobservation recueillies de la bibliographie et lors de prospections herpétologiques réalisées dans le nord du Maroc entre 1989 et 2014, nous ont per- mis dactualiser les cartes de distribution des amphibiens et des reptiles de ce e région en utili- sant un système de grille UTM 5 x 5 km. One amphibiens et 53 reptiles ont été observés, dont trois et neuf endémiques marocains, respectivement. Pour les deux groupes taxonomiques, trois catégories distinctes ont été identiées 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 ones de grande diversité ont été identiées. Ces ones 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 lOriental. La complexité orographique du nord marocain crée apparemment des conditions micro-environnementales pour chaque groupe et est liée à limportante diversité spécique 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 one prioritaire pour la conservation de lherpétofaune au niveau national.
Key words: conservation; herpétofaune; richesse spécique; sélection dhabitat; one prioritaire.
Northern Morocco is located in the a large portion of the terrestrial biodiversi- Mediterranean Basin hotspot, one of 34 ty in the Mediterranean Basin and am- global areas simultaneously gathering phibians and reptiles constitute a major high biodiversity and high levels of threat component of such diversity, especially in (M et al., 2000; M et al., the western Mediterranean and north Afri- 2004). Northern Morocco also concentrates ca (B Gz, 1996; S et al.,
82 AMPHIBIANS AND REPTILES OF NORTHERN MOROCCO
1996; Gz et al., 2004). The region is also and analysing changes in population sie characterised by a high proportion of en- and range, providing framework data for demic species (S et al., 1996; M- survey designs, evaluating habitats occu- z-F 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- (B Gz, 1996). The high richness in tion (e.g. A et al., 2002; Hz 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 (M Qz, 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 Pz et al., 2002; AÓ et al., allow for distinguishing at least three cli- 2002-2003; S et al., 2005; S et al., matic regions: an Atlantic climate a enuat- 2005) and Morocco (e.g. F P- ed by moisture from the ocean in the west- z, 1996, 2001; B A, 2001; ern area, a mountain climate in the main B et al., 2001; E H 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 (S R, 2000). This ge- of Morocco was published in the mid- ographical diversity also allowed the allo- 1990s (B Gz, 1996), and there patric speciation of several species (e.g. have also been some publications focusing B et al., 2002; Fz et al., 2005; on partial regions of the country, such as R et al., 2007). Moreover, phylogenetic the Rifs mountains (F Pz, analyses over the past decade have identi- 1996, 2001) or the southern region (Gz ed a large number of genetic lineages et al., 2004). However, there are still many within Moroccan herpetofauna, sometimes knowledge gaps in distribution pa erns, leading to the description of several new especially in poorly sampled and inacces- species or species complexes (e.g. H sible regions, such as the Algerian- et al., 2003; P et al., 2007; Cz et Moroccan frontier regions and the highest al., 2008; P et al., 2008; F et al., Rif and Atlas Mountains. Furthermore, 2008, 2009; V-AÓ et al., 2012). since the seminal work of B Gz 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 pa erns of species geographical (e.g. W, 2001; Cz et al., 2004, ranges and changes in their distribution in 2006, 2008; G-P et al., 2012; M- space and time (S et al., 2005). These 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. B, 2005; of species and determining the geography H et al., 2008, 2010; B et al., of population distribution, documenting 2011; P et al., 2012; B et al.,
83 MEDIANI ET AL.
2013). As such, the present work aims to: Tissouka) and 2170 m (Jbel Bouhalla, Jbel 1) revise the taxonomic list of amphibians Lexhab and Jbel Lakraa). Sebou landscape and reptiles present in northern Morocco; is characterised by low altitude and mostly 2) update the knowledge on the spatial at areas. Mountains of Beni Snassen have distribution of amphibians and reptiles in rock formations of limestone and can northern Morocco at the 5 x 5 km UTM reach an altitude of 1530 m. The north of grid scale; 3) identify areas of high am- Morocco is considered very rich and di- phibian and reptile species richness; and 4) verse in vegetation cover (B, 1982; identify preliminary relationships between V et al., 2002; V, 2013). Major species distribution and habitat variability. plant formations are generally of thermo- Ultimately, we expect to provide a frame- Mediterranean type (S, 1961), oc- work basis for the denition of conserva- curring in the Tingitana peninsula, the tion strategies for these two taxonomic western and central Rif, Jbel Taekka, Deb- groups in northern Morocco. dou and Beni Snassen mountains, but have been degraded in some areas and trans- M M formed into croplands and pastures in oth- Study area er places like the Gharb Basin and the east- ern Rif. The study area is located in northern Morocco and covers approximately 53 013 Taxonomic species list km2. It is bordered by the Mediterranean Since the publication of the lists devel- Sea to the north, Algeria to the east, the oped by B (1972), M D Atlantic Ocean to the west, and minimum (1988), B Gz (1996), S et latitude of N 33.389 degrees (datum WGS al. (1996) and Gz et al. (2004), changes in 1984) to the south (Fig. 1). The maximum species status have not ceased to modify altitude is 2548 m at Jbel Taekka. The cli- the list and taxonomy of amphibians and mate is mainly of Mediterranean type and reptiles of Morocco. In this study, we used it is characterised by high levels of precipi- the most updated and most complete taxo- tation and drainage, with an average an- nomic species data. For amphibians, we nual rainfall and soil drainage above 1100 adopted the work of B et al. (2013), mm. The high plains of eastern Morocco except for Bufo spinosus (G-P et exhibit a hot and dry climate. Coastal are- al., 2012; R et al., 2012; Az et as experience moderate rainfall levels and al., 2013) and for the genus Discoglossus temperature is milder in comparison with (V et al., 2014), for which D. scovazzi inland areas that exhibit a continental-type was separated from D. pictus. For reptiles, climate. we took into account the following taxo- Limestone formations are relatively nomical considerations: we used Timon common in northern Tingitana Peninsula tangitanus separated from Timon pater , and east of the central Rif. To the east, the Scelarcis perspicillata and Podarcis vaucheri terrain becomes high and steep, with based on the revision of the phylogeny of climbs reaching elevations of 1700 m (Jbel Eurasian Lacerta by A et al. (2007), Taaout), 1928 m (Jbel Kelti), 2050 m (Jbel discarded Acanthodactylus lineomacula- 84 AMPHIBIANS AND REPTILES OF NORTHERN MOROCCO
Figure 1: Location of the study area, altitudinal variation and identication of the main toponims cited in the text. tus, which was lumped into Acanthodactylus et al. (2006), and used Hemorrhois hippocrepis erythrurus following F et al. (2009), based on N et al. (2004) and Daboia mau- used Agama impalearis after B et al. ritanica following L et al. (2001). (2002), considered Trapelus boehmei Species observations based on W et al. (2011), used Uro- mastyx nigriventris following the genetic anal- Published distributional data were yses of H et al. (2007) and W et al. gathered from the following works: B (2007), considered Stenodactylus mauri- Gz (1996), F Pz tanicus after M et al. (2012) and (1996, 2001), B et al. (2002), D- M C (2013), used Hy- B B (2003), B alosaurus koellikeri based on M et al. (2005), F et al. (2005, 2007), P (2006), (1999), followed for Macroprotodon F M (2007), Gz et al. snakes the works of W (2001) and C- (2007), H et al. (2007, 2008, 2010), z et al. (2004), separating M. cucullatus Cz et al. (2008), F et al. from M. brevis and M. abubakeri, consid- (2008), M et al. (2009), B et ered Malpolon insignitus after Cz al. (2010, 2012), E H H
85 MEDIANI ET AL.
(2010), Sz et al. (2010), B et al. scale published by the French Institut (2011), P et al. (2011a, 2012), Géographique National (IGN). Field obser- D et al. (2011a,b), Ez et al. vations collected after 1996 were georefer- (2011), Gz et al. (2011), G-P enced with a global positioning system et al. (2012), B et al. (2013), D- (GPS) on the WGS 84 coordinate system. M et al. (2014) and V-AÓ et al. Distribution atlas, species richness and (2014). relationships with land cover We also gathered data collected in the eld 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 eld- pling e orts in regions where previous work observations over a 5 x 5 km UTM knowledge about species distribution was grid cell sie (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 B 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 Articial 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
86 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 Chalcides ebneri, Chalcides mauri- distribution, such as Salamandra algira, tanicus, Chalcides parallelus, Psammodromus 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, Chalcides ocellatus, in their distribution areas in Morocco (see Chalcides pseudostriatus, Emys orbicularis, B Gz, 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 gu ulata, T. boehmei, The eld observations georeferenced Lytorhynchus diadema, M. cucullatus and S. with a GPS were intersected with land- dolichospilus; and (4) rare species with less cover categories (B 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 pa erns of habitat selection. Analyses ebneri, C. mauritanicus, C. parallelus and E. were conducted using Spatial Analyst tool jaculus. Concerning the la er group, C. mau- functions (ArcGIS). ritanicus was recorded in two locations, the Moulouya River mouth and Ras El Mae R (WD 5986 and WD 5587, respectively), C. Overall, we identied 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 pa erns, four groups of amphibians and 9993, respectively). reptiles were identied: (1) species with Several pa erns 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-
87 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
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 % 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) 3 (1) 7 (1) 6 42 (4) 42 (4) 43 (6) 45 (0) 55 (4) 25 (3) 22 (1) 11 (6) 13 (6) 20 (5) 40 (2) 11 (0) 11 80 (11) 80 (13) 56 (12) 34 (11) 55 (15) 43 (19) 90 (18) 60 242 (52) 242 (13) 150 (18) 111 (59) 225 (32) 137 (38) 152 (38) 182 (70) 216 N UTM N 3 9 7 N 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 waltl Pleurodeles algira Salamandra maurus* Alytes mauritanicus Amietophrynus spinosus Bufo boulengeri Bufotes pictus D. + scovazzi* Discoglossus meridionalis Hyla varaldii* Pelobates saharicus Pelophylax graeca Testudo orbicularis Emys leprosa Mauremys boskianus Acanthodactylus erythrurus Acanthodactylus maculatus Acanthodactylus impalearis Agama colosii* Chalcides ebneri* Chalcides mauritanicus Chalcides minutus* Chalcides mionecton* Chalcides ocellatus Chalcides parallelus Chalcides polylepis* Chalcides pseudostriatus* Chalcides chamaeleon Chamaeleo algeriensis Eumeces turcicus Hemidactylus koellikeri Hyalosaurus Taxonomic list of amphibians and reptiles observed in northern Morocco. Asterisks (*) indicate endemic species. N obs: number number N obs: species. endemic indicate (*) Asterisks Morocco. northern in observed reptiles and amphibians of list Taxonomic Order / / Order suborder Urodela Anura Chelonia Sauria Table 2: Table occu- area of percentage %: records), news of (number observed was species which in squares km 5 x 5 of number UTM: N observations, of pied, percentageand observationsof in eachland-cover category(see Tablefor 1 land-cover category abbreviations).
88 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) 3 (2) 8 (0) 6 (0) 3 (0) 3 (0) 1 (0) 6 35 (6) 35 (2) 12 (2) 18 (4) 25 (4) 33 (2) 11 (9) 36 (3) 16 (3) 10 (1) 11 (3) 11 (6) 33 (4) 19 44 (15) 44 (15) 51 (13) 59 (18) 62 (14) 44 (10) 59 174 (52) 174 (72) 247 (72) 227 (25) 100 (30) 157 (27) 129 (17) 130 N UTM N 4 8 6 3 3 1 6 N 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 Taxa gu Mesalina olivieri Mesalina occidentalis Ophisops vaucheri Podarcis algirus Psammodromus blanci Psammodromus microdactylus* Psammodromus fasciatus* Saurodactylus mauritanicus Saurodactylus perspicillata Scelarcis mauritanicus Stenodactylus mauritanica Tarentola tangitanus Timon pater Timon boehmei Trapelus nigriventris Uromastyx tingitanus* Blanus wiegmanni Trogonophis girondica Coronella jaculus Eryx mauritanica Daboia hippocrepis Hemorrhois maura Natrix natrix Natrix diadema Lytorhynchus abubakeri Macroprotodon brevis Macroprotodon cucullatus Macroprotodon insignitus Malpolon monspessulanus Malpolon schokari Psammophis dolichospilus Spalerosophis latastei Vipera (cont.). (cont.).
Order / / Order suborder Sauria Amphisbaenia Serpentes Table 2
89 MEDIANI ET AL.
Figure 2: Representation in UTM 5 x 5 km grid of (A) amphibian 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 pa erns 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
90 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 (Melilla and Sidi Ifni; Z, 1909; insignitus and Psammophis schokari. J, 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 (L, 1935) has been considered as located in the western Rif, Tingitana Pen- doubtful (B Gz, 1996). insula, Mamoura Forest (Gharb Basin), Given that sampling e ort was not uni- Jbel Taekka, 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 Taekka, 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 eldwork sampling e orts 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- pa erns exhibited by the distribution of ed according to our eld observations and reptiles richness (Fig. 2c). literature. Some old observations were re- evaluated and in some cases they were D 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 B Gz, 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 (Y R relative surface of the study area (about C Hz, 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 (F Pz, 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 (B Gz, 1996; Beukema et gave veracity to the observation of P. waltl al., 2013) and reptiles (B Gz, 1996; at Talamagaït (M, 1991), despite our F Pz, 1996, 2001). All am- intense sampling in eastern Rif and in this phibians and reptiles of northern Morocco locality failed to nd the species. Howev- were included in this study with the ex- er, there are some local guides conrming 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 specic status of P. waltl
91 MEDIANI ET AL. in this area. which can be a ributed to increased sam- In comparison with the previous atlas- pling e orts in recent years by both pro- es of distribution of amphibians and rep- fessional and amateur herpetologists (e.g. tiles in Morocco (B Gz, 1996; P, 2006; Gz et al., 2007; H et F Pz, 1996, 2001; B al., 2008, 2010; B et al., 2010, 2012; et al., 2013), new observations were record- B et al., 2011; D et al., 2011a). ed outside the known distribution area for During our eld expeditions in north- one amphibian and three reptile species. ern Morocco, contact ones 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 di ers from its congener D. pic- (western Rif) by F M (2007). tus by the absence of tympanum (F et This species had been considered absent al., 2004; Mz-S et al., 2004; from this region by previous works Z et al., 2006; P et al., 2012). (D et al., 2011b; B 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 la er species garding reptiles, C. pseudostriatus was occurs on the eastern side of Moulouya observed (May 2002) in a wetland of the River (B et al., 2013; V 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 (Gz pictus. This species was also found along the S, 1994). This species was recorded in Mediterranean Coast west of Moulouya southern Debdou (VC9758, D- River, in the cities of Nador and Melilla, M et al., 2014), also outside its previ- suggesting that the potential barrier to the ously known distribution range. These distribution of these frogs corresponds to two observations merit more a ention in the wide and arid river valley and not to future genetic analyses, because the identi- the river itself (V et al., 2014). During cation of these two specimens was based our eld 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 V et al. (2014). tions extended signicantly 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 (W, work also contributed to extend the 2001; Cz et al., 2004). During our known ranges of P. varaldii and N. natrix, eld expeditions in the Trois Fourches
92 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) a ributed to M. ty in contact ones 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 ones is highly probable (W, palearis, C. ocellatus, H. hippocrepis, M. mon- 2001; Cz 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 di culties 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 conrm order to be er understand the habitat se- their presence in the region. The liards lection pa erns 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 (S, 1982; A, 1983, B genus Malpolon (M. insignitus and M. mon- Gz, 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 (L, 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 we est environments of the highlands of the phylogenetic study of Cz et al. Debdou and Meseta-Oran, as shown by (2006), and most citations of this species ecological modelling ( P et al., 2013). are found in the valley of Moulouya, at the To clarify the status of these species in eastern high plateau (B Gz, 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. gu ulata and ered at Saïdia (Gz et al., 2006) suggest- H. koellikeri, no new records were made, sug- ing the possibility of hybridiation be- gesting also that further sampling is need-
93 MEDIANI ET AL. ed in particular areas of northern Morocco. cies according to their habitat selection The majority of new data collected in pa erns: 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 pa erns 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 rst 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 one of Morocco the previously known range of the species. (E, 1962; B, 1982, 2000) and Concerning pa erns of habitat selec- support also rich and diversied forest tion, the main results are supported by communities, including Abies marocana, previous works on the subject (e.g. B Cedrus atlantica, Quercus suber, Quercus ilex, Gz, 1996; R et al., 1997; F P- Quercus canariensis and Quercus fructicosa z, 2001). All amphibians appar- (V 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- di erent 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 a ni- 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 (S 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 (F Pz, 1996; Real et obvious and direct e ects 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 ( P et al., 2011b; B 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 Lu e Con-
94 AMPHIBIANS AND REPTILES OF NORTHERN MOROCCO tre la Désertication (HCEFLCD) for all provincia de Ciudad Real (Castilla-La Man- permits and assistance in the eldworks cha, España). Zoologica Baetica 13/14: 155- during all years. Part of this study was 202. B, M.; P, A.; H, D.J.; V D funded by Convention cooperative M, A.; Cz, S.; C, F.; CNRST / FCT (GRICES. Portugal), 889- G-MÑz, E.; Gç, D.; H- 08/09. José Carlos Brito is supported by a , S.; J, F.; M, J.C.; P, FCT contract (IF/00459/2013). Study sup- L. S, P. (2011). New observations of ported by project Biodiversity pa erns 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 B, J.A.M.; Gzz V, J.P.; and Manuel Orti-Santaliestra as well as Jz-Cz, F. G-B, V. (2010). Contribución al atlas de la herpeto- two anonymous reviewers for their help- fauna de Marruecos. Boletín de la Asocia- ful comments that improved the manu- ción Herpetológica Española 21: 76-82. script. B, J.A.M.; D-B, D.; R Gzz V, J.P.; VÓ, A. E M, E.H. (2012). Contribución al A, R.P.; GÓz-L, M. P- conocimiento de la herpetofauna de Ma- , A.T. (2002). Geographical distributions rruecos: Nuevos datos corológicos (octubre of spiny pocket mice in South America: 2003). Butlletí de la Societat Catalana dHer- insights from predictive models. Global petologia 20: 57-71. Ecology and Biogeography 11: 131-141. B, B. A, P.H. (2001). Distribution du A, E.N. (1983). Osteology, genitalia and genre Prosimulium Roubaud (Diptera, Si- the relationships of Acanthodactylus muliidae) dans le Rif (Nord du Maroc). (Reptilia: Lacertidae). Bulletin of the British Zoologica Baetica 12 : 119-134. Museum of Natural History (Zoology) 44: 291- B, A. (1982). Etudes Phytoécologique, Bio- 339. géographique et Dynamique des Associations et A, E.N.; A, O. Cz, S. Séries Sylvatiques du Rif Occidental (Maroc): (2007). Systematics of the Palaearctic and Problèmes Posés par la Reforestation et lAmé- Oriental liard tribe Lacertini (Squamata: nagement des Peuplements Forestiers Actuels. Lacertidae: Lacertinae), with descriptions of Ph.D. Dissertation, Université Paul Cé- eight new genera. Zootaxa 1430: 1-86. anne, Aix-en-Provence - Marseille, France. Az, J.W.; MA, J.; R, E.; Z- B, A. (2000). Flore et Écosystèmes du Ma- , J.M.; O, A.; A, J. roc. Evaluation et Préservation de la Biodiversi- Mz-S, I. (2013). Morphological té. Ibis Press, Paris, France. and genetic di erentiation of Bufo toads: B, N.; Sz-C, C.E. O, 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- AÓ, E.; B, P.; C, F.; F, ca Baetica 12: 135-168. L.; G, A.J.; Gz, R.U.; H- B, W.; P, P.; D-B, z, J.M.; M, M.; T, C. Z- D.; B, S.; G-P, J.; E- , F. (2002-2003). Atlas provisional de z, D.; A, O.J.; E M, E.H. distribución de los anbios y reptiles de la Cz, 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- W, P.; M, J.; W, T.M. ogische Beiträge 56: 55-99. Sz, A. (2011). Opening a box of cryptic Y R, R. C Hz, J.M. (1986). taxa the rst review of the North African Guía de la Naturaleza de la Región de Melilla. desert liards in the Trapelus mutabilis Ayuntamiento de Melilla, Melilla, Spain. Merrem, 1820 complex (Squamata: Z, F.; C, R. N, 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. loymes and mitochondrial markers: evolu- W, T.M.; BÖ, W.; W, P.; Lz- tionary and taxonomic inferences , N. Sz, 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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A 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 eld observations.
Pleurodeles waltl Salamandra algira
Discoglossus scovazzi Alytes maurus Discoglossus pictus
Amietophrynus mauritanicus Bufo spinosus
Bufotes boulengeri Hyla meridionalis
102 AMPHIBIANS AND REPTILES OF NORTHERN MOROCCO
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
107