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Herpetology Notes, volume 12: 787-793 (2019) (published online on 25 July 2019)

Reptile diversity of southern : range extensions and the role of the Djebel Ouarkziz as a biogeographical barrier

Daniel Kane1,*, Steve Goodwin1, Gerrit Jan Verspui2, Anniek Tump3, and Gabriel Martínez Del Mármol Marin4

Abstract. The present work provides new records, including range extensions for Ptyodactylus oudrii, Macroprotodon brevis and leucogaster, as well as the first observations of P. oudrii south of the proposed biogeographical barrier formed by the Djebel Ouarkziz mountain range and the westernmost record of Echis leucogaster in Morocco. Data presented herein shows that at least two of thought geographically-limited by this chain of mountains, or previously not known from a particular ecoregion in the country, have ranges encompassing a greater portion of these areas than was formerly known. This new knowledge highlights the importance of faunal surveys in regions where fieldwork is often difficult, as well as the need for further surveys in such environments to help improve knowledge of species’ distributional ranges.

Keywords. Reptilia; ; distribution; ; Oued Drâa;

Introduction diverse community of reptile species due to the meeting of several different ecoregions including Mediterranean Morocco has one of the best-studied herpetofaunal Acacia-Argania dry woodlands and succulent thickets, assemblages of any African country (e.g. Bons and Saharan Atlantic coastal desert and north Saharan xeric Geniez, 1996; Schleich et al., 1996; Geniez et al., steppe and woodland (Bons and Geniez, 1996; Real et 2004; Mediani et al., 2015). Situated in the northwest al., 1997; Geniez et al., 2000; Dinerstein et al., 2017; of the African continent this country presents a wide Martínez-Freiría et al., 2017). variety of ecoregions including Mediterranean High Natural boundaries of terrestrial species’ distributions Atlas juniper steppe, Mediterranean conifer and are frequently marked by geographical barriers to mixed forests, Mediterranean woodlands and forests, dispersal such as impassable water bodies or mountain Mediterranean dry woodlands and steppe, Saharan ranges which cause abrupt changes in habitat or Atlantic coastal desert and north Saharan xeric steppe climatic conditions potentially preferred by one species and woodland (Dinerstein et al., 2017). Within these over another. The Djebel Ouarkziz range, a chain of ecoregions a variety of habitat types including montane mountains up to 770 m high and approximately 300 grasslands, rocky slopes, forests, Macronesian coastal km long running in a WSW-ENE direction between vegetation and inland rocky and sandy desert plains southern Morocco and (Somerville et al., 2013) provide suitable conditions for a variety of to has been hypothesised as a biogeographical barrier for occur. In particular, southern Morocco has an especially certain herpetofaunal elements; separating, for example, species with Mediterranean affinity from those with a North Saharan affinity, as defined by Geniez et al. 2000. The authors of the present work sampled part of the region immediately north and south of the Djebel 1 Zoological Society of London, London Zoo, Regent’s Park, London, United Kingdom, NW14RY. Ouarkziz range and provide further knowledge on the 2 ROC Veiligheidsacademie, Campusplein 16, 3192 CD potential role these mountains have in forming the Hoogvliet, Rotterdam, The Netherlands. distributional limit of several reptile species. 3 Jan van Egmond Lyceum, Hoornselaan 10, 1442 AX Purmerend, The Netherlands. Materials and Methods 4 34, Calle Pedro Antonio de Alarcón, 34, 18002, Granada, Spain. Five sites adjacent to the R103 road between the * Corresponding author. E-mail: [email protected] towns of Assa and Zag were surveyed on foot and by 788 Daniel Kane et al. car, over a period of three days and nights, between 27 Results April and 1 May 2018. A sixth survey site, from further During the course of our surveys we encountered west of our main search area, is also included due to its ten species belonging to six squamate families which potential importance in understanding the distribution warrant reporting and discussion in the present work. of species and threats posed to Moroccan herpetofauna as well as validating previous distribution modelling. A map of these search areas can be seen in Fig. 1A and Fig. 1B. Visual encounter surveys (VES) were Tarentola boehmei Joger, 1984.—Tarentola specimens non-standardised and specific locations which were were identified as belonging to either T. boehmei Joger, expected to harbour the highest diversity of reptiles, 1984 or T. mauritanica (Linnaeus, 1758) at survey site such as rocky features or water storage buildings in two and three. Ceacero et al. (2010) highlighted the an otherwise flat landscape, were chosen to increase difficulties of separating T. boehmei and T. m. pallida the likelihood of encountering the greatest possible in the field based on morphology or colouration and variety of species. VES were undertaken by day and by some of the suggested diagnostic characters including night. Identification of individuals to species level was subdigital lamellae of the 5th toe on the hind foot, the performed in the field and photographs of each species shape of dorsal tubercles, regenerated tail colour and and habitat were taken. translucent/opaque appearance of the skin appear to A species inventory for the region is provided below. overlap between these two species (Geniez et al., 1999; GPS coordinates are provided for all survey sites, Geniez et al., 2004). T. boehmei, being associated with followed by notes on parameters such as altitude, inland pre-Saharan habitats (Geniez et al., 1999) is the habitat, surface temperature as measured by a digital more likely species as T. mauritanica is not known to infra-red non-contact thermometer and activity of the naturally occur in this area and henceforth we refer to species observed. these specimens as T. boehmei. However, with the ability Fig. 1A shows the region of southern Morocco with of T. mauritanica to disperse over wide areas via human main towns indicated and the scale bar represents 70 transport (Harris et al., 2004), and with no molecular km. Fig. 1B shows a closer view of the main study area data available to confirm species identification for our with the Djebel Ouarkziz range visible across the centre specimens, it is possible that the species represented and the scale bar represents 35 km. Across Fig. 1A and could be T. mauritanica. An individual from survey site 1B red place marks numbered one to six are used to 3 is depicted in Fig. 2F. Maximum surface temperatures indicate survey sites. GPS coordinates of survey sites as of around 16 °C were recorded on survey nights in these follows: 1) 28.2374°N, -9.3363°E, altitude 304 m a.s.l.; locations and, due to a persistent strong wind blowing, 2) 28.2840°N, -9.3370°E, 305 m a.s.l.; 3) 28.3910°N, activity was mostly limited to the sheltered cracks -9.3941°E, 285 m a.s.l.; 4) 28.4632°N, -9.3749°E, 240 between rocks. m a.s.l.; 5) 28.5002°N, -9.4600°E, 208 m a.s.l.; 6) Ptyodactylus oudrii Lataste, 1880.—Many individuals 28.3722°N, -10.7208°E, 184 m a.s.l. Images downloaded were seen to be active during each survey night between from Google Earth, 2018. 27 April and 1 May in survey sites two and three. These were observed climbing on rocky surfaces and in cracks between rocks, as is typical for the species. Each night maximum surface temperatures of around 16 °C were recorded at 22:00; however, there was a strong wind blowing and most geckos were observed in more sheltered areas between rocks. Ptyodactylus geckos have distinctive toe morphology with fan-shaped ends to each of their digits, on the underside of which is multiple rows of lamellae. All known species of Ptyodactylus are closely associated with rocky habitats and are reported to have a poor ability to disperse over sandy terrain (Metallinou et al., 2015). With the majority of Ptyodactylus occurring allopatrically (Metallinou et al., Figure 1. Map and survey sites south of Assa, Morocco. 2015) and with vast expanses (~1100 km) of seemingly Reptile diversity of southern Morocco 789 unsuitable sandy areas separating our study areas and during wetter times and was moving through small dry the distribution of other species in the , we are flakes of mud when first seen. Although this species confident in our identification of P. oudrii, it being the has a large range across arid regions of North Africa, only member of its genus reported from Morocco (Perera in Morocco it is known from only a few published and Harris, 2010). However it must be noted that future observations (see Bouazza et al., 2018 for a recent study on the deep genetic divergence between different overview). clades of P. oudrii reported by Metallinou et al. (2015) may lead to the elevation of one or more clades within P. oudrii to species level. Telescopus tripolitanus (Werner, 1909).—On the southern edge of the Djebel Ouarkziz range, at survey Agamidae site three, a single dead-on-the-road (DOR) Telescopus Uromastyx nigriventris Rothschild and Hartert, tripolitanus was found during the day on April 27. 1912.—On the night of 27 April two specimens of U. Identification was based on the specimen having black nigriventris were observed at survey site two, deep head colouration, brown body with multiple darker within rock cracks. By 12 noon the following day circular-shaped vertebral markings and eyes with neither had emerged to bask, despite clear skies vertical pupils. The surrounding habitat on each side of and surface temperatures of 39.0 °C. No evidence of the the road where the was found comprised of rocky occurrence of Uromastyx dispar Heyden, 1827, a species steep-sided cliffs with a few small bushes in the lower hypothesised to have its northern distribution limit as areas. the southern edge of the Djebel Ouarkziz (Geniez et al., Macroprotodon brevis (Günther, 1862).—A single 2000), was found around this location. Fig. 2A shows juvenile Macroprotodon brevis (Fig. 2C) was found the more or less solid yellow dorsal colouration of one active during the night of 28 April 2018 on the ground of our specimens, typical of U. nigriventris, as opposed beneath a large tree at survey site five. Identification to the dark transverse bars present on the dorsal surface was based on presence of black head colouration, eyes of U. d. flavifasciata (Geniez et al., 2004). with circular pupils and a tessellated pattern on the body which no other snake species in this region possesses. Scincidae Maximum surface temperature recorded at this location ° Chalcides boulengeri Anderson, 1892.—A single was between 18 – 20 C. The hard and cracked mud individual encountered beneath the sand by following substrate in this location was covered in a several surface tracks during a nocturnal survey on 27 April at centimetre-deep layer of xerophytic leaf litter which the survey site two. Identification was based on the presence snake retreated into after photographs were taken. of five digits on all toes, distinguishing this species Hemorrhois algirus (Jan, 1863).—On 27 April, on the from the congener C. sphenopsiformis (Duméril, 1856) northern slope of the Djebel Ouarkziz, survey site four, a which possesses one, two or exceptionally no toes on single juvenile DOR H. algirus was found. Identification the front legs and four toes on each hind leg (Geniez et was based on a light brown body colouration with al., 2004). C. boulengeri is typical of inland sandy areas darker transverse bars crossing the dorsal surface and in southern Morocco and is known from 71 km south one supra-labial scale in contact with the eye. Seeing of Aouinet Lahna towards M’sied (Bons and Geniez, this arid-adapted species present in this location is 1996). unsurprising however represents, to the best of our knowledge, the only record from the Djebel Ouarkziz Leptotyphlopidae range. Barata et al. (2011) reported a specimen of H. algirus from around 40 km west of our report. Myriopholis algeriensis (Jacquet, 1896).—A single M. algeriensis was found active on the surface of cracked Spalerosophis dolichospilus (Werner, 1923).—The dry mud with sparse organic debris on the night of 27 most southerly reptile recorded during field work was April 2018 at survey site five. Identification was based S. dolichospilus at survey site one. This snake was on translucent pinkish body colouration, a hook-shaped found DOR during the day. This animal (Fig. 2B), snout and general vermiform appearance. No similar clearly showing rounded dorsal blotches typical of the species are known from the Maghreb. The animal was species, appeared to have been run over by vehicles on the bottom of a channel formed by the flow of water the preceding night. A second DOR S. dolichospilus 790 Daniel Kane et al. was found approximately 5 km north, at survey site our survey effort was relatively low. Species recorded two, on the same day. These records fill an existing in the present work are all known to occur in southern gap in the knowledge of the distribution of this species Morocco, however there are a few notable observations between southern Moroccan and Western Saharan when viewed at a more local scale. The records of P. records, however the relative distributions and any oudrii and T. boehmei are the first reported from south potential contact zone between S. dolichospilus and S. of the Djebel Ouarkziz range in Morocco. These species diadema (Schlegel, 1837) in this region remain poorly were classified as belonging to the ‘North Saharan’ group understood in contrast to the more thoroughly-explored by Bons and Geniez (1996) and Geniez et al. (2000), coastal areas (Geniez et al., 2004). with the hypothesised biogeographical border created by the northern slopes of the Djebel Ouarkziz mountain range believed to constitute their southern-most distribution (Wilms et al., 2009). Our records show that Echis leucogaster Roman, 1972.—An adult male distributional ranges for both species span southwards E. leucogaster Roman, 1972 was seen in an ambush of the Djebel Ouarkziz range, by approximately 30 km position beneath a shrub during the night of 27 April for each species, and therefore these mountains do not at survey site five. Identification was based on several constitute a biogeographical barrier to these species. features including the intense orange iris with vertical There are numerous valleys between these mountains pupil; dorsal colour pattern of whitish transverse with an elevation no greater than 400 m a.s.l. which markings alternating with brown areas of colour on an could be used by these species to disperse north and orange background; immaculate white ventral surface; a south through these mountains. We strongly encourage lack of supraocular horns; and there being no other snake further studies in this area to help determine the range species in Morocco possessing keeled and angled body of these and other reptile species in the region. U. scales used in characteristic well-documented defensive nigriventris has previously been reported from the behaviour in conjunction with these characteristics general vicinity of survey site two (Barata et al., 2011) (Geniez et al., 2004). The substrate at this site was however, prior to this, was thought to be distributed only hardened dry mud with numerous interconnected cracks to the north of the Djebel Ourakziz range. Our findings approximately one to six cm wide and reaching over show the importance of supporting and following up site 20 cm deep. Numerous undulations in the ground had visits to help realise the true number of species living in been formed from a previous flow of water and were often poorly-sampled areas. With reference to relative around 2 m deep when compared to the highest ground distribution of Uromastyx sp. in this region it would height. Trees and shrubs were growing from the higher be interesting to understand where the distribution portion of the ground whereas the bottom of these ranges of U. dispar and U. nigriventris lie. Based on the channels consisted of baked, cracked mud. The ground observations described in the present work we expect temperature in the sheltered position where the snake U. nigriventris to occur in rocky habitats at least as was discovered was 19.5 °C. This record represents a far south as Zag, approx. 37 km south of the locality new location for this species in southern Morocco and reported herein and approximately 70 km further south in a habitat type not yet known to be occupied in this than the previous most southerly records (Geniez et al., region: seasonally-flooded oued lacking stones (Fig. 2004). Zag lies at approximately 28.0000°N, which is 2D). A second individual of this species (Fig. 2E) was the northern limit of the range of U. d. flavifasciata as removed from a water hole during the late afternoon in reported by Wilms et al. (2009). During our relatively the surroundings of Tilemsoune at survey site six on 24 brief period of field work we were not able to validate October 2018. This record is within the high to medium- this statement however, again, further research in this probability of occurrence of the range predicted by region is encouraged. The northwest-most records of U. Brito et al. (2011) however further west than any other dispar are from the Tindouf region in Algeria to the east live specimens of this species reported from Morocco as well as the Saguiat al Hamra in to (Herrmann et al., 2000; Herrmann and Herrmann, 2003; the south (Geniez et al., 2004). There appear to be no Geniez et al., 2004). large geographical barriers to the species’ dispersal from these regions when heading north and east, potentially Discussion up until the mountains around Zag, therefore we expect These records of reptiles for this region of the Djebel that the contact zone of these two species will be Ouarkziz range should be considered preliminary as around this area. Reptile diversity of southern Morocco 791

Figure 2. Photographs of Uromastyx nigriventris (A), Spalerosophis dolichospilus (B), Macroprotodon brevis (C), habitat of Echis leucogaster in Oued Drâa (D), Echis leucogaster (E) and Tarentola boehmei (F).

In recent years, the known distribution of T. locations in Western Sahara include Laâyoune, Tichla tripolitanus around the Drâa valley and associated areas and Guelta Zemmur (Geniez et al., 2000). has increased from the original four localities reported The finding of Macroprotodon brevis 12 km south of by Bons and Geniez in 1996 (see Vesely et al., 1995; Assa, in Oued Drâa, is a first for the area. The previous Robbins and Hearst in Crochet et al., 2008). This new most southerly anecdote of this species was from the record represents, to the best of our knowledge, the first surroundings of Icht; therefore, this record represents record of this species from the Djebel Ouarkziz range a southwestern range extension of approximately 81 which although unsurprising, does fill a gap between km and now represents the most southerly point of current known localities in Morocco and Western Sahara the distribution currently known for this species. It is and lends support to the possibility of a more continuous likely that the more humid microclimate maintained population from Morocco southwards. Currently-known by the Oued Drâa in comparison to the surrounding 792 Daniel Kane et al. desert allows this species of Mediterranean affinity to with that reported by Hermann and Hermann (1999), penetrate further into this region than would otherwise combined with the rapid increase of known locations be possible; a similar phenomenon to that described for for this species in recent years (Koleska et al., 2018), it other species by Geniez et al. (2000). It is likely that seems likely that this species may be found along much M. brevis can be found along much of, if not all, the of the length of the Oued Drâa where it passes through Oued Drâa and therefore the same may also hold true suitable climatic zones (Brito et al., 2011). With future for other reptiles of a more mesic affinity. According field work in this region a greater area of occurrence to molecular analysis individuals from coastal areas than is presently understood in Morocco may well be south of Guelmim appear assignable to M. brevis revealed. brevis (unpublished data, Martínez del Mármol Marin), however individuals from further inland, including Acknowledgements. We are grateful to Fernando Martínez- Ouarzazate and Icht, are awaiting further study to Freíra for providing a pre peer-review letter and helpful determine the genetic relationship to other populations comments on an earlier version of this manuscript. We are also to see if these individuals belong to the M. brevis textillis grateful to Benjamin Tapley who provided useful comments on a prior version of this manuscript. This work was supported by the clade, M. brevis brevis clade or a hypothetic new third Zoological Society of London. clade. The finding of Echis leucogaster in a cracked mud References habitat lacking stones in Oued Drâa was novel as within Arnold, N., Robinson, M., Carranza, S. (2009): A preliminary this region, until this point, this snake was only known analysis of phylogenetic relationships and biogeography of from rocky habitats in two main locations near the towns the dangerously venomous carpet vipers, Echis (Squamata, of Assa and Aouinet Lahna (Koleska et al., 2018). In Serpentes, Viperidae) based on mitochondrial DNA sequences. poorly-explored arid regions, site accessibility can play Amphibia-Reptilia 30: 273‒282. a key role in our understanding of species’ distributions Barata, M., Perera, A., Harris, D.J., Van der Meijden, A., Carranza, (Kane et al., 2017) as more accessible locations receive S., Ceacero, F., García-Muñoz, E., Gonçalves, D., Henriques, S., greater survey attention. A sampling bias likely exists Jorge, F., Marshall, J.C. (2011): New observations of and reptiles in Morocco, with a special emphasis on the Eastern in favour of the known areas of occurrence for E. region. Herpetological Bulletin 116: 4‒14. leucogaster in Morocco and this is evidenced by the Bons, J., Geniez, P. (1996): Amphibiens et reptiles du Maroc large distances between published clusters of locations (Western Sahara compris). Atlas Biogéographique. of this species in Morocco coupled with the seemingly Herpetological Association Espanola, Barcelone. continuous areas of suitable habitat. A photograph of the Brito, J.C., Fahd, S., Geniez, P., Martínez-Freiría, F, Pleguezuelos, exact location in which our specimen was found is shown J.M., Trape, J.F. (2011): Biogeography and conservation of in Fig. 2D. It should be noted that the of Echis viperids from North-: an application of ecological niceh-based models and GIS. Journal of Arid Environments 75: in Africa is complicated; very low genetic divergence 1029‒1037. between E. leucogaster and E. pyramidum was shown Bouazza, A., Lansari, A., Martínez Del Mármol Marin, G., Barthe, by Arnold et al. (2009), however according to Pook et L., Berroneau, M., Donaire, D. (2018): New records in Morocco al. (2009) E. leucogaster is evolving as an independent and predictive distribution modeling for the rare Algerian lineage albeit within the pyramidum clade. The first Thread-snake: Myriopholis algeriensis (Jacquet, 1895). Bulletin Echis locality reported herein represents an additional de la Sociétié Herpétologique du France 166: 43‒50. data point for the Oued Drâa; see Herrmann and Ceacero, F., García-Muñoz, E., Pedrajas, L., Perera, A., Carretero, M. (2010): Tarentola and other gekkonid records from Djebel Herrmann (1999) and Herrmann et al. (2000) for Echis Ouarkziz (SW Morocco). Acta Herpetologica 5: 13‒17. leucogaster localities in the Oued Drâa approximately Crochet, P., Rasmussen, J., Wilms, T., Geniez, P., Trape, J., Boehme, 45 km ESE of here. The second record of this species W. (2008): Systematic status and correct nomen of the western reported in the present work shows the westernmost North African cat snake: Telescopus tripolitanus (Werner 1909) record of this species in Morocco, north of the Djebel (Serpentes: Colubridae), with comments on the other taxa in the Ourakziz and approximately 50 km from the Atlantic dhara-obtusus group. Zootaxa 1703: 25‒46. coast. It also indicates that this species can be affected Dinerstein, E., Olson, D., Joshi, A., Vynne, C., Burgess, N.D., by human infrastructures that retain water; this is one of Wikramanayake, E., Hahn, N., Palminteri, S., Hedao, P., Noss, R., Hansen, M. (2017): An ecoregion-based approach to the most serious hazards for the Moroccan herpetofauna protecting half the terrestrial realm. BioScience 67: 534‒545. according to the expeditions made by these authors and Garcia-Cardenete, L., Pleguezuelos, J. M., Brito, J. C., Jimenez- others (e.g. Garcia-Cardenete et al., 2014). Considering Cazalla, F., Perez-Garcia, M. T., Santos, X. (2014): Water cisterns the records of E. leucogaster in the present work along as death traps for amphibians and reptiles in arid environments. Reptile diversity of southern Morocco 793

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Accepted by Saeed Hosseinian Yousefkhani