Herpetology Notes, volume 14: 415-420 (2021) (published online on 23 February 2021)

The westernmost record of Chalcides boulengeri Anderson, 1892: an overlooked species in the Atlantic coast of ?

Pablo García Antón1, David López Bosch2, Javier Lobón-Rovira3,*, Alex Torres-Riera4,5, César L. Barrio-Amorós6, and Alberto Sánchez-Vialas4,7

Morocco is one of the best sampled countries in the and reduced limbs (Carranza et al., 2008). In this sense, Maghreb in terms of herpetofauna, hosting a large former morphologically-based classifications included portion of the North African reptile , with the elongated sand-diving species C. sphenopsiformis 107 species of squamates (Bouazza et al., 2021). During (Duméril, 1856) (usually two fingers), C. delislei the last two decades, the knowledge about Moroccan (Lataste and Rochebrune, 1876) (three fingers), and C. herpetofauna has vastly improved through the description boulengeri Anderson, 1892 (five fingers) into a separate of new species and new distribution records (e.g., Harris genus, namely Sphenops. Carranza et al. (2008) revealed et al., 2008, 2010; Crochet et al., 2015; Sánchez-Vialas the non-monophyly of Sphenops, being synonymised and Aznar-González de Rueda, 2016; Javanmardi with the genus Chalcides. The latter is currently et al., 2019; Kane et al., 2019; Miralles et al., 2020). represented in Morocco by 15 species (see Bouazza et This region also represents a source of diversification al., 2021). Chalcides boulengeri is a widespread species for different genera, such as Tarentola and Chalcides in northern Africa, ranging west from to Morocco (Carranza et al., 2002, 2008; Harris et al., 2004). (Trape et al., 2012; del Mármol et al., 2019) (Fig. 1E). In The genus Chalcides Laurenti, 1768, displays a Morocco, this species has been reported in continental remarkable morphological diversity, ranging from sandy areas, from Figuig at the East to the surroundings robust, limbed, pentadactyl species to slender-bodied of Aouinet Ighoumane at the West (del Mármol et al., species with reduced limbs and digits (Lataste, 1876; 2019). Anderson, 1892; Schleich et al., 1996). Fossorial On 12 November 2017 around midday, during a morphological adaptations characterise the sand-diving herpetological survey carried out across Morocco, species, which have usually an elongated shaped body we observed an adult individual of C. boulengeri underneath plastic waste around Tarfaya, in the northern region of Laâyoune-Sakia El Hamra (27.9157°N, 12.9604°W). This region is characterised by a warm 1 Universidad Autónoma de Madrid (UAM), Ciudad climate with oceanic influences (Kriticos et al., Universitaria de Cantoblanco, 28049 Madrid, Spain. 2012) and is located within the Atlantic Coastal Desert 2 Museu de Ciències Naturals de Granollers, C. Palaudàries, eco-region (Burguess et al., 2004). The habitat where 102 – Jardins Antoni Jonch Cuspinera, 08402 Granollers, Catalunya, Spain. the specimen was found is formed by coastal dunes 3 Centro de Investigação em Biodiversidade e Recursos with dispersed stones covered by sparse and shrubby Genéticos, Universidade do Porto, Rua Padre Armando vegetation, dominated by Zygophyllum gaetulum Emb. Quintas, Campus de Vairão, 4485-661 Vairão, Portugal. and Maire, and Launaea arborescens (Batt.) Murb. 4 Asociación Bio+, Av. de América, 64. 7oB, 28028 Madrid, (Fig. 1D). Interestingly, C. sphenopsiformis is widely Spain. distributed along the sandy soils of the southern coastal 5 Department of Evolutionary Biology, Ecology and plain of Morocco, being the only formerly reported Environmental Sciences - Institut de Recerca de la Biodiversitat, Faculty of Biology, Universitat de Barcelona, species within the genus Chalcides in Tarfaya region. Av. Diagonal 645, 08028 Barcelona, Catalunya, Spain. Chalcides boulengeri can be readily distinguished from 6 CRWild / Doc Frog Expeditions, Uvita de Osa, Costa Rica. C. sphenopsiformis by a different account of scales rows 7 Museo Nacional de Ciencias Naturales, C/ José Gutiérrez at mid-body [22–24 in C. sphenopsiformis versus 24–28 Abascal, 2, 28006 Madrid, Spain. in C. boulengeri], limb morphology [extremely reduced * Corresponding author. E-mail: [email protected] fore-limbs in C. sphenopsiformis versus more robust © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. limbs in C. boulengeri], digit numbers [two fingers 416 Pablo García Antón ������ and four toes in C. sphenopsiformis versus five fingers have contributed to C. boulengeri gone unnoticed to and five toes in C. boulengeri], and supralabial scale date. The occurrence of C. boulengeri in coastal dunes arrangement [the fourth supralabial in contact with the with oceanic influences, different from the prevailing eye in C. sphenopsiformis versus the fifth supralabial arid climate in previously known continental records, in contact with the eye in C. boulengeri] (Schleich et suggests that this species may have a wider distribution al., 1996), therefore, the specimen herein reported was than has been considered in previous research. However, identified due to unequivocal morphological features human-mediated introduction cannot be rejected (e.g., (Fig. 1A–C). throughout sand carriage from inner regions occupied This work reports the first coastal record of C. by the species and used for road works or constructions boulengeri in Morocco and the westernmost record of as the specimen was located close to the road). the species, 250 km west from the closest known locality In order to better understand the bioclimatic (del Mármol et al., 2019), being the first area of syntopy requirements of C. boulengeri, we performed an between C. boulengeri and C. sphenopsiformis (Fig. 1E). Ecological Niche Model (ENM) along its natural The high abundance of C. sphenopsiformis in this region distribution area in northern Africa (see Table 1), and the fossorial behaviour of the genus Chalcides, may using the R package Maxnet (Phillips et al., 2017).

Figure 1. (A–B) Photographs showing the details of the head, the forearm, and the whole body of the individual Chalcides boulengeri observed at Tarfaya, Morocco; (C) photograph showing the details of the head and the forearm of a C. sphenopsiformis individual from the same region; (D) habitat where C. boulengeri and C. sphenopsiformis were found in syntopy; (E) geographical distribution of C. boulengeri and C. sphenopsiformis in northern Africa: green dots represent available records of C. boulengeri; blue dots represent records of C. sphenopsiformis reported by Bons and Geniez, 1996; and the red star depicts the new record of C. boulengeri; (F) bioclimatic niche model of C. boulengeri showing its potential geographic distribution in northern Africa. Photographs taken by: Javier Lobón-Rovira (A–B), Alberto Sánchez-Vialas (C), and Pablo García-Antón (D). The westernmost record of Chalcides boulengeri 417

Table 1. Occurrence localities of Chalcides boulengeri in northern Africa with information on country, locality, coordinates, and source.

Country Locality Latitude Longitude Source/Reference 33.6543°N 7.1783°E Trape et al. (2012) Algeria Naama Province: Aïn Séfra 32.7500°N 0.5833°W GBIF Algeria Province 33.1085°N 6.1417°E Trape et al. (2012) Algeria Gardaya Province 32.5175°N 3.6359°E Trape et al. (2012) Algeria 29.5775°N 0.3673°E Trape et al. (2012) Algeria Tinduf Province 27.6541°N 8.0922°W Trape et al. (2012) Algeria Tamanghasset Province 23.5905°N 5.0974°E Trape et al. (2012) Algeria Province 24.9975°N 8.4090°E Trape et al. (2012) Algeria Béchar Province 30.4622°N 2.2886°W Trape et al. (2012) Algeria Mogheul 31.9299°N 1.9199°W Philip de Pous, pers. comm. Algeria Tinduf Province: Tinduf 27.7000°N 8.1700°W del Mármol et al. (2019) Algeria : Tassili n’Ajjer 25.8129°N 8.1339°E Philippe Geniez, pers. comm. Libya Tripoli 32.8925°N 13.1800°E Bauer et al. (2017) Libya Mellaha 32.8950°N 13.2802°E Bauer et al. (2017) Libya Tripoli 32.7845°N 13.2143°E Bauer et al. (2017) Libya Formolga 32.5166°N 13.2666°E Bauer et al. (2017) Libya Jabal Tarrhona 32.4338°N 13.6344°E Bauer et al. (2017) Libya Nalut 31.8667°N 10.9833°E Bauer et al. (2017) Libya Cabao 31.8500°N 11.3000°E Bauer et al. (2017) Libya Badr 32.0408°N 11.5438°E Bauer et al. (2017) Libya Gadamis 30.1333°N 9.4833°E Bauer et al. (2017) Libya Bu Njem 30.6141°N 15.4005°E Bauer et al. (2017) Libya Sawknah 29.0786°N 15.7842°E Bauer et al. (2017) Libya Jufra Oasis 29.0833°N 15.8500°E Bauer et al. (2017) Gafsa: pont Oued el Malah 34.1481°N 8.2925°E Kalboussi et al. (2006) Tunisia Daouz 32.8535°N 10.2895°E Anderson (1892) “Holotype” Tunisia Oued Tefront 32.0868°N 9.7776°E Blanc (1986) Tunisia Kasserine: Firyanah 34.9500°N 8.5670°E GBIF Tunisia 36 km SE of Naftah 33.6485°N 8.1571°E GBIF Tunisia Kebili Gobernorate 33.4607°N 9.0509°E Trape et al. 2012 Tunisia Tataouine Gobernorate 32.3972°N 9.5660°E Trape et al. 2012 Tunisia Medeine Governorate 33.1011°N 9.9485°E Trape et al. 2012 Tunisia Magrane 33.6543°N 7.1783°E Trape et al. 2012 Morocco Figuig 32.1000°N 1.2300°W del Mármol et al. (2019) Morocco Aouinet Lahna 28.4800°N 9.8700°W del Mármol et al. (2019) Morocco Taouz 30.9200°N 3.9900°W del Mármol et al. (2019) Morocco Taouz Ighrem 30.8600°N 4.0300°W del Mármol et al. (2019) Morocco Assa 28.8100°N 9.1400°W del Mármol et al. (2019) Morocco Mahmid 29.8200°N 5.7200°W del Mármol et al. (2019) Morocco Merzouga 31.9300°N 1.9200°W del Mármol et al. (2019) 418 Pablo García Antón ������

Table 1. Continued.

Country Locality Latitude Longitude Source/Reference Morocco Merzouga 31.1000°N 4.0200°W del Mármol et al. (2019) Morocco Tamegroute 30.2700°N 5.6700°W del Mármol et al. (2019) Morocco El Gouera 29.8400°N 6.2100°W del Mármol et al. (2019) Morocco North of El Gouera 29.8800°N 6.1200°W del Mármol et al. (2019) Morocco North of El Gouera 29.9100°N 6.1500°W del Mármol et al. (2019) Morocco South of El Gouera 29.8300°N 5.6300°W del Mármol et al. (2019) Morocco West of El Gouera 29.7200°N 6.2000°W del Mármol et al. (2019) Morocco Ouled Driss 29.8000°N 6.4000°W del Mármol et al. (2019) Morocco Ifraouene n`Naouene 30.2700°N 5.3200°W del Mármol et al. (2019) Morocco Ikhf nÒuzerg 30.1800°N 5.3300°W del Mármol et al. (2019) Morocco Ikhf nÒuzerg 30.2200°N 5.3200°W del Mármol et al. (2019) Morocco Oulad Ouchah 30.4200°N 5.9200°W del Mármol et al. (2019) Morocco Fam El Hisn 28.8200°N 8.9200°W del Mármol et al. (2019) Morocco Assa 28.5600°N 9.5200°W del Mármol et al. (2019) Morocco Southwest of Aouinet Lahna 28.4800°N 9.8700°W del Mármol et al. (2019) Morocco Taskala 28.3591°N 5.7200°W del Mármol et al. (2019) Morocco Sidi SaIïd 28.2899°N 5.7199°W del Mármol et al. (2019) Morocco Erfoud 31.4300°N 4.3100°W del Mármol et al. (2019) Morocco Southeast of Aouinet Lahna 28.2900°N 10.4400°W del Mármol et al. (2019) Morocco Southeast of Foum Zguid 29.8801°N 6.7119°W del Mármol et al. (2019) Morocco Foum Zguid 29.8801°N 6.7119°W del Mármol et al. (2019) Morocco South of Tarfaya 27.9157°N 12.9604°W This work

Nineteen bioclimatic variables were obtained from – 0.954) indicates that the highest suitable areas for the WorldClim 2.0 dataset (Fick and Hijmans, 2017) C. boulengeri are found continuously over northern at a spatial resolution of 30 arc-second (~1 km2), Libya, the southern half of Tunisia, and along the and a correlation model was performed in order to southern slopes of the and the Anti-Atlas eliminate collinearity between the variables (correlation from Algeria and Morocco, respectively, with annual coefficient ≥ 0.7). Variables were selected in order to precipitation (56.9%) and mean diurnal temperature capture all the bioclimatic range within the distribution range (30.7%) being the variables that influenced more area. Therefore, the variables included were: mean markedly the habitat suitability of the species. Moreover, diurnal temperature range, maximum temperature of the the in southern Algeria, and two warmest month, minimum temperature of the coldest additional areas in Morocco, namely the Souss Valley month, annual precipitation, precipitation seasonality, and the arid plain between Marrakech and Essaouira, and precipitation of wettest quarter. Hinge features only represent relatively suitable bioclimatic areas for the with the regularisation parameter set to 2.5 and cross- species. Whereas there have been some reported records validation mode, which uses all the samples leaving one of C. boulengeri in the Hoggar Mountains (Trape et al., out in each run (Bittencourt-Silva et al., 2016), were 2012), the species is absent northwards from the Anti- used to produce smoother response curves and reduce Atlas range in spite of the potential bioclimatic suitability overfitting due to the small sample size (Briscoe et al., of the Souss Valley. The absence of the species in these 2016). Moroccan areas could be explained by the presence of The species distribution model (Fig. 1F, AUC = 0.944 geographic barriers, such as the Anti-Atlas, the lack of ± 0.012, with 95% confidence interval (CI) = 0.934 sandy areas, and the presence of competitive congeneric The westernmost record of Chalcides boulengeri 419 species, such as C. mionecton and C. sphenopsiformis. on Scincus and Scincopus and the age of the Desert. It is noteworthy that the specimen herein reported from Molecular Phylogenetics and Evolution 46(3): 1071–1094. Tarfaya was located outside of suitable bioclimatic Carranza, S., Arnold, E.N., Mateo, J.A., Geniez, P. (2002): Relationships and evolution of the North African geckos, areas (Fig. 1F). This fact could be a consequence of Geckonia and Tarentola (Reptilia: Gekkonidae), based bioclimatic model bias, due to the lack of information on mitochondrial and nuclear DNA sequences. Molecular along the real distribution area for C. boulengeri, Phylogenetic and Evolution 23(2): 244–256. potentially underestimated till date. Consequently, we Crochet, P.-A., Leblois, R., Renoult, J.P. (2015): New reptile encourage future studies to apply mechanistic models records from Morocco and Western Sahara. Herpetology Notes which may help to better understand the potential 8: 583–588. del Mármol, G., Harris, D.J., Geniez, P., de Pous, P., Salvi, D. distribution area of the species, as well as the ecological (2019): Amphibians and Reptiles of Morocco. Frankfurt, segregation between these species (Enriquez-Urzelai et Germany, Edition Chimaira. al., 2019). Enriquez-Urzelai, U., Kearney, M.R., Nicieza, A.G., Tingley, Future research should be focused on gaining R. 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Accepted by Idriss Bouam