Distributional review of the genus Tarentola (Reptilia, Sauria) in Tunisia (North Africa)

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1 Herpetology Notes, volume 5: (2012) (published online on 12 October 2012) Distributional review of the genus Tarentola (Reptilia, Sauria) in Tunisia (North Africa) Wided Tlili 1,*, Michel Delaugerre 2, Ridha Ouni 3 and Saïd Nouira 1 Abstract. During , field observations were made regarding the distribution and habitat occupation of Tarentola ssp. in Tunisia, in order to update our knowledge on their specific distributions. Four of the nine Mediterranean members of the genus Tarentola are present in Tunisia. Prior to our study, Tarentola mauritanica was known to occur from the extreme north to the extreme south of the country. Herein, we limit its distribution at latitude Additionally, we provide sympatric allotopic records of the former and Tarentola fascicularis in central Tunisia. New distribution records and natural history observations are also provided for Tarentola neglecta and Tarentola deserti from southern Tunisia. The herein presented data fills in gaps and marginally extends the known ranges of these species. Additional observations regarding habitat occupation and occurrence in distinct climatic regions are discussed. Keywords. Moorish gecko, Desert wall gecko, Algerian wall gecko, distribution, climatic stages, biotopes. Introduction Geckos of the genus Tarentola have been placed in the Phyllodactylidae family (Gamble et al., 2008b). The Mediterranean members form a complex of species, whose differentiation was initiated during the middle Miocene (Bauer et al., 1997; Kluge, 2001; Carranza et al., 2002; Joger, 2003; Harris et al., 2004; Harris et al., 2009; Rato et al., 2012). Several of these species are indigenous to Tunisia (located on the central-southern shore of the Mediterranean Sea). However, despite the multitude of studies concerning the herpetofauna of Tunisia (Brito et al., 2008), the majority of research conducted on members of the genus Tarentola was limited to travel narratives, faunal lists or minor parts within broader research (Boulanger, 1891; Mayet, 1903; Chabanaud, 1916; Mosauer, 1934; Blanc & Shane, 1980; Bons et al., 1984; Blanc, 1986; Le Berre, 1 Unité de recherche Biodiversité and Biologie des populations, 05/UR/ Département de Biologie, Faculté des Sciences Mathématique, physique et biologiques de Tunis (FST), Campus Universitaire 2092, El Manar Tunis. 2 Reptiles et Amphibiens, Département Systématique & Évolution, Muséum national d Histoire naturelle. Present adress : Conservatoire du littoral, 3, rue Luce de Casabianca F20200 Bastia France. 3 Tunisian Wildlife Conservation Society. Faculté des Sciences Mathématique, physique et biologiques de Tunis (FST), Campus Universitaire 2092, El Manar Tunis. *Corresponding author; alwided@yahoo.fr 1989). More recent studies (Nouira, 1996; 1997; Joger, 2003) reported the occurrence of four species within the country: Tarentola deserti, Tarentola neglecta, Tarentola mauritanica and Tarentola fascicularis. Several occurrence localities have been presented for these four species in the above mentioned literature (Fig. 1B). However, in much of the Tunisian territory that has not been surveyed (due to ancient political circumstances), the distribution of many species remains poorly known. Additionally, the large omission errors and the absence of functional museums make it necessary to describe the maximum geographical extent of these species and compile new distribution maps. Our recent surveys revealed new records within some previously unexplored areas such as the Borma and Jeffara regions. Accordingly, we herein present a distribution review of the genus Tarentola in Tunisia. More importantly, we provide details and comments on the species distributions which are crucial for targeting conservation issues. Materials and Methods Study area Tunisia is characterized by a mosaic of juxtaposed biotopes with distinct local characteristics (Karray, 1979). These mainly include: 1) the Tell region, bordered southwards by the Tunisian Dorsal, 2) the Cape Bon Peninsula, 3) the Sahel Plain, 4) Chott El Jerid, 5) the Grand Erg Oriental, 6) the Jeffara region and 7) the Dahar region (Fig. 1B). The climate of Tunisia is divided into five bioclimatic regions ranging from humid to Saharan (Emberger, 1950). The climate is strongly influenced by the Tunisian Dorsal which separates humid Mediterranean areas from those exposed

2 486 Wided Tlili et al. Figure 1. Map of Tunisia: A: Inventoried sites; B: Literature sightings of Tarentola ssp. Figure 2. Distribution of Tarentola mauritanica in Tunisia.

3 Distributional review of the genus Tarentola 487 Table 1. Inventoried sites

4 488 Wided Tlili et al. Table 2. Taxonomic status of Tarentola ssp. in Tunisia Family Genus & Species Subspecies Reported area of occurrence IUCN statut Ranges from the Iberian Peninsula near threatened Tarentola to Italy in the north of the species mauritanica (Linné, mauritanica Mediterranean sea; from Morocco (Vorgin et al., 1758) to the Nile Delta in the south 2008) (Aprea et al., 2011) Phyllodactylidae Tarentola neglecta Strauch, 1895 Tarentola deserti Boulenger, 1891 : neglecta Endemic to the northern Sahara. Known with certainty in Algeria and Tunisia. Presence in Libya has not yet been confirmed (Schleich et al., 1996). Present in Morocco, Algeria and Tunisia (Schleich et al., 1996, Harris et al., 2006). Least Concern taxa (Joger et al., 2006 a& b) Tarentola fascicularis (Daudin,1802) wolfgangi Reported to occur in Libya and Tunisia (Joger & Bshaenia, 2010) Not assessed to arid climates (Bellil, 1979). There are 15 national parks and nature reserves in Tunisia; the most important ones are: Ichkeul ( ha), El Feydja (417 ha), Dar Chichou (100 ha), Bou Kornine (1 939 ha), Bou Hedma ( ha), Jbil ( ha) and Sidi Toui (6 315 ha). Sampling Within the scope of a thesis project Biodiversity and Biogeography of Tunisian Gekkota the majority of the Tunisian territory was surveyed from 2005 to Field expeditions and specimen collection were carried out after obtaining authorization from the Tunisian Ministry of Agriculture, Department of Forestry Management. Several trips were made in cooperation with the Faculty of Sciences of Tunis and the Tunisian Wildlife Conservation Society. We located geckos by means of searching for active individuals, their burrows and their tracks. We consistently noted the Governorate, GPS coordinates (Longitude, Latitude), date, number of captured specimens, number of individuals released, microhabitat (trash can, mailbox, wall, ruins, rock,...), the vegetal cover, the soil type, regional climate, the presence of a water plan or a water source, proximity to the coast and the altitude. Figure 3. Potential biotopes of Tarentola mauritanica: A: Electricity meters; B: ruin; C: small road bridges; D: urban wastes and E: milestones. Data analysis A total of 115 localities for four species of the genus Tarentola were recorded (Table 1, Fig. 1A). Geographical coordinates and occurrence data were explored with QUANTUM-GIS software (Q-GIS, 2009). A total of 128 specimens were captured; 86 were identified, measured and released. 42 specimens with unknown status were fixed in 95 alcohol, numbered and held in the Laboratory of Population Biology and Ecology, Faculty of Science of Tunis for further identification. Collection numbers are provided in the text between brackets. Species were identified based on the keys provided by Loveridge (1947), Joger (1984) and Schleich et al. (1996). The frequency of occurrence was estimated by the degree of presence expressed as: Dp = (s / S) 100; in which s is the number of sites inhabiting the species and S is the total number of inventoried sites.

5 Distributional review of the genus Tarentola 489 Table 3. Distribution of Tarentola ssp. within Bioclimatic stages Humid Subhumid Sub-arid Arid Saharian upper lower upper median lower upper Inf. upper lower T.m *** *** *** *** *** *** *** *** T.n *** *** T.d *** *** T.f *** *** Total Figure 4. Distribution of Tarentola ssp. in central and southern Tunisia. Results The family Phyllodactylidae in Tunisia comprises four species of the genus Tarentola, which represent 44.44% of the nine Mediterranean species (Rato et al., 2012). Their taxonomic status, their global distribution and their IUCN conservation status are presented in Table 2. Tarentola mauritanica (Linnaeus, 1758) The geographical distribution of the wall gecko extends from the extreme north of Tunisia southwards to latitude (Fig. 2). Tarentola mauritanica was found in 82.6% of the inventoried sites. The most southern point of occurrence is Matmata (33.55, ) where two specimens were encountered [5572] [5576]. While T. mauritanica occupies mainly urban environments, the species was also encountered within rural areas where individuals hide under building bricks, milestones, electricity meters, ruins, graves, or bridges along local roads (Fig. 3). Tarentola fascicularis Joger & Bshaenia, 2010 Recently, Joger & Bshaenia (2010) described Tarentola fascicularis wolfgangi and provided several records for this taxon from Bou Hedma National Park (central Tunisia) (Fig. 1B). Additional to the type

6 490 Wided Tlili et al. Figure 5. Tarentola ssp; A: Tarentola neglecta from Ghour El Kelb; B: Tarentola fascicularis from Bou Hedma national Park; C: Tarentola deserti from Sidi Toui national park and D: Tarentola mauritanica from El Feydja national Park. locality, ten specimens were encountered to the northeast of these records: 2 [5689][5691] and 1 [5693] from Swassi (35.35, 10.55), 1 [5578] from Mezzouna ( , ), 1 [5584] from Meknessi ( , 9.6), 1 [5593] and 1 [5596] from Ouled Chabou ( , ), 1 [5812] and 1 [5814] from Oued Bou Hedma and finally one juvenile [5828] from Jbel Bou Hedma ( , ). Accordingly, 6.1% of inventoried sites harbor T. fascicularis (Fig. 4). The species is usually found under rocks, rarely at the base of shrubs. Behavior is generally nocturnal, while individuals hide during daytime in rock crevices, under bridges or within ruins. Tarentola neglecta Strauch, 1895 The Algerian gecko is endemic to the northern Sahara region. It was initially described to occur essentially around Chott El Jerid (Fig. 1B). We herein add four new records within this region, but more importantly we report five new records that confirm presence of the species in the Grand Erg Oriental: 2 [5774] [5775] around Jbil National Park; 3 [ ] at El Abyedh Sid Achikh; 3 [ ] at Ghour el Kelb ( , ); 1 at Ramadha ( , 10.4) and 1 at Lorzot ( , ). Together, these occurrences comprise 7.8% of inventoried sites in Tunisia (Fig. 4). Tarentola neglecta is usually encountered under tree bark or in dead bushes (e.g. Calligonum azel, Retama retama). However, at Douz and Jbil two individuals were found hidden under stones. Tarentola deserti Boulenger, 1891 Initial occurrence of T. deserti in Tunisia was mentioned by Le Berre (1989) in Metlaoui (34.32, 8.37). Subsequently, a second record was provided by Joger (2003). We encountered T. deserti at 7.4% of the

7 Distributional review of the genus Tarentola 491 Table 4. Occurrence of Tarentola ssp. within Tunisian national parks National park Bioclimatic stage Area (ha) Tarentola species T. m. T.f. T.d. T.n. Ichkeul Sub-Humid *** El feydja Sub-Humid 417 *** Dar Chichou Sub-Humid 100 *** Bou Kornin Sub-Humid *** Bou Hedma Arid-continental *** *** Jbil Saharan *** *** Sidi Toui Arid continental *** inventoried sites (Fig. 4). Most of these sightings fall eastward of the earlier described records (Le Berre, 1989; Joger, 2003), which extends the distribution to cover nearly the entire Jeffara region. Additionally, 2 specimens [5833] [5834] captured at Ghour El Kleb ( , ) show T. deserti to be present in the Grand Erg Oriental. Tarentola deserti is associated with the tabular rocky relief of the great ergs bordering the desert, where individuals were found under stones. Discussion We herein reveal that from north to south Tunisia, the species of the genus Tarentola are gradually replaced. Each bioclimatic area harbors either one or two species (Table 3). The humid region comprising the northern part of the country is inhabited by T. mauritanica, the most ubiquitous and anthropogenic-associated species. Between latitudes and 34 00, i.e. within the subarid and arid regions, the occurrence of T. mauritanica is restricted to minor traces of urbanization. In contrast, nonanthropogenic habitats are occupied by T. fascicularis. Southwards from latitude corresponding to the Jeffara region (arid stage), T. deserti occurs at inland localities and occupies both natural and urbanized regions. Within this area T. mauritanica is restricted to coastal areas, i.e. arid regions under marine influence. Finally, the Saharan region is occupied by T. neglecta which is rarely sympatric allotopic with T. deserti. Finally, we focus attention on the occurrence of Tarentola ssp. in Tunisian national parks. Species richness of each national park seems to be related its local ecological conditions. Specifically, Bou Hedma and Jbil, located within arid and Saharan stages, harbor two species each. The other parks harbor only a single species (Table 4).. Acknowledgements. We express our gratitude to the Tunisian Ministry of Agriculture (Forestry Management Department), specifically Lazhar Hamdi and Jamel Ghouaiel for providing authorizations and assistance during fieldwork. We also thank Mr. Aymen Nefla who helped the achievement of the field work. The editor and the anonymous reviewers provided helpful comments on previous version of the manuscript. References Aprea, G., Lo Cascio, P., Corti, C., Zuffi, M. (2011): Tarentola mauritanica Linné, In: Fauna d Italia, Reptilia, p Corti, C., Capula, M., Luiselli, L., Razzetti, E., Sindaco, R. Ed., Edizioni Calderini de Il Sole 24 ORE Editoria specializzata S.r.l., Bologna. Bauer, A.M., Good, D.A., Branch, W.R. (1997): The taxonomy of the southern African leaf-toed geckos (Squamata: Gekkonidae), with a review of Old World Phyllodactylus and the description of five new genera. Proceeding of the California Academy of Sciences 49: Bellil, M. (1979): Climat de la Tunisie, p In: Atlas de la Tunisie; Les Atlas de l Afrique. ED, Jeune Afrique, Tunisie. Blanc, C.P. (1986): Le peuplement en reptiles de l extrême sud tunisien. Amphibia-Reptilia 7: Blanc, C.P., Shane, M.H. (1980): Les reptiles et les Batraciens de la région de Bou Hedma. Bulletin de la Société des Sciences Natturelles de la Tunisie 13: Böhme, W. Mateo Miras, J.A. Joger, U., El Mouden, E.H. Slimani, T.

8 492 Bons, J., Cheylan, M., Girot, B. (1984): Les reptiles Méditerranéens. Bulletin de la Société Herpétologique de la France 29: Boulenger, G.A. (1891): Catalogue of the reptiles and batracians of Barbary (Morocco, Algeria and Tunisia) based chiefly upon the notes and collections made in by M. Fernand Lataste. Transactions of the Zoological Society of London 13: Brito, J.C., Rebelo, H., Crochet, P.-A., Geniez, P. (2008): Data on the distribution of amphibians and reptiles from North and West Africa, with emphasis on Acanthodactylus lizards and the Sahara Desert. Herpetological Bulletin 105: Carranza, S., Arnold, E.N., Mateo, J.A., Geniez, P. (2002): Relationships and evolution of the North African geckos, Geckonia and Tarentola (Reptilia: Gekkonidae), based on mitochondrial and nuclear DNA sequences. Molecular Phylogenetics and Evolution 23: Chabanaud, P. (1916): Sur divers reptiles de Kébili (Sud tunisien) recueilli par M. le Commandant Vibert. Bulletin du Musée de Histoire naturelle 22: Emberger, L. (1950) : Rapport sur les régions arides et semiarides de l Afrique du Nord, Institut national de la zone aride, UNESCO. 12p. Gamble, T., Bauer, A.M., Greenbaum, E., Jackman, T. R. (2008b): Out of the blue: a novel, trans-atlantic clade of geckos (Gekkota, Squamata). Zoologica Scripta 37(4): Harris, D.J., Carretero, M.A., Corti, C., Lo Cascio, P. (2009): Genetic affinities of Tarentola mauritanica (Reptilia: Gekkonidae) from Lampedusa and Conigli islet (SW Italy). North- Western Journal of Zoology 5(1): Harris, D.J., Batista, V., Lymberakis, P., Carretero, M.A. (2004): Complex estimates of evolutionary relationships in Tarentola mauritanica (Reptilia: Gekkonidae) derived from mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 30: Joger, U. (1984): Taxonomische Revision der Gattung Tarentola (Reptilia: Gekkonidae). Bonner Zoologische Beiträge 35: Joger, U. (2003): Reptiles and Amphibians of Southern Tunisia. Kaupia 12: Wided Tlili et al. Joger, U., Bshaenia, I. (2010): A new Tarentola subspecies (Reptilia: Gekkonidae) endemic to Tunisia. Bonn Zoological Bulletin 57 (2): Joger, U., Slimani, T., El Mouden, H., Geniez, P. (2006). Tarentola deserti. Available at: Last accessed on 25 June Karray, R. (1979) : Relief, Géologie et Géomorphologie de la Tunisie, p In: Atlas de la Tunisie; Les Atlas de l Afrique. Jeune Afrique, ED, j.a., Tunisie. Kluge, A.G. (2001): Gekkotan lizards taxonomy. Hamadryad 26(1): Le Berre, M. (1989): Faune du Sahara. 1: Poissons, Amphibiens et Reptiles. Edition Le Chevalier, Chabaud, Paris. Loveridge, A. (1947): Revision of the African lizards of the family Gekkonidae. Bulletin of the Museum of the Comparative Zoology 98: Mayet, E. (1903): Catalogue raisonné des Reptiles et Batraciens de la Tunisie. Exploration Scientifique de la Tunisie, Paris, Zoologie : Reptiles et Batraciens 32p. Mosauer, W. (1934): The Reptiles and Amphibians of Tunisia. Publications of the Univercity of California of Biological Sciences 1(3): Nouira, S. (1996): Systématique, Ecologie et Biogéographie évolutive des Lacertidae (Reptilia, Sauria). Importance dans l herpétofaune tunisienne. Unpublished PhD thesis. Faculty of Sciences of Tunis. Nouira, S. (1997): Biodiversité de l herpétofaune tunisienne : II. Les Gekkonidae (Reptilia, Sauria). Bulletin de la Société des Sciences Naturelles de la Tunisie 26: Rato, C., Carranza, S., Harris, D.J. (2012): Evolutionary history of the genus Tarentola (Gekkota: Phyllodactylidae) from the Mediterranean Basin, estimated using multilocus sequence data. Evolutionary Biology 14: Schleich, H.H., Kästle, W., Kabisch, K. (1996): Amphibians and Reptiles of North Africa, Ed., Koeltz, Koenigstein. Vogrin, M., Corti, C., Perez-Mellado, V., Sá-Sousa, P., Cheylan, M., Pleguezuelos, J., Baha El Din, S. Martínez-Solano, I. (2008) : Tarentola mauritanica. Available at: www. iucnredlist.org. Last accessed on 25 June Accepted by Wouter Beukema

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