Opening a Box of Cryptic Taxa the First Review of the North African Desert Lizards in the Trapelus Mutabilis Merrem, 1820 Compl

Home , Agama aculeata, Agama armata, Agama hispida, Agama impalearis, Agaminae, Imatong Mountains

Zoological Journal of the Linnean Society, 2011, 163, 884–912. With 12 ﬁgures

Opening a box of cryptic taxa – the ﬁrst review of the North African desert lizards in the Trapelus mutabilis Merrem, 1820 complex (Squamata: Agamidae) with

descriptions of new taxazoj_726 884..912

PHILIPP WAGNER1,2*, JANE MELVILLE3, THOMAS M. WILMS4 and ANDREAS SCHMITZ5

1Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, D-53113 Bonn, Germany 2Department of Biology, Villanova University, 800 Lancaster Avenue, Villanova, Pennsylvania 19085, USA 3Department of Sciences, Museum Victoria, Melbourne, Victoria 3001, Australia 4Zoologischer Garten Frankfurt, Bernhard-Grzimek-Allee 1, 60316 Frankfurt am Main, Germany 5Department of Herpetology and Ichthyology, Muséum d’histoire naturelle, C.P. 6434, 1211 Geneva 6, Switzerland

Received 26 May 2010; revised 14 November 2010; 10 December 2010; accepted for publication 15 December 2010

We present a review of the morphology and current taxonomy of North African Trapelus species. The Saharo- Sindian agamid genus contains 15 species, of which five occur in northern Africa. The taxonomy of this complex group continues to provide difficulties for taxonomists because of a lack of consistent morphologically diagnostic characters and relatively high intraspecific morphological variation. In particular, the widespread species Trapelus mutabilis, which occurs from Egypt in the east to Mauritania in the west, has been identified as a species complex and probably represents an artificial grouping of unrelated taxa. This taxonomic uncertainty is exacerbated because a type specimen for T. mutabilis was never designated. In our taxonomic review, we designate a neotype for T. mutabilis, allowing a review of the northern African species, the description of two new taxa, and the compilation of a comprehensive identification key. We present a multivariate analysis of morphology within T. mutabilis and, in addition, we present a molecular phylogenetic analysis incorporating a ~500-bp region of the mitochondrial 16S ribosomal RNA gene, and a relaxed molecular clock analysis to estimate the ages of clades within Trapelus. Our results demonstrate that these lineages have a deep and complex biogeographical history.

ADDITIONAL KEYWORDS: Africa – Morocco – neotype – Trapelus mutabilis ssp. nov.–Trapelus sp. nov.

INTRODUCTION This genus currently consists of 15 species that are characterized by short, thick heads, deeply sunken The genus Trapelus Cuvier, 1817 in the agamid sub- tympana, and a few spiny scales above the ear family Agaminae was resurrected by Moody (1980). opening. The genus Trapelus has a broad distribution across northern Africa into the Middle East and Asia. As a whole this genus has caused considerable *Corresponding author. Current address: Department of difficulties for taxonomists, with numerous species Biology, Villanova University, 800 Lancaster Avenue, Villanova, Pennsylvania 19085, USA. E-mail: complexes having been identiﬁed (e.g. Trapelus rud- [email protected] eratus: Rastegar-Pouyani, 2000; Trapelus agilis:

Figure 1. Figures of Geoffroy’s ‘Changeant d’Egypte’ mentioned in the description of Agama mutabilis Merrem, 1820.

Rastegar-Pouyani, 2005). There remain many unre- 1971) additionally have to be regarded as synonyms solved taxonomic and distributional problems, which of T. pallidus (Reuss, 1834). is particularly apparent in the northern African Recent work on T. mutabilis clearly demonstrates species, for which relatively little taxonomic work has that it is a species complex (Wagner & Böhme, 2007). been undertaken. However, it still remains to be determined whether Five species in the genus occur in Africa: Trapelus synonyms represent valid species or if there are mutabilis (Merrem, 1820): northern Africa; Trapelus unrecognized taxa. A significant impediment to the pallidus (Reuss, 1834): Egypt, Republic of Djibouti resolution of this species complex is that a type speci- (Ineich, 2001), Jordan; Trapelus savignii (Duméril & men of Agama mutabilis Merrem, 1820 was never Bibron, 1837): eastern Egypt; and Trapelus tournev- designated, despite the long history of taxonomic illei (Lataste, 1880): Algeria and Tunisia. The recently research. The original description of the species (‘C. A. described Trapelus schmitzi Wagner & Böhme, 2007, squamis minimis laeuibus [sic!], Habitat in Aegypto’) a member of the T. mutabilis complex, is so far only [Merrem, 1820] is inadequate to differentiate between known from its type locality and a record further west the different cryptic taxa and it appears that no types in Algeria (Wagner, Wilms & Schmitz, 2008). One of were designated. Blasius Merrem published several these species, T. mutabilis, is a widespread taxon, herpetological publications, such as the work ‘Versuch occurring across northern Africa from the western eines Systems der Amphibien – Tentamen Systematis Sahara (Geniez et al., 2004) through Mauritania Amphibiorum’ (Merrem, 1820), where he not only (Padial, 2006), Mali (Joger & Lambert, 1996), split firstly the amphibians from the reptiles and Morocco (Pasteur & Bons, 1960; Schleich, Kästle & covered all known species but also ‘described’ several Kabisch, 1996), Algeria (Doumergue, 1901), Tunisia new taxa (e.g. Bitis arietans and Hypnale hypnale). In (Joger, 2003), Libya (Schleich et al., 1996), and the the description of A. mutabilis, Merrem (1820) refer- Sudan (Geniez et al., 2004) to Egypt (Baha el Din, enced figures in Geoffroy de Saint-Hilaire [see Fig. 1; 2006). The taxonomic complexity of T. mutabilis is published originally in Geoffroy de Saint-Hilaire demonstrated by numerous synonyms (Agama (1809: plate 5, figs 3, 4)] and a description with inermis Reuss, 1834; Agama gularis Reuss, 1834; subspecific classification given by Cuvier (1817), but Agama latastii Boulenger, 1855; Agama leucostigma both of these earlier authors failed to name the Reuss, 1834; Agama aspera Werner, 1893). Several species in accordance to the Linnaean system. There- other taxa (Agama deserti Lichtenstein, 1823; Agama fore, Merrem (1820), who used a German and Latin loricata Reuss, 1834; Agama nigrofasciata Reuss, name for the species within a generic key, is the 1833; Agama leucostygma Reuss, 1834; Trapelus author of A. mutabilis [confirmed by Geoffroy de aegyptius Cuvier, 1829; Agama pallida haasi Werner, Saint-Hilaire, 1827: 128 (footnote)].

differs significantly from other African Trapelus species in morphology, body size, and colour pattern. We address the taxonomic status of these specimens along with all the available types in the T. mutabilis complex in the current study. In addition, the taxonomic status of T. pallidus has caused much debate. Wermuth (1967) and Schleich et al. (1996) referred to the taxon as a synonym of T. mutabilis, whereas Moody (1980), Ineich (2001), Disi et al. (2001), and Baha el Din (2006) recognized it as a valid species. Two subspecies are currently recognized within T. pallidus, including T. pallidus pallidus and T. pallidus agnetae (for the latter see species account). We further investigate the taxonomic status of T. pallidus using molecular data. In full, our review of the North African species of the genus Trapelus incorporates the designation of a neotype for T. mutabilis, a morphological comparison of all available type specimens across the species, and the compilation of an identification key. We also include multivariate morphological analysis on speci- Figure 2. The distribution of Trapelus mutabilis and mens within the T. mutabilis complex and a molecu- Trapelus sp. nov. along the first two morphological prin- lar phylogenetic analysis of ~500-bp region of the cipal components axes. mitochondrial 16S ribosomal RNA gene across seven lineages of Trapelus. We then discuss the biogeographical and evolutionary implications of the Merrem (1820) used an illustration, rather than a updated taxonomy of North African Trapelus. specimen, for the description (Fig. 1) and provided names in two languages [‘schillernde’ (= iridescent) in MATERIAL AND METHODS German and ‘mutabilis’ (= variable) in Latin] as this TAXONOMIC REVIEW research was a review rather than a species description. In addition, a thorough investigation of the Approximately 100 museum specimens, housed pre- collections of the Muséum Nationale d’Histoire dominately at the ZFMK collection (see Appendix 1), Naturelle, Paris, and the University of Marburg were examined and compared with the available type failed to uncover a type specimen of T. mutabilis, material of the relevant species. Measurements and designated by Merrem or Geoffroy de Saint-Hilaire. scale counts were recorded according to Grandison Baha el Din (2006) mentioned that the holotype is (1968) and Moody & Böhme (1984). Where type speci- part of the BMNH collection but a search there also mens were lacking, the original description and addi- failed to uncover a holotype (Colin McCarthy, pers. tional literature were used to compare the different comm.). Thus, we designate a neotype of Agama taxa. The synonymy used follows Wermuth (1967) mutabilis Merrem, 1820 which is in accordance with and Barts (1997). the guidelines of Article 75 of the International Code Museum abbreviations are as follows: BMNH, of Zoological Nomenclature (ICZN 1999). This British Museum of Natural History, London, neotype designation then allows us to review the England; MHNG, Muséum d’histoire naturelle de taxonomy of the T. mutabilis complex. la Ville de Genève, Geneva, Switzerland; MNHN, There are numerous taxa within the T. mutabilis Muséum Nationale d’Histoire Naturelle, Paris, complex for which there has been no taxonomic France; NMW, Naturhistorisches Museum Wien, assessment. For example, Schleich et al. (1996) illus- Austria; SMF, Senckenberg Museum, Frankfurt, trated morphologically unusual specimens from Germany; ZFMK, Zoologisches Forschungsmuseum Cyrenaica in Libya. They provide a colour image of a Alexander Koenig, Bonn, Germany; ZMH, Zoologis- single male in nuptial coloration with a complete ches Museum der Universität Hamburg, Germany. bluish-throat, which they refer to as T. mutabilis (Schleich et al., 1996: plate 21, no. 61). It is obvious MORPHOLOGICAL MEASUREMENTS AND that this specimen is not closely related to T. muta- MORPHOLOGICAL MULTIVARIATE ANALYSIS bilis, despite often being associated with this species Twenty-two meristic and metric characters (Table 1) (e.g. Schleich et al., 1996; Geniez et al., 2004), as it that were thought to be potentially diagnostic were

Figure 3. Projection of two principal components from a principal components analysis run with 92 individuals of North African Trapelus species. REGR (Regression coefficient). analysed. All measurements were carried out using a using nine characters (Table 1) that had initially been dial calliper to the nearest 0.1 mm. identified as possibly diagnostic. The methods Hierarchical cluster analysis and principal compo- detailed above were utilized. nent analysis (PCA) were used to evaluate the morphological data and to explore the phenetic relationships amongst the taxa examined. The Excel TISSUE COLLECTION 2000, SYSTAT 10 and SPSS (10.0) statistical pack- We sequenced a 512-bp region of 16S to determine the ages were used to run the analyses. phylogenetic relationships between North African For analysis 1, voucher specimens of T. mutabilis Trapelus species. We obtained tissues for 14 taxa, (N = 42) and four specimens believed to be a new including outgroups and additionally used six cryptic species were measured to determine whether sequences from existing GenBank entries (Table 1), there were significant morphological differences including the North African species T. mutabilis between these putative species using 11 meristic (neotype, defined within this publication), T. pallidus, and metric characters (Table 1) that were initially T. savignii (neotype defined by Wagner & Crochet, identified as possibly being diagnostic. PCA and dis- 2009), and type material from the two new taxa criminant functional analysis (DFA) were used to recognized in this study. To determine the phyloge- investigate whether T. mutabilis could be distin- netic placement of these North African taxa with guished morphologically from the putative new other Trapelus species, ‘Trapelus sanguinolentus’ species. A PCA was used to reduce the dimensionality (synonymized with T. agilis by Rastegar-Pouyani, of the data and remove collinearity of variables. The 1998), T. ruderatus, and T. agilis were included in the principal components (PCs) were extracted from a study. correlation matrix of the raw data. The number of PCs utilized in the analysis was determined by using the scree test of eigenvalues plotted against factors, DNA SEQUENCING, ALIGNMENT, maximising the adequacy of extraction. PC axes were AND PHYLOGENETIC ANALYSES named by the correlations of the original variables to Samples of muscle tissue were taken from preserved the PC: correlations with absolute values of greater specimens in the MNHN and ZFMK collections. than 0.5 were considered important. We then used DNA was extracted using QiAmp tissue extraction DFA to determine whether the position on each PCA kits (Qiagen) or a modified chelex-protocol (Walsh, axis differed between putative species. Metzger & Higuchi, 1991; Schmitz, 2003). The For analysis 2, 92 additionally voucher specimens primers 16sar-L (light chain; 5′–CGC CTG TTT ATC of all North African species (T. mutabilis: N = 53; T. AAA AAC AT–3′) and 16sbr-H (heavy chain; 5′–CCG pallidus: N = 11; T. savignii: N = 4; T. schmitzi: N = 3; GTC TGA ACT CAG ATC ACG T–3′) of Palumbi et al. T. tournevillei: N = 12; T. sp. nov. N = 5) were analysed (1991) were used to amplify a portion of the mito-

Figure 4. Cladogram of the tree recovered by analysis based on 512 bp of the 16S mtDNA gene. Values above nodes are neighbour-joining bootstrap replicates (20 000 replicates; values below 50% not shown); values below nodes are Bayesian posterior probabilities (values below 0.80 not shown). Red dots (grey in print) and values on the nodes indicate the estimated age of the clade.

Table 1. Abbreviation and definition of the 22 characters Bayesian analysis was executed in MrBayes 3.1.2 used in the morphological analysis (Ronquist & Huelsenbeck, 2003), with the evolutionary model estimated in MrModeltest 2.3 (Nylander, Abbreviation Definition 2008) and the parameters used for the Bayesian analyses following those described in detail by BES Belly scales keeled or smooth Schmitz et al. (2004, 2005b) and Brandley, Schmitz BOS Body scales homogeneous or & Reeder (2005). Thirty-three 16S sequences compris- heterogeneous ing 512 bp (lengths refer to the aligned sequences DS Length of the largest dorsal tubercle including gaps) were obtained. Laudakia stellio (Aga- DSC Dorsal scale rows from shoulder to midae), Agama impalearis (Agamidae), and Chamae- beginning of the tail leo dilepis (Chamaeleonidae) were used as outgroups. FEMUR Femoral length from axilla to knee Sequences have been submitted to GenBank (for FOOT Length of left foot from hinge to claw accession numbers see Table 2). of the longest toe GP Gular pouch present or absent HAND Length of left hand from hinge to ESTIMATES OF DIVERGENCE TIME claw of the longest finger A relaxed molecular clock method within the program HH Head height BEAST v. 1.4.2 (Drummond & Rambaut, 2003) was HL Head length used to estimate divergence times for the different HW Head width clades. All calibration points used in the BEAST IPS Number of scales surrounding the analysis represent the minimum age of the common interparietal scale ancestor of a clade. For the data set we implemented NAS Scale rows between the nasal scales calibration points used in previous studies (Robinson PCS Number of precloacal scales & Van Devender, 1973; Rieppel, Walker & Odhiambo, SAM Scale rows around midbody 1992; Evans, Prasad & Manhas, 2002) and incorpo- SNL Length of snout from tip of snout to rated 82 previously published sequences (Appendix 2) anterior end of orbit to allow a calibration of the data set used in this SVL Snout-vent-length, from tip of snout study. Lognormal distributions were used for three to cloacal scale TH Tail height five scale rows from fossil calibrations (Table 3). A general time-reversible cloacal area +Gmodel of evolution was employed, using an uncor- TL Tail length related lognormal relaxed molecular clock with a log- TOE Length of forth toe excluding the claw normal distribution on the substitution rate across TS Tubercle scales present or absent the tree, with a Yule speciation prior. The analysis VSC Ventral scales from shoulder to was run for ten million generations. The output was cloacal scales. input into TRACER v. 1.3 (Drummond & Rambaut, WDS Width of the largest dorsal scale 2003) to check if stationarity had been reached and to WIP Width of the interparietal scales assess the autocorrelation of rates from ancestral to descendant lineages (Drummond et al., 2006).

RESULTS chondrial 16S ribosomal RNA gene. PCR cycling pro- cedure was as described in Schmitz, Ineich & Chirio MORPHOLOGICAL ANALYSIS (2005a). The designation of a T. mutabilis neotype was PCR products were puriﬁed using Qiaquick puriﬁ- required to clarify the taxonomy of North African cation kits (Qiagen). Sequences were obtained using Trapelus species. A specimen from Egypt was an automatic sequencer (ABI 377). Sequences were selected, which possessed relatively smooth scales, aligned using ClustalX (Thompson et al., 1997; based on the short description given by Merrem default parameters) and manually checked using the (1820): ‘C. A. squamis minimis laeuibus (sic!), Habitat original chromatograph data in the program BioEdit in Aegypto’ (= with very small smooth scales, lives in (Hall, 1999). To construct a preliminary phylogenetic Egypt). In this context, a taxonomic revision of the tree for the full dataset a neighbour-joining (NJ) North Africa Trapelus species is provided in the fol- analysis and Bayesian inference were used. PAUP* lowing section. Further work, beyond the scope of the 4.0b10 (Swofford, 2002) was used to compute the current study, will be needed to determine whether NJ tree and the corrected pairwise distances for specimens from Egypt that have strongly keeled all sequences. Bootstrap analyses with 20 000 scales are also T. mutabilis or whether they are one of NJ-pseudoreplicates were used to evaluate the rela- the synonyms of T. mutabilis or T. pallidus or a new tive branch support in the phylogenetic analysis. The cryptic taxon.

Table 2. Details of voucher specimens included in genetic analysis

Code Species Locality Collection no. Accession no.

Aa Agama atra South Africa: Gordon’s Bay AF355477 Aac Agama aculeata Namibia: Helmeringshausen AF355516 Ac Agama castroviejoi Mauritania: Dahr Chinguetti AY522926 Ai1 Agama impalearis – AJ414675 Ai2 Agama impalearis – AJ414673 Ai3 Agama impalearis – AJ414672 Ap Agama planiceps – AF355476 Lc Laudakia caucasica Iran: Khorasan: 68 km before Quchan; MHNG 2646.15 HQ901098 on road Sabzawar-Quchan Lc1 Laudakia caucasica – AY053765 Lm Laudakia cf. microlepis Iran: Khorasan: km. 44 of road MHNG 2642.10 HQ901097 Gonabad-Ferdows Lme Laudakia cf. melanura Iran: Khorasan: Germad; 50 km before MHNG 2642.15 HQ901099 Torbat-e-Heydaniyen Ln1 Laudakia nupta Iran: Esfahan: Natanz MHNG 2642.18 HQ901100 Ln2 Laudakia nupta Iran: Yazd: km 5 of road Deh Shir-Taft MHNG 2642.13 HQ901101 Ls Laudakia stellio – AB120318 Ls1 Laudakia stellio – AB031993 Lsb Laudakia stellio brachydactyla Egypt: Sinai: El Arish HQ901096 Pa Phrynocephalus albolineatus – AY053768 Pac Phrynocephalus acutirostris – AY053766 Pax1 Phrynocephalus axillaris – AY053771 Pax2 Phrynocephalus axillaris – AB031989 Ph Phrynocephalus helioscopus – AY053805 Ps Pseudotrapelus sinaitus Saudi Arabia: Taif ZFMK 87239 HQ901102 Psc Phrynocephalus scutellatus Iran: Khorasan: Germad; 50 km before MHNG 2642.1 HQ901103 Torbat-e-Heydaniyen Ta1 Trapelus cf. agilis Iran: Sistan, Divaneh to Zabol MHNG 2646.32 HQ901104 Ta2 Trapelus cf. agilis Iran: Sistan, Divaneh to Zabol MHNG 2646.30 HQ901105 Ta3 Trapelus cf. agilis Iran: Khorasan: Shish Pol, 8 km MHNG 2642.41 HQ901107 before Gonabad Ta4 Trapelus agilis Iran: Khorasan: 68 km before Qaen, MHNG 2646.17 HQ901110 on the road Gonabad-Birjand Ta5 Trapelus agilis Iran: Mazandaran: Lar High Valley MHNG 2626.39 HQ901108 Ta6 Trapelus agilis Iran: Boyer Ahmadi va Kohkiluyeh, MHNG 2626.95 HQ901109 Autour de Do Gonbadan Ta7 Trapelus cf. agilis Iran: Kerman, Baft MHNG 2646.50 HQ901106 Tb1 Trapelus boehmei sp. nov. Algeria: Colomb-Bechar ZFMK 49664 HQ901112 Tb2 Trapelus boehmei sp. nov. Mauritania: 220 km south of Nouadhibou MNHN 2006.0343 HQ901113 Tmm Trapelus mutabilis mutabilis Egypt: Kairo ZFMK 64395 HQ901114 Tmp Trapelus mutabilis pallidus Egypt: Sinai, between Wadi Feran and ZFMK 77473 HQ901115 St. Katharina Tp Trapelus mutabilis poppeki ssp. nov. Libya: east of Tarbu ZFMK 63678 HQ901116 Tr1 Trapelus ruderatus Iran: Esfahan: Gonharan, c. km 110 MHNG 2642.35 HQ901117 Esfahan-Daran, c. 30 km before Daran Tr2 Trapelus ruderatus Iran: Esfahan: Gonharan, c. km 110 MHNG 2642.36 HQ901118 Esfahan-Daran, c. 30 km before Daran Tr3 Trapelus ruderatus Iran: Fars: Mehkuyeh MHNG 2642.38 HQ901119 Tr4 Trapelus ruderatus Iran: Fars: Mehkuyeh MHNG 2642.55 HQ901120 Ts1 Trapelus sanguinolentus – AY053886 Ts2 Trapelus sanguinolentus – AY053884 Ts3 Trapelus sanguinolentus – AY053763 Ts4 Trapelus sanguinolentus – AY053885 Tsa Trapelus savignii Egypt: El Arish ZFMK 77470 HQ901121

Table 3. Fossil and biogeographical calibrations for estimation of divergence times, including the settings implemented in the BEAST relaxed clock analyses. All calibration points used in the BEAST analysis (Bayesian evolutionary analysis by sampling trees) represent the minimum age of the common ancestorofa clade

BEAST settings BEAST settings olgclJunlo h ina Society Linnean the of Journal Zoological (lognormal distribution) (normal distribution)

Fossil age Description Calibration Zero off-set Std dev. Mean Std dev.

Middle Jurassic Primitive acrodont iguanian, Common ancestor of all 154 1.25 (154–180 Mya) from the Kota Formation iguanians OF REVIEW in peninsular India. (Iguanidae + Agamidae + Chameleonidae) (Evans et al., 2002). Early Miocene (22.8 Mya) Fossils assigned to Minimum age estimate for 22.8 1.0 ‘sceloporine’ genera, from the clade including

Wyoming and Nebraska Sceloporus, Uma, TRAPELUS (Robinson & Van Devender Holbrookia, Phrynosoma, 1973) and Callisaurus Early Miocene (18 Mya) Fossil Chameleo, but with Minimum age estimate for 18 1.0 morphological similarities the clade including 2011, , to Rhampholeon, from Chameleo and RMNRHR AFRICA NORTHERN FROM Rusinga Island, Lake Rhampholeon

163 Victoria, Kenya (Rieppel

884–912 , et al., 1992; Townsend and Larson, 2002).

Std dev., standard deviation. 891 892 P. WAGNER ET AL.

Table 4A. Principal component (PC) axis loadings and Table 4B. Factor loadings of the ﬁrst two principal com- mean PC scores for traits for Trapelus mutabilis and a ponents (PC) from a correlation matrix of nine variables putative new species of Trapelus. Analysis of morphologi- for 92 individual specimens of the genus Trapelus cal measurements include the following characteristics. Signiﬁcant values are in bold. Variable PC1 PC2

PC1 PC2 PC3 SVL/TL 0.486 -0.438 SVL/HL 0.399 0.632 Morphological traits HW/HL 0.734 0.184 SVL 0.907 0.011 0.013 HH/HL 0.477 0.763 HAND 0.886 0.370 0.046 SAM 0.626 -0.628 FEMUR 0.941 0.108 -0.005 DSC -0.971 0.052 FOOT 0.924 0.164 0.083 VSC -0.971 0.052 SNL 0.836 -0.267 -0.118 TS 0.891 0.007 TOE 0.878 0.206 0.040 GP -0.971 0.052 TH 0.776 -0.077 -0.143 Accumulated % of trace 57.481 750.377 WIP 0.135 0.599 0.688 Eigenvalues 5.173 10.611 WDS 0.577 -0.525 -0.065 PCS 0.395 -0.791 0.143 See Table 1 for definitions of morphological traits. NAS -0.082 -0.564 0.734 Total % variance explained 53.95% 17.04% 9.84% Eigenvalues 5.935 1.874 1.083 had more negative scores (see Fig. 2). These results Species show that the putative new species is significantly Trapelus mutabilis -0.271 -0.019 0.018 longer in SVL, HAND, FEMUR, FOOT, SNL, TOE, Trapelus sp. nov. 2.267 0.806 -0.300 TH, and DS when compared to T. mutabilis. A second PCA analysis was used to identify whether See Table 1 for definitions of morphological traits. there are significant morphological differences amongst North African Trapelus species (N = 92) to identify different lineages and to support the genetic A multivariate analysis was first used to determine results. The following nine characters were analysed: whether there are significant morphological differ- SVL/TL, SVL/HL, HW/HL, HH/HL, SAM, DSC, VSC, ences between T. mutabilis (N = 42) and four speci- TS, and GP (see Table 4B). The analysis indicated that, mens believed to be a new cryptic species. The after excluding certain morphological values (e.g. following 11 combined meristic and metric characters gular pouch present or absent, dorsal scales homo- or were analysed using a PCA: SVL, HAND; FEMUR; heterogeneous or ventral scales smooth or keeled), a FOOT; SNL; TOE; TH; DS; PCS; NAS; IPS (for significant separation of several Trapelus species is not abbreviations see Table 1). The PCA that incorporated possible. Even including these values resulted in a three factors accounted for 80.83% of the variance of separation of two distinct lineages only, which are the raw data (Table 4A). The first PCA was positively supported by genetic analysis, and a separation of all correlated with SVL, HAND, FEMUR, FOOT, SNL, species of the T. mutabilis complex was not possible TOE, TH, DS, where a positive value on this axis based on these characters (see Fig. 3). indicated larger values for all these variables (Fig. 4). PC axis two was positively correlated with IPS and negatively correlated with DS, PCS, and NAS, indi- PHYLOGENETIC RELATIONSHIPS AND cating that animals with positive values on this axis DIVERGENCE TIME ESTIMATES have higher numbers of IPS and fewer counts of PCS, Phylogenetic relationships amongst seven Trapelus NAS, and shorter lengths of DS. Finally, the third PC taxa, based on the NJ and Bayesian analyses of a axis was positively correlated with IPS and NAS, 512-bp portion of the 16S ribosomal RNA gene are where a positive value designated an animal with presented in Figure 4. Trapelus is highly supported as higher counts of IPS and NAS. DFA indicated that monophyletic (99%). Within Trapelus there is a large T. mutabilis could be distinguished morpholo- polytomy with three strongly supported clades: (1) T. gically from the putative new species, with a signifi- cf. agilis, T. sanguinolentus, T. mutabilis, T. pallidus, cant discriminant function (l=0.40, F3,42 = 21.47, and T. sp. nov. (91%); (2) T. savignii and Trapelus P < 0.001) and 98% (41/42) of T. mutabilis and 100% agnetae (100%); and (3) T. ruderatus (100%). Within of the putative new species classified correctly. The the first of these lineages, T. mutabilis and T. pallidus putative new species had strongly positive classifica- form a well-supported clade (82%), as does T. sp. nov. tion functions on PC1 and PC2, whereas T. mutabilis (99%). The uncorrected genetic divergences between

© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 884–912 REVIEW OF TRAPELUS FROM NORTHERN AFRICA 893 the Trapelus species range between 3 and 8% Species included and not part of this review: Trapelus (Table 5). Trapelus mutabilis and T. pallidus were microtympanum, Trapelus agilis, Trapelus megalo- found to have the smallest genetic divergence (1.4%), nyx, Trapelus lessonae, Trapelus rubrigularis, Trape- bringing into question the species status of T. palli- lus sanguinolentus, Trapelus flavimaculatus, Trapelus dus. The genetic divergence between T. sp. nov. and T. jayakari, Trapelus ruderatus. mutabilis/T. pallidus ranged between 2.7 and 3.3% and between T. sp. nov. and T. cf. agilis and T. agilis was 2.6% (Table 5). Our analysis does not include TRAPELUS MUTABILIS (MERREM, 1820) T. schmitzi and T. tournevillei, which may provide 1820 Agama mutabilis Merrem, Tent. Syst. Amph. 50. important insight into phylogenetic relationships – Terra typica: in Aegypto. within this genus in future studies. 1823 Agama deserti Lichtenstein, Verz. Doubl. Mus. The relaxed lognormal clock analysis of the 16S data berolin. 101. – Terra typica: Aegyptius. set was undertaken to provide an estimate of diver- 1833 Agama inermis Reuss, Mus. Senckenberg., gence times within Trapelus (Table 6). Examination of Frankfurt am Main 1: 33. – Terra typica: the log file in TRACER v.1.3 indicated a slight ten- Ober-Ägypten. dency toward a positive correlation in the rate of 1833 Agama gularis Reuss, Mus. Senckenberg., parent to child branches, with a covariance of 0.042 but Frankfurt am Main 1: 36. – Terra typica: zero was included in the 95% HPD (highest posterior Ober-Ägypten. density) (-0.091–0.185); thus, this autocorrelation was 1885 Agama latastii Boulenger, Cat. Liz. Brit. Mus. 1: not considered significant (Drummond et al., 2006). 344. – Terra typica: Egypt. The coefficient of rate variation was estimated to be 1893 Agama aspera Werner, Zool. Anz., Leipzig 16: 0.705 (95% HPD: 0.570–0.842), indicating that the 359. – Terra typica: Algerische Sahara zwischen data set is not strictly clock-like and that a lognormal Kef-el-Dhor und Chegga; Biskra-Bordj-Saada; Zab- relaxed clock is appropriate. Divergence time esti- el-Zig südlich von El Meranyer. mates indicate that Trapelus is an old lineage, dating back to the late Oligocene – early Miocene (Table 6). The entire clade containing T. sp. nov., T. mutabilis, T. Neotype: ZFMK 64395: Egypt, 10 km north-west of pallidus, T. agilis, T. cf. agilis,andT. sanguinolentus is Cairo; leg. Hans-Werner Herrmann, ix.1990 (Fig. 5). estimated to have originated during the mid-Miocene (Table 6). The single putative new species T. sp. nov. is much younger, with an age estimate of a Pliocene– Diagnosis: Trapelus mutabilis is a small [largest Pleistocene origin. These results indicate that there is voucher from Egypt SVL 90 mm (Baha el Din, 2006)] a complex history of diversification and speciation in species within the genus, possessing irregular dorsal North African Trapelus species. scalation. This species differs from its probable closest relative, T. pallidus, in having a heterogeneous dorsal TAXONOMIC REVIEW OF THE NORTH scalation with rhomboidal and scattered enlarged scales. In contrast, T. pallidus has a matrix of com- AFRICAN SPECIES OF THE GENUS paratively uniform, smooth dorsal scales, with some TRAPELUS AND DESCRIPTION scattered larger keeled scales. In addition, T. muta- OF NEW TAXA bilis differs from T. pallidus in having homogeneous TRAPELUS CUVIER, 1817 scalation on the hindlimbs and base of the tail. 1817 Trapelus Cuvier, Règne animal 2, Rept. 35. Coloration in life is uniformly sandy grey with four 1843 Eremioplanis Fitzinger, Syst. Rept 1: 18, 82. to five transverse bands and a barred tail. Male T. Species typica (by monotypy): Agama mutabilis mutabilis have nuptial coloration of violet-blue flanks Merrem, 1820 and throat; in contrast male T. pallidus coloration is 1843 Planodes Fitzinger, Syst. Rept 1: 18, 81. Species restricted to having a completely blue head. typica (designatio originalis): Agama agilis Olivier, Trapelus mutabilis differs from two specimens from 1807 Libya in not possessing scale rows of enlarged verte- 1843 Trapeloides Fitzinger, Syst. Rept 1: 18, 81. bral scales (for details see description below). Trapelus mutabilis differs from T. savignii in having Type species: Agama mutabilis Merrem, 1820 smooth ventral scales and no gular pouch, from T. schmitzi in having heterogeneous dorsal scalation and Diagnosis: Tympanum small, diameter less than half from T. tournevillei in having a shorter tail (average of of the orbit, deeply sunk. Head usually high rather ratio TL/SVL 1.39 in T. mutabilis instead of 1.60 in T. than short. Caudal scales not forming distinct annuli. tournevillei), no gular pouch, a heterogenous dorsal sca- Only males with callous precloacal scales. lation, and the lack of longitudinal stripes on the belly.

© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 884–912 894 Table 5. Uncorrected 16S pairwise sequence divergences between several Trapelus species, including the neotype of Trapelus mutabilis and the holotype of the herein-described species. Pseudotrapelus sinaitus and Phrynocephalus scutellatus were used as outgroups. .WAGNER P. P. sinaitus Ps P. scutellatus Psc T.cf.agilis Ta1 T.cf.agilis Ta2 T.cf.agilis Ta7 T.cf. agilis Ta3 T. agilis Ta5 T. agilis Ta6 T. agilisTa4 T. sanguinolentus Ts1 T. pallidus Tmp

Pseudotrapelus sinaitus Ps–––––––––– – Phrynocephalus scutellatus Psc 0.1836 – –––––––– – Trapelus cf. agilis Ta1 0.1550 0.1271 –––––––– –

T.cf.agilis Ta2 0.1550 0.1271 0.0000 ––––––– – AL ET 01TeLnenSceyo London, of Society Linnean The 2011 © T.cf.agilis Ta7 0.1611 0.1352 0.0443 0.0443 – – – – – – – T.cf.agilis Ta3 0.1631 0.1271 0.0221 0.0221 0.0564 – – – – – –

T. agilis Ta5 0.1671 0.1271 0.0262 0.0262 0.0483 0.0221 – – – – – . T. agilis Ta6 0.1671 0.1271 0.0262 0.0262 0.0483 0.0221 0.0000 – – – – T. agilis Ta4 0.1631 0.1271 0.0221 0.0221 0.0564 0.0000 0.0221 0.0221 – – – Trapelus sanguinolentus Ts1 0.1549 0.1271 0.0241 0.0241 0.0463 0.0221 0.0161 0.0161 0.0221 – – Trapelus pallidus Tmp 0.1733 0.1351 0.0403 0.0403 0.0342 0.0423 0.0342 0.0342 0.0423 0.0322 – Trapelus savignii Tsa 0.1652 0.1272 0.0725 0.0725 0.0665 0.0806 0.0685 0.0685 0.0806 0.0705 0.064 Trapelus boehmei Tb1 0.1611 0.1311 0.0443 0.0443 0.0342 0.0423 0.0383 0.0383 0.0423 0.0322 0.026 T. boehmei Tb2 0.1615 0.1363 0.0446 0.0446 0.0361 0.0404 0.0403 0.0403 0.0404 0.0340 0.027 Trapelus mutabilis Tmm 0.1734 0.1331 0.0423 0.0423 0.0403 0.0443 0.0362 0.0362 0.0443 0.0342 0.014 T. mutabilis Tp 0.1693 0.1412 0.0443 0.0443 0.0423 0.0423 0.0383 0.0383 0.0423 0.0362 0.018 Trapelus agnetae Tag 0.1876 0.1425 0.0856 0.0856 0.0756 0.0935 0.0803 0.0803 0.0935 0.0855 0.0726 Trapelus ruderatus Tr1 0.1576 0.1277 0.0669 0.0669 0.0526 0.0790 0.0689 0.0689 0.0790 0.0689 0.056 T. ruderatus Tr2 0.1576 0.1277 0.0669 0.0669 0.0526 0.0790 0.0689 0.0689 0.0790 0.0689 0.056 T. ruderatus Tr3 0.1637 0.1316 0.0728 0.0728 0.0626 0.0829 0.0728 0.0728 0.0829 0.0728 0.060

olgclJunlo h ina Society Linnean the of Journal Zoological T. ruderatus Tr4 0.1637 0.1316 0.0728 0.0728 0.0626 0.0829 0.0728 0.0728 0.0829 0.0728 0.060

T. savignii Tsa T. boehmei Tb1 T. boehmei Tb2 T. mutabilis Tmm T. mutabilis Tp T. agnetae Tag T. ruderatus Tr1 T. ruderatus Tr2 T. ruderatus Tr3 T. ruderatus Tr4

Pseudotrapelus sinaitus Ps–––– –––––– Phrynocephalus scutellatus Psc–––– –––––– Trapelus cf. agilis Ta1–––– –––––– T.cf.agilis Ta2–––– –––––– T.cf.agilis Ta7–––– –––––– T.cf.agilis Ta3–––– –––––– T. agilis Ta5–––– –––––– T. agilis Ta6–––– –––––– T. agilis Ta4–––– –––––– Trapelus sanguinolentus Ts1–––– –––––– Trapelus pallidus Tmp–––– –––––– Trapelus savignii Tsa–––– –––––– Trapelus boehmei Tb1 0.0665 – – – – – ––––

2011, , T. boehmei Tb2 0.0700 0.0021 – – – – –––– Trapelus mutabilis Tmm 0.0564 0.0322 0.0337 – – – –––– T. mutabilis Tp 0.0665 0.0282 0.0254 0.0201 – – ––––

163 Trapelus agnetae Tag 0.0392 0.0781 0.0809 0.0673 0.0803 – –––– Trapelus ruderatus Tr1 0.0626 0.0607 0.0641 0.0627 0.0648 0.0779 –––– 884–912 , T. ruderatus Tr2 0.0626 0.0607 0.0641 0.0627 0.0648 0.0779 0.0000 – – – T. ruderatus Tr3 0.0687 0.0687 0.0726 0.0707 0.0687 0.0876 0.0182 0.0182 – – T. ruderatus Tr4 0.0687 0.0687 0.0726 0.0707 0.0687 0.0876 0.0182 0.0182 0.0000 – REVIEW OF TRAPELUS FROM NORTHERN AFRICA 895

Table 6. Estimated age of the common ancestor of selected phylogenetic clades in millions of years, using relaxed molecular clock analyses. The estimate and 95% credibility intervals (CIs) are presented for 16S

Estimated age (Mya) 95% CI (Mya)

Trapelus boehmei sp. nov., Trapelus mutabilis, Trapelus pallidus, 14.4 9.3–18.9 Trapelus agilis, T. cf. agilis, Trapelus sanguinolentus T. boehmei sp. nov. 1.8 0.5–4.4 T. mutabilis, T. m. pallidus, Trapelus mutabilis poppeki ssp. nov. 5.7 2.1–8.0 Trapelus ruderatus 5.4 2.3–9.6 Trapelus savignii, Trapelus haasi 9.1 4.9–14.1 Trapelus 21.7 15.5–28.6 Agama 32.4 18.0–42.5 Agaminae 53.7 33.3–72.3

Figure 5. Neotype (ZFMK 64395) of Agama mutabilis Merrem, 1820.

Description of the neotype: Habitus: stout; tail only eye with the tip of the longest digit. Coloration in moderately longer than the body; hindlimbs relatively alcohol. Uniform dirty white but a blue throat and long. blue flanks are visible. Measurements. Snout-vent length 74.2 mm; tail length 90.5 mm; head length 22.3 mm; head height TRAPELUS MUTABILIS PALLIDUS 11.8 mm; head width 18.1 mm; length of left forelimb (REUSS, 1834) STAT. NOV. 33.9 mm; length of left hindlimb 54.5 mm. Scalation. Nostril sits on the canthus rostralis, 1834 Agama pallida Reuss, Mus. Senckenberg., piercing the posterior portion of a large, flat nasal Frankfurt am Main 1: 38. – Terra typica: scale; nostril is directed obliquely upwards. Head Ober-Ägypten. scales heterogeneous in size and shape, supraocular 1834 Agama loricata Reuss, Mus. Senckenberg., scales smooth, interorbital region with a median Frankfurt am Main 1: 40. – Terra typica: peträis- row of three longitudinal scales separating the ches Arabien. sideward originating scales. Interparietal scale 1834 Agama nigrofasciata Reuss, Mus. Senckenberg., small, more or less rectangular, surrounded by eight Frankfurt am Main 1: 40. – Terra typica: Nubien, enlarged scales; parietal organ visible and half of Ober-Ägypten und Arabien. the size of the parietal scale. A median series of 1834 Agama leucostygma Reuss, Mus. Senckenberg., longitudinal and quadrangular scales is visible from Frankfurt am Main 1: 44. – Terra typica: the parietal scale to the rostral. Scales originating Ober-Ägypten. from both sides of the parietal midline have imbri- 1848 Trapelus aegyptius Duvernoy, in Cuvier, Règne cations directed laterally and the free anterior animal, Rept. 54. – Terra typica: Egypte. margins of the scales have sensory pits. Mucronate scales on the eyelids form a ring. The ear openings Holotype: SMF 10007 (Fig. 6). are small, approximately one third of the diameter of the eye, with the superior margin having six Diagnosis: Small to medium-sized species of the spinous, mucronate scales in two rows on both sides genus with an average ratio TL/SVL of 1.1. Gular of the ear opening. The tympanum is sunken and pouch absent. Ear opening more or less round, not clearly visible. A rudimentary nuchal crest is usually with a smooth margin, but often spiny scales present, consisting of ten spiny, mucronate scales. are present. Dorsal scales small, equal in size, Gular scales are smooth, being enlarged and imbri- forming a matrix with intermixed larger scales. cate at the posterior margin, and are slightly Ventral scales smooth. smaller on the gular fold. A very weakly defined Trapelus mutabilis pallidus is distinct from the gular pouch is present. Ventral scales are smooth, nominate form in possessing a higher count of slightly imbricate, and equal in size. Dorsal scales scale rows around midbody and in having a matrix of are heterogeneous, rhomboidal, smooth to keeled, uniform small dorsal scales with some intermixed slightly imbricate; larger scales are keeled and larger scales. mucronate, being two to three times larger than the other scales and intermixed with smaller scales Taxonomic note: Even though T. pallidus is often across the dorsum. Scales on tail are strongly keeled recognized as a distinct species or synonym of T. and mucronate, not arranged in whorls. The tail is mutabilis by other authors (e.g. Schleich et al., 1996; cylindrical and relatively short – only 22% longer Sindaco & Jeremcˇenko, 2008), both results from mor- than the snout-vent length. Two rows of 21 (11 ante- phology (Table 7) and genetics (Table 5) support its rior, 10 posterior) precloacal pores. Forelimbs have validity as a subspecies of T. mutabilis. strongly keeled scales on the upper side, becoming smooth on the underside, being homogeneous in TRAPELUS MUTABILIS POPPEKI SSP. NOV. size; fourth digit longest, digital length decreasing 4-3-2-5-1, plantar scales and subdigital lamellae Holotype: ZFMK 63678: juvenile, Libya: east of Tarbu, (with two keels) strongly keeled. Hindlimbs have 24.48.27N, 16.19.11E, 490 m a.s.l., leg. Hemmo keeled scales on the upper side, becoming smooth on Nickel, ix.1996 (Fig. 7). the underside, scales on upper side are homogeneous in size, becoming smaller on the underside; Paratype: ZFMK 20848: female, Libya: Tripolis, leg. digits are long with long claws, fourth digit longest, W. Schlüter, 1913 (Fig. 7). approximately 25% longer than the third digit, digital length decreasing 4-3-5-2-1, plantar scales Diagnosis: A small to medium sized subspecies of T. and subdigital lamellae (with two keels) strongly mutabilis with all the typical characteristics of the keeled. Hindlimbs are relatively long, reaching the genus. Trapelus m. poppeki ssp. nov. differs from

Figure 6. Holotype (SMF 10007) of Agama pallida Reuss, 1834.

many other valid Trapelus species and T. m. mutabilis – T. m. mutabilis (type locality: Egypt) in possessing and T. m. pallidus in its typical body scalation of enlarged vertebral scales in comparison to much enlarged vertebral scales and much smaller lateral smaller scales on the ﬂanks. scales. Only T. savignii has a similar body scalation. – T. m. pallidus (type locality: southern Egypt) in A second characteristic is the small pineal scale, possessing enlarged vertebral scales in comparison which is not much larger than the pineal organ. to much smaller scales on the ﬂanks. Trapelus m. poppeki ssp. nov. differs from valid – T. tournevillei (type locality: Ouargla, Algeria) African species of Trapelus: in having a shorter head, brownish transverse bands on the body, and smooth ventral – T. savignii (type locality: Egypt) in not possessing a scales (instead of keeled ventral scales in T. gular pouch, in having the ventral scales smooth tournevillei) and in lacking longitudinal lines on and in a high genetic distance. the belly.

– T. schmitzi (type locality: Ennedi Mts., Chad) in ) possessing a very heterogenous body scalation with enlarged vertebral scales and smaller lateral scales, and in having brownish transverse bands on the body. Trapelus m. poppeki ssp. nov. differs from the following synonyms (Agama aspera is maybe a valid taxon, but clearly different to the here-described subspecies and more research is needed to clarify the status of this taxon):

Trapelus – Agama inermis Reuss, 1833 (type locality: southern Egypt) in possessing enlarged vertebral scales. – Agama gularis Reuss, 1833 (type locality: southern Egypt) in possessing enlarged vertebral scales. – Agama latastii Boulenger, 1885 (type locality: Egypt) in lacking equal sized, rhomboidal dorsal scales. – Agama aspera F. Werner, 1893 (type locality: Alge- rian Sahara, between Kef-el-Dhor and Chegga; Biskra-Bordj-Saada; Zab-el-Zig south of El Mer- anyer) in possessing no spiny scales and a hetero- and a putative new species of geneous dorsal scalation.

Description of the holotype: Measurements. Snout-vent length 36.5 mm; tail length 49.3 mm; head length 10.8 mm; head height 6.9 mm; head width 9.6 mm; length of left forelimb 19.8 mm; length of left hind-

Trapelus mutabilis limb 31.1 mm. Scalation. Nostril on the canthus rostralis, piercing in the posterior part of a large, flat nasal scale; nostril is directed obliquely upwards. Head scales heterogeneous in size and shape: supraocular scales smooth; parietal organ pierces the corner of an enlarged scale, giving the impression that it is in the middle of four enlarged scales that are surrounded backwards by four larger scales. Between the eyes a row of three longitudinal scales is obvious. Scales originating from both sides of the parietal midline have imbrications directed laterally, with their free anterior margins having sensory pits. Eyelid with mucronate scales forming a ring. The ear opening is medium in size, less than half of the size of the eye, having a superior margin with five spiny, mucronate scales on both sides; tympanum sunken but visible. A rudimentary nuchal crest is present, consisting of five spiny, mucronate scales. Gular scales are flat, smooth, with the posterior margins being enlarged and slightly imbricate; gular scales are equal in size but become smaller on the gular

75.82 (1.053) 11.94 (0.156) 16.88 (0.225) 20.48 (0.261) 8.19 (0.104) 10.48 (0.155) 6.82 (0.181) 0.98 (0.043) 1.86 (0.056) 2.62 (0.059) 3.42 (0.116) fold. Gular fold small. Gular pouch absent. Ventral SVL111.75 (1.582) HAND 16.35 (0.343) 22.38 (0.730) FEMUR 25.75 (0.690) 9.60 (0.183) 13.25 FOOT (0.405) 10.40 (0.204) 1.075 (0.111) SNL 2.20 (0.147) 2.625 (0.131) 3.00 (0.0 TOE TH WIP WDS PCS NAS scales are smooth, slightly imbricate, and equal in size. Dorsal scales smooth to keeled, slightly imbricate, (44) Mean (± SE) values of diagnostic morphological characteristics for sp. partly mucronate, and heterogeneous, intermixed with

(4) larger, keeled scales. Vertebral scales much larger than scales on the ﬂanks. Scales on tail strongly mutabilis nov. Table 7. See Table 1 for deﬁnitions of morphological traits. Trapelus Trapelus keeled, mucronate, and not arranged in whorls. The

Figure 7. Holotype (A, ZFMK 63678) and paratype (B, ZFMK 20848) of Trapelus mutabilis poppeki ssp. nov. tail is cylindrical and relatively long, nearly as long as 4-3-2-5-1, plantar scales and subdigital lamellae the snout-vent length. Only one row of about ten strongly keeled. weakly developed precloacal pores is present. Fore- Coloration in alcohol. Ground coloration sandy to limbs with strongly keeled scales on the upperside, grey and some of the enlarged scales are recognizable becoming smooth to the underside, homogeneous in as whitish dots. The tail is barred. On the shoulders size; digits are long with long claws, fourth digit a black blotch is visible. Underparts of the specimen longest, digital length increasing 4-3-2-5-1, plantar are uniform whitish. On the throat pale brownish scales and subdigital lamellae are strongly keeled. lines are visible. Hindlimbs have strongly keeled and slightly mucronate scales on the upper-side, becoming smooth Paratype: Habitus of the paratype, a pregnant female, and nonmucronate to the underside, scales on is stout; tail only moderately longer than the body. the upperside are homogeneous in size, becoming Measurements. Snout-vent length 75.4 mm; tail smaller on the underside; digits are very long with long length 94.0 mm; head length 21.0 mm; head height claws, fourth digit longest, digital length increasinge 11.6 mm; head width 17.1 mm; length of left forelimb

35.8 mm; length of left hindlimb 53.1 mm. Scalation. Holotype: ZFMK 2590 (Fig. 8). The parietal scale is small, more or less rectangular, surrounded by three enlarged scales and four scales of Diagnosis: A small species of Trapelus with a short equal size; pineal organ visible, piercing the middle of tail. Head short and thick. Gular pouch absent. Easy the scale, in contrast to the holotype. Likewise, there to identify by its homogeneous, smooth to feebly are no elongate scales between the eyes. Ventral keeled dorsal scales, intermixed with only a few scales usually smooth, but with the impression of larger scales. Scalation of hindlimb homogeneous. keels and also partly very feebly keeled. Coloration in alcohol. Basic dorsal coloration of body, tail and head uniform yellowish to sandy. On Remarks: This species was described by a single the body fragments, three brown transverse bands voucher from Chad. Recently, a second voucher from are obvious, interrupted by yellowish stripes and Algeria was identiﬁed in the MHNG collection dashes. The tail is barred; the ﬁrst six bars are (Wagner, Wilms & Schmitz., 2008). Andersson (1935) interrupted by a yellowish line. Head with some reported a specimen from the Hoggar Mountains with brownish shades, which gives the impression that ‘scales on the back are uniform smooth, without any the brownish bands are also present there. Ventral scattered larger scales among them’. This description coloration uniform whitish without any markings on clearly refers to T. schmitzi and the Hoggar Moun- the throat. tains are within the supposed distribution range.

Relationships: Regarding the interspecific molecular data between the North African taxa of Trapelus, and TRAPELUS BOEHMEI SP. NOV. the new subspecies the uncorrected 16S pairwise Holotype: ZFMK 49751: Morocco, between Akka and sequence divergences were calculated as follows: T. Icht; leg. W. Bischoff & U. Joger, 27.v.1988 (Fig. 9). sp. nov. – T. m. poppeki ssp. nov. = 2.55–2.82%; T. m. mutabilis – T. m. poppeki ssp. nov. = 2.02%; T. m. Paratypes: ZFMK 49752–754: Morocco, between Akka pallidus – T m. poppeki ssp. nov. = 1.82%; T. savignii and Icht; leg. W. Bischoff & U. Joger, 27.v.1988; ZFMK – T. m. poppeki ssp. nov. = 6.65%. Within the T. muta- 49664: Algeria, Colomb-Bechar; leg. W. Bischoff & U. bilis complex, the genetic distances are highest Joger, 13.v.1988; MNHN 2006.0343: Mauritania, between the new species described in this paper and about 220 km south of Nouadhibou on the main road T. mutabilis poppeki ssp. nov., whereas they are to Nouakchott; leg. I. Ineich, 21.vii.2005; ZMB 52277: slightly lower for the recognized subspecies of T. Morocco, 40 km north of Zagora; leg. M. Barts, mutabilis. Moreover, the genetic analysis completely iv.1993; ZSM 207/1993: Morocco, 10 km south-east of supports the morphological results as it corroborates Goulmima; adult female; leg. H. H. Schleich, vi.1993; the distinctiveness of the new taxon as a subspecies of ZSM 225/1993: Morocco, 25 km west of Tissint, adult the T. mutabilis complex and shows it to be clearly male; leg. H. H. Schleich, vi.1993; ZSM 688/1979/1-5: distinct from T. savignii. Morocco, Ksar es Souk (W Bou Denib), adult males, leg. E. Linsenmair, 26.vi.1967. Habitat: Details of the habitat are unknown, but similar requirements to the habitat as in other North Diagnosis: A large Trapelus species with the typical African Trapelus species seem obvious. ear opening found in the genus: sunken tympanum and spiny scales above the ear opening. Trapelus Etymology: The new species is named after Hans- boehmei sp. nov. has a relatively long head tapering Jürgen Poppek for his decades of honorary work, e.g. abruptly at the nose, giving it a stout appearance. as chairman of the German national scout and guide Body scalation is a matrix of small, feebly keeled and association ‘Verband Christlicher Pfadfinderinnen homogeneous scales intermixed with larger keeled und Pfadfinder’. scales, which usually differ in coloration from the matrix scales in breeding coloration of adult males; Distribution: The new species is so far only known sometimes vertebral matrix scales are larger than the from the two localities of the type specimens (Libya: lateral matrix scales and nearly as large as the inter- Tripolis; Libya: east of Tarbu). mixed scales. Males have bluish coloration on the throat and body when in nuptial coloration, and a small gular pouch. The new species differs from all TRAPELUS SCHMITZI WAGNER &BÖHME, 2007 described African taxa in Trapelus by its unique col- 2007 Trapelus schmitzi WAGNER &BÖHME, Bonn. oration, body proportions, and scale morphology. zool. Beitr. 55: 82. – Terra typica: Guelta Archei, Trapelus boehmei sp. nov. differs from currently Ennedi Mts., Chad. valid African species of Trapelus (some selected

Figure 8. Holotype (ZFMK 2590) of Trapelus schmitzi Wagner & Böhme, 2007. variable characters comparing the new species with – Trapelus savignii (type locality: Egypt) in having T. mutabilis s.l. are given in Table 8): smooth ventral scales and a small, instead of large, gular pouch, and DNA sequences. – Trapelus m. mutabilis (type locality: Egypt) in – Trapelus tournevillei (type locality: Ouargla, possessing higher scale counts, larger size, and a Algeria) in having a shorter head, a small gular relatively shorter tail (average of ratio TL/SVL pouch, different coloration (e.g. no longitudinal 1.39 in T. mutabilis instead of 1.19 in T. boehmei lines on the belly) and smooth ventral scales, sp. nov.; for details see Table 7), and DNA instead of keeled ventral scales. sequences. – Trapelus m. pallidus (type locality: southern Egypt) Trapelus boehmei sp. nov. differs from the following in having homogeneous scalation on the upper synonyms (A. aspera is a probably valid taxon but hindlimb and base of the tail, and in having a clearly different to the herein-described new species): greater proportion of enlarged body scales and all dorsal scales keeled instead of only the enlarged – Agama inermis Reuss, 1833 (type locality: southern ones, and DNA sequences. Egypt) in possessing a lower proportion of slightly – Trapelus m. poppeki ssp. nov. (type locality: Libya: enlarged scales, only one row of precloacal scales, east of Tarbu) in not possessing enlarged vertebral and a nonvisible tympanum. scales, a lower count of scale rows around midbody – Agama gularis Reuss, 1833 (type locality: southern and a smaller size. Egypt) in possessing heterogeneous scales and a – Trapelus schmitzi (type locality: Ennedi Mts., dorsal crest. Chad) in not possessing dorsal scales equal in size, – Agama latastii Boulenger, 1885 (type locality: Egypt) with only few intermixed larger scales. in lacking equal sized, rhomboidal dorsal scales.

Figure 9. Holotype (ZFMK 49751) of Trapelus boehmei sp. nov.

– Agama aspera F. Werner, 1893 (type locality: Alge- Head scales are heterogeneous in size and shape: rian Sahara, between Kef-el-Dhor and Chegga; supraocular scales smooth; parietal scale small, more Biskra-Bordj-Saada; Zab-el-Zig south of El Mer- or less rectangular, surrounded by three enlarged anyer) in possessing no spiny scales and a hetero- scales and four scales of equal size; pineal organ geneous dorsal scalation. visible, piercing the middle of the scale. Posterior to the parietal scale: scales originating from both sides Description of the holotype: Habitus: stout; tail only of the parietal midline have imbrications directed moderately longer than the body; limbs and digits laterally, with their free anterior margins having relatively long. Measurements. Snout-vent length sensory pits. The eyelids have mucronate scales that 107.1 mm; tail length 135.9 mm; head length form a ring. The ear opening is of medium size, about 27.7 mm; head height 15.4 mm; head width 24.7 mm; half of the size of the eye, having a superior margin length of left forelimb 49.3 mm; length of left hind- with five spiny, mucronate scales on both sides; the limb 70.6 mm. Scalation. Nostril sits on the canthus tympanum is sunken but visible. A rudimentary rostralis, piercing the posterior portion of a large, flat nuchal crest is present, consisting of six spiny, mucr- nasal scale; nostril is directed obliquely upwards. onate scales. Gular scales are flat, smooth, with the

Table 8. Selected character values of Trapelus mutabilis s.l.

Trapelus boehmei sp. nov. Trapelus mutabilis T. mutabilis Trapelus pallidus

Morocco Tunisia Egypt Egypt

Snout-vent length, mm Min 108.1 69.7 61.6 61.3 Max 113.7 98.8 74.9 80.2 x 111.5 77.9 69.3 68.9 N 441113 Tail length, mm Min 125.3 96.9 74.8 73.1 Max 134.4 134.5 102.5 98.0 x 129.0 108.6 88.2 90.0 N 341113 Midbody scales Min 103 72 91 105 Max 105 91 97 118 x 104 81 94.7 112.7 N 3667 Cloacal pores Min 12 8 17 14 Max 19 13 20 24 x 16 10 18.7* 19.9† N 48610

*In two rows. †In two to three rows. Min, minimum; Max, maximum. x = average (value in bold). posterior margins being enlarged and slightly imbri- long with long claws, fourth digit longest, approxi- cate; gular scales are equal in size but becoming mately 25% longer than the third digit, digital length smaller on the gular fold. The gular pouch is small. increasing 4-3-2-5-1, plantar scales and subdigital Ventral scales are smooth, slightly imbricate, and lamellae strongly keeled. The hindlimbs are relatively equal in size. Dorsal scales are heterogeneous (larger long, reaching the ear with the tip of the longest digit. scales interspersed amongst a matrix of smaller Coloration in alcohol. Body is pale bluish-grey above, scales), being smooth to keeled, slightly imbricate, larger scales dirty-white, giving the impression of and partly mucronate, with the base of the scales speckled coloration. Tail dirty-white but the concre- being thickened; the intermixed larger scales are two tive annulations of dark bands are visible. Lateral to three times larger than the other scales, keeled, scales and margins of belly are bluish, undersides of mucronate, and strongly raised. Scales on tail the limbs, tail, chest and centre of the belly dirty- strongly keeled, mucronate, and not arranged in white. Throat bluish, with slightly striated margins. whorls. The tail is cylindrical and relatively short – Coloration in life (Fig. 10): Nuptial (seasonal) col- only 27% longer than the snout-vent length. There oration of males resembles the nuptial coloration of T. are two rows of 18 (ten anterior, eight posterior) ﬂavimaculatus from Arabia. Males get a more or less precloacal pores. Forelimbs have strongly keeled complete blue and additionally white speckled body scales on the upperside, becoming smooth to the and a uniform blue throat while head and belly underside, homogeneous in size; digits are long with remain in normal coloration; the tail becomes orange long claws, fourth digit longest, digital length increas- (see Schleich et al., 1996: plate 21, ﬁg. 61). Pregnant ing 4-3-2-5-1, plantar scales and subdigital lamellae and normal coloration in females is unknown. are strongly keeled. Hindlimbs have strongly keeled Variations: The adult male paratypes are more or and slightly mucronate scales on the upperside, less concordant with the characters outlined for the becoming smooth and nonmucronate to the underside, holotype, but show more distinctly barred tails and scales on the upperside are homogeneous in size, striped throats. Some voucher specimens show becoming smaller on the underside; digits are very enlarged vertebral matrix scales, more or less as large

chungsmuseum A. Koenig, for his considerable and invaluable contributions to African herpetology.

Distribution: Trapelus boehmei sp. nov. probably has a broad distribution in north-western Africa. The holotype and some paratypes were collected between Akka and Icht in Morocco, and the images presented by Schleich et al. (1996: no. 61, pl. 21) and Geniez et al. (2004; no. 94) show specimens from Erfoud and Oued Mird near Ikhf-n-Ouaroun, respectively. Other Moroccan vouchers are known from 40 km north of Zagora (ZSM 52277), 10 km south-east of Goulmima (ZSM 207/1993), 25 km west of Tissint (ZSM 225/ 1993) and Ksar es Souk (ZSM 688/1979/1-5). An addi- Figure 10. Live male of Trapelus boehmei sp. nov. of tional voucher in the ZFMK collection is from Colomb the ZFMK-type series from the type locality. Béchar (Algeria) and can be conﬁdently assigned to T. boehmei sp. nov. (ZFMK 49664). One of the paratypes as the intermixed scales. Other material. One small was collected 220 km south of Nouadhibou on the male (SVL 84.3 mm) from Algeria (ZFMK 49664) main road to Nouakchott in northern Mauritania. All mostly shows the coloration described above, but only these specimens indicate that the new species has a with a striped throat instead of the uniform blue one distribution from Algeria through Morocco to Mauri- of the type series and lacking the uniform brilliant tania (Fig. 11). Therefore, it is most probable that T. blue coloration with white dots. This coloration seems boehmei sp. nov. is a widespread species in north- to represent the nonbreeding coloration. western Africa.

Relations: We compared again the molecular uncor- TRAPELUS SAVIGNII (DUMÉRIL &BIBRON, 1837) rected 16S pairwise sequence divergences between the North African taxa of Trapelus and the newly 1837 Agama savignii Duméril & Bibron, Erpétol. described taxon: T. boehmei sp. nov. – T. m. Gén. 4: 508. – Terra typica: Egypt, El Arish. mutabilis = 3.23–3.37%; T. m. mutabilis – T. m. pallidus = 1.41%; T. boehmei sp. nov. – T. m. Neotype: ZFMK 77470 (Fig. 12). pallidus = 2.63–2.76%; T. boehmei sp. nov. – T. boehmei sp. nov. = 0.22%; T. boehmei sp. nov. – T. Diagnosis: Medium-sized Trapelus [largest known savignii = 6.65–7.01%; T. m. mutabilis – T. savig- voucher from Egypt SVL 123 mm (Anderson, 1898)] nii = 5.65%; T. m. pallidus – T. savignii = 6.45% (see with an average ratio TL/SVL of 1.3. Gular pouch well Table 5). Here again the molecular analyses clearly developed. Dorsal scales relatively uniform with support the morphological results as they corroborate intermixed larger scales. Ventral scales keeled. the full distinctiveness of the new species from the Usually vertebral scales slightly larger than the other Trapelus species (Fig. 4). scales on the flanks. Coloration uniformly sandy grey with five brown transverse bands, which are inter- Habitat: Detailed habitat preferences of this species rupted by a yellowish stripe and whitish lines on the remain unclear. The image shown in Schleich et al. body and a barred tail. Additionally two transverse (1996) refers to a stony desert or semi-desert with bands are on the interorbital area. Adult males get a little vegetation. Additionally, the image by Geniez characteristic coloration under nuptial conditions: et al. (2004) shows a bare stony soil, lacking vegeta- throat and flanks bright to violet blue, the flanks with tion. Trapelus mutabilis favours open, dry country interspersed white spots. Additionally, pregnant with precipitation under 250 mm (Schleich et al., females have a special coloration, with dorsal bands 1996), for example coastal plains, semi-desert, erosion becoming brick red. terraces, and steppes up to 1500 m. In such habitats, individuals are known to stay close to shelter, such as Taxonomic note: Saleh (1997) synonymized T. savignii rocks or small bushes. Similar habitat preferences of with T. flavimaculatus but failed to explain his T. boehmei sp. nov. can be assumed. reasons for this specific taxonomic step. Therefore he was not followed by subspecific authors (e.g. Baha el Etymology: This new species is dedicated to Prof. Dr Din, 2006). Wolfgang Böhme, former Curator of Herpetology and Audouin (1827) also described a ‘Trapelus savignyi’ former Deputy Director at the Zoologisches Fors- but this taxon was recognized as a synonym of the

Figure 11. Distribution of Trapelus boehmei sp. nov. Morocco: 1 = between Akka and Icht (ZFMK 49751–754); 2 = Oued Mird near Ikhf-n-Ouaroun (Geniez et al. 2004); 3 = Erfoud (Schleich et al., 1996); 6 = 10 km south-east of Goulmima (ZSM 207/1993), and Ksar es Souk (ZSM 688/1979/1-5); 7 = 40 km north of Zagora (ZMB 52277); 8 = 25 km west of Tissint (ZSM 225/1993). Algeria: 4 = Colomb Béchar (ZFMK 49664). Mauritania: 5 = 220 km south of Nouadhibou (MNHN 2006.0343). gekkonid species Stenodactylus sthenodactylus and Diagnosis: A medium-sized, slender Trapelus with Stenodactylus petrii by Anderson (1898). Also Wagner large gular pouch. Head longer than in other African & Crochet (2009) recognized the problem of the two Trapelus species. Dorsal scales equal in size, strongly very similar names and the mixed usage of the names keeled but not mucronate, no intermixed larger by the different authors. Therefore, and because of scales. other reasons outlined in their publication the name was ﬁxed by a neotype by Wagner & Crochet (2009). Taxonomic note: This species was formerly regarded as a subspecies of T. ﬂavimaculatus. The holotype is TRAPELUS TOURNEVILLEI (LATASTE, 1880) mentioned as lost from the Paris collection (MNHN) 1880 Agama tournevillei Lataste, Le Naturaliste, by Brygoo (1988), but present in the London collection Paris, 2: 325. – Terra typica: Ouargla (Wargla?), (BMNH). The clear distinctness of this species Algérie. is supported by many authors (e.g. Schleich et al., 1996; Sindaco & Jeremcˇenko, 2008) and in this Holotype: BMNH 1920.1.20.1241. publication.

Figure 12. Neotype (ZFMK 77470) of Trapelus savignii Duméril & Bibron, 1837.

TRAPELUS AGNETAE (WERNER, 1929) STAT. NOV. surface of lower leg and basis of tail heterogeneous. 1929 Agama agnetae Werner, Zool. Anz., Leipzig Differs from T. pallidus in having a fringe of three to 81:329. – Terra typica: Bir Molusi zwischen Dam- four distinct spines situated on the upper edge of the askus und Bagdad. ear opening. Dorsal scales small, equal in size, 1971 Agama pallidus haasi Werner, Bull. Brit. Mus. forming a matrix with intermixed larger scales. 21: 213. – Terra typica: Azraq in Transjordan. Ventral scales usually smooth.

Holotype: NMW 23349. Taxonomic note: As it is mentioned in the introduction, T. agnetae was formerly known as a synonym of Diagnosis: Small to medium sized member of the T. pallidus, but Disi et al. (2001) recognized T. agnetae genus. Head longer than broad, limbs relatively long. as identical to Trapelus pallidus haasi described by Y. Gular pouch absent. Ear opening longer than high, Werner (1971) and placed the latter in the synonymy bordered by a row of spiny scales. Scales on dorsal of the former. Nevertheless, because of differences in

KEY TO THE AFRICAN TAXA OF THE GENUS TRAPELUS 1 – Vertebral scales larger than lateral scales, as large as intermixed scales...... 2 – Matrix scales homogeneous in size, with intermixed larger scales; vertebral matrix scales only sometimes nearly as large as intermixed scales; or body scales homogeneous...... 3 2 – Gular pouch absent...... T. m. poppeki ssp. nov. – Gular pouch present...... T. savignii 3 – Gular pouch well developed, body scalation homogeneous...... T. tournevillei – Gular pouch absent, body scalation heterogeneous...... 4 4 – Hindleg and basis of tail scalation heterogeneous; dorsal scalation as a matrix small and smooth homogeneous scales with only few intermixed larger and keeled scales...... T. m. pallidus – Hindleg and basis of tail scalation homogeneous, many intermixed larger scales body scales or homogeneous ...... 5 5 – Dorsal scalation heterogeneous ...... 6 – Dorsal scalation homogeneous ...... T. schmitzi 6 – Dorsal scalation smooth to keeled, heterogeneous in shape and with intermixed larger keeled scales, ventrals smooth. Occiput without spines, ventrals smooth, hindleg and basis of tail scalation homogeneous, small gular pouch in males. Coloration sandy-grey with four to five dark transverse bars, tail barred. Males in nuptial coloration with a blue throat and flanks, females with reddish transverse bars...... T. m. mutabilis – Dorsal scalation keeled, homogeneous in shape, heterogeneous in size (smaller scales intermixed with larger ones), ventrals smooth, hindleg and basis of tail scalation homogeneous. Males in nuptial coloration with blue throat and blue, white speckled body, tail orange; head and belly remain in normal coloration ...... T. boehmei sp. nov. morphology (see Disi et al., 2001), which are also additional sampling or genes will resolve the question. supported by a clear genetic distinctness we follow In contrast to the biometric data, it was possible to Werner’s (1929) decision and regard T. agnetae as full distinguish species with a morphological examination valid species. of fine-scale scalation characters. Our genetic data were correlated to the small morphological differences Remark: This species does not occur in Africa but found amongst species. because of its resurrection it is mentioned here. De Queiroz (1998, 1999, 2007) has introduced his new nomenclatural system ‘Phylocode’. In it, he argued that the descriptions of subspecies are useless, because they DISCUSSION are often not described as monophyletic groups, but TAXONOMY AND SPECIATION IN TRAPELUS rather as colour morphs of more widespread species. The genus Trapelus is a taxonomically complex group, This specific system is still strongly under debate and with numerous taxa still requiring systematic review. has elicited a number of unfavourable comments (e.g. Species complexes have been identified in Trapelus Kraus, 2004; Sluys, Martens & Schram, 2004; Dubois, lineages in the Middle East, in central Asia, and herein 2005; Pickett, 2005a, b, Rieppel, 2006). Several of these in Africa, making this a genus that is inherently latter authors also elucidate the clear advantages of complicated and problematic (Rastegar-Pouyani, 1998, describing subspecies as a useful recognition of natural 2000, 2005; Wagner & Crochet, 2009). Issues with steps in the evolutionary developments of new species morphological similarities amongst populations with (see below). Therefore, we herein followed the high intrapopulational variation and differential levels approved nomenclatural system described in the Inter- of morphological variation between sexes are ongoing national Code of Zoological Nomenclature (ICZN problems in identifying species (Rastegar-Pouyani, 1999), which includes the rank of a subspecies. We 2005). Previous studies (Wagner & Böhme, 2007), plus think that in both nomenclatural systems, it is indis- the current study, have clearly demonstrated that T. putable that full species arise through speciation, mutabilis s.l. is also a species complex, with several which is an ever on-going process and not all taxa or cryptic taxa. Our preliminary phylogenetic results do populations will have completed it. Authors such as not provide enough basal resolution within the T. Dubois (2006) or Bauer et al. (2010) have pointed out mutabilis-complex (T. mutabilis, T. m. pallidus, T. m. the importance of the availability of nomina and the poppeki ssp. nov. and T. boehmei sp. nov.) to answer the need for intrinsic organism attributes (= characters) in question of a true monophyly of the T. mutabilis- taxon descriptions. Therefore, naming also these complex. As there are indications that T. boehmei sp. monophyletic subunits is useful to describe and name nov. forms an independent evolutionary lineage, only evolution in the sense of nomenclature and in their

© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 884–912 908 P. WAGNER ET AL. true evolutionary context (subspecies as developing cific variation in hemipenis structures. However, a evolutionary units). review of hemipenis structure did not find this to be In the herein described subspecies and for T. pal- the case (Böhme, 1988). lidus (now recognized as subspecies of T. mutabilis) Thus far, there have been no complete surveys of characters were identified distinguishing it clearly hemipenis structures in Trapelus. Böhme (1988) from the nominate subspecies. In the case of T. pal- analysed the genital morphology of several agamid lidus, these characters are even supported by many taxa and highlighted similarities between T. san- other authors who distinguished T. pallidus from T. guinolentus and Laudakia tuberculata, which differ mutabilis in the past. It was not possible to recognize significantly from species in Agama, Pseudotrapelus, evidence of clinal effects in any of the subspecies, and Phrynocephalus. Böhme (1988) also found especially in the subspecies T. mutabilis and T. obvious similarities amongst the hemipenial morphol- pallidus with several dozens of examined specimens ogy of Agama, Acanthocercus, and Laudakia (exclud- from all across their distribution range. ing L. tuberculata). These preliminary results suggest The clade that includes the T. mutabilis complex has that genital morphology may show a high level of heterogeneous scales with scattered large tubercle homoplasy and be morphologically conserved in the scales, whereas the T. agilis – T. sanguinolentus Agaminae, providing limited information for resolving species have homogeneous scalation. In addition, T. taxonomic relationships within Trapelus. Conse- mutabilis is currently recognized from Egypt in the quently, it is probable that another mechanism of east to Morocco and Mauritania in the west, but our species recognition exists in the African agamids. results and P.-A. Crochet (pers. comm.) imply that Numerous premating mechanisms of species recog- West African populations probably represent several nition have been identified in lizards, including body new species. Our genetic results also indicate that T. coloration. For example, dominant males in many agilis Olivier, 1807 is polyphyletic, which suggests that species of the genus Agama have brilliant secondary this is also a cryptic species complex. Thus, further sexual coloration that clearly distinguishes species work is required on this group, both genetically and (Loveridge, 1933; Thys van den Audenaerde, 1963; morphologically, to determine the taxonomic status of McLachlan, 1981; Wagner, 2007, Wagner, Burmann & the constituent lineages, including T. sanguinolentus. Böhme, 2008; Wagner, Krause & Böhme, 2008). These Although we were able to identify some fine-scale species live in colonies with one dominant male. In morphological differences amongst species, the most contrast, some of the southern African species of the obvious and identifiable diagnostic character is male genus lack this coloration (e.g. Agama hispida, nuptial coloration. However, this coloration in Trape- Agama aculeata, Agama armata) and are believed to lus is transitory and only occurs during the breeding be solitary-living, nonterritorial species (Branch, season. Thus, other diagnostic characters will allow 1998; Spawls et al., 2002). Like Trapelus, these the identification of species throughout the year. For agamid lizards also lack a conspicuous permanent example, genital morphology is a useful taxonomic colour pattern and only show a seasonal male colora- character in lizards (Branch, 1981; Klaver & Böhme, tion. Trapelus species are also solitary living and 1986; Böhme, 1988; Böhme & Ziegler, 2008). territorial only during the reproductive period, with Hemipenial structures have been particularly useful males showing temporary breeding colorations (Schle- for determining evolutionary lineages (Böhme, 1988; ich et al., 1996). Thus, in African agamids there may Ziegler & Böhme, 1997; Böhme & Ziegler, 2008) within be a complex evolutionary relationship between male the Chamaeleonidae, which is the sister lineage to the coloration and life-history traits, which means that Agamidae and together they form the Acrodonta (e.g. using such characters to resolve taxonomic issues Dowling & Duellman, 1978; Estes & Pregill, 1988; within Trapelus may prove difficult. Joger, 1991, Macey, Schulte II & Larson, 2000). For Delineation of species in Trapelus is more difficult example, the horned chameleons have similar hemipe- than in Agama because the male breeding colours are nial structure, whereas lineages lacking horns have only temporary and morphological variation within very distinct hemipenes (Böhme & Klaver, 1980; single populations tends to be relatively high. Thus, Klaver & Böhme, 1986). Therefore, it can be hypoth- at this time it is difficult to theorize about the evolu- esized that species recognition in horned chameleons is tionary processes of T. boehmei sp. nov. within Trape- related to body ornamentation, whereas in the species lus. We found that this new species has only a few lacking horns hemipenis structure reinforces species similarities to T. schmitzi, T. savignii, and T. tournev- boundaries. illei, and no clear similarities to T. m. pallida, T. m. African agamids, unlike chameleons, are particu- poppeki ssp. nov., or T. mutabilis s.s. Additionally, we larly conservative in body form, with very little varia- found that T. boehmei sp. nov. exhibited some mor- tion in body ornamentation. Thus, it might be phological similarities to cryptic taxa within the T. expected that there would be high levels of interspe- mutabilis complex but more data will clarify the

© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 884–912 REVIEW OF TRAPELUS FROM NORTHERN AFRICA 909 status of these taxa. For instance, some smaller males 9 Mya. At this period of time the Rif and Betic Moun- from Algeria resemble adult males of T. boehmei sp. tains were islands and the lower parts of northern nov. in coloration but differ in aspects of scalation. Africa and Arabia were flooded. These processes prob- These species probably represent so far undescribed ably led to the divergence between western and (sub)species. Thus, our taxonomic review highlights eastern Trapelus populations (De Jong, 1998). The the importance of undertaking a detailed phyloge- historical split of the T. mutabilis clade from other netic study of all species and biogeographically impor- species of the genus is from this period. 5.5 to 6.0 Mya tant populations within African Trapelus.In the Mediterranean lost the contact to the Atlantic and particular, a phylogeographical study of this genus began to dry out for a period of 0.5 Myr. This resulted will be important in allowing an assessment of the in several colonization events (Brown et al., 2002) and variation within species across their distributions. probably speciation. Such a study should fully resolve outstanding issues We estimated the age of Trapelus in northern Africa of cryptic taxa within T. mutabilis. to be late Miocene (6.3 Mya), using relaxed molecular clock analyses. This result is similar to other xeric species groups of this area. A number of studies has BIOGEOGRAPHICAL HISTORY OF TRAPELUS MUTABILIS found that a wide range of reptile taxa, including The estimated age of Trapelus (21.7 Mya) indicates skinks, snakes, and geckos date back to the late that this is an old genus, probably originating in the Miocene – early Pliocene (Carranza, Arnold & Plegu- early Miocene. The two lineages of the T. mutabilis ezuelos, 2006; Geniez & Arnold, 2006; Carranza et al., complex (1. T. mutabilis, T. m. pallidus, T. m. poppeki 2008). These estimated dates correlate with the ssp. nov.; and 2. T. boehmei sp. nov.) are relatively estimated age of the Saharan desert. Goudie (2003) young, dating back to the late Miocene and Plio- suggested that the recent hyperarid phase is a com- Pleistocene, respectively. paratively recent phenomenon about 1–2 Myr old but It is probable that there has been more than one Aeolian sand and dust occurring in deep seas of the dispersal event of Trapelus into northern Africa. This Atlantic Ocean suggest earlier stages of dryness. is supported by morphology, as the African taxa are Schuster et al. (2006) found fossil sand dunes of about arranged in two distinct clades with T. savignii/T. 7 Myr old deep in the present Sahara (Chad), inter- tournevillei as one group and the T. mutabilis complex spersed with more mesic strata. Thus, significant as the other. The most remarkable morphological climate changes during the late Miocene could have difference between the two clades is the development driven speciation events in Trapelus. of a gular pouch in males. In T. mutabilis, T. agilis, In conclusion, our review of the northern African and ‘T. sanguinolentus’ a gular pouch is lacking, Trapelus lizards, focusing on the T. mutabilis whereas males of T. savignii and T. tournevillei have complex, has provided a solid foundation for future a well-developed gular pouch. However, T. savignii phylogeographical and evolutionary research. There occurs in northern Africa in Egypt only, but T. has been a complex interaction amongst climate tournevillei occurs in both Algeria and Tunisia and changes since the Miocene, speciation, and morpho- therefore a second lineage of Trapelus species is logical evolution in this genus. present in northern Africa. Broadly, the mechanisms of speciation in North Africa are relatively unknown. A number of studies ACKNOWLEDGEMENTS has looked at the role of biogegraphical barriers in speciation of North African fauna. As far back as We are thankful to Wolfgang Böhme for his support Wagner (1841) such mechanisms have been discussed. and discussions. We thank Adam Leaché who contrib- He highlighted rivers and mountain systems in north- uted some Trapelus sequences. We are grateful to ern Africa (Algeria) as limits to distributions and Sven Mecke for his contributions to scale counts. suggested mechanisms of speciation of beetles and Ulrich Joger, Colin McCarthy, Michael Kroniger, Felix small mammals. These observations were the basis of Hulbert, Wolfgang Bischoff, and particularly Aaron his concept of ‘speciation by isolation’ (Wagner, 1889), Bauer provided information on type specimens, which he published in many articles shortly after images, and historical literature. Specimens were pro- Darwin’s ‘Origin of species’. Recently, the Moroccan vided by Frank Glaw (ZSM, Munich, Germany), Atlas Mountains have been identified as an important Jakob Hallermann (ZMH, Hamburg, Germany), Ivan mountain system in speciation (Brown & Znari, 1998; Ineich (MNHN, Paris, France), Gunther Köhler (SMF, Brown, Suárez & Pestano, 2002; Fritz et al., 2005). Frankfurt, Germany), and Mark-Oliver Rödel (ZMB, De Jong (1998) summarized biogeographical pat- Berlin, Germany). P. W. is especially grateful to terns in northern Africa and referred to an opening of Michael Barej for fruitful ‘office’ discussions on the Mediterranean to the Atlantic between 7 and nomenclature and naming new species.

REFERENCES evidence from mtDNA evolution in the Agamid lizard Agama impalearis. Molecular Phylogenetics and Evolution Andersson LG. 1935. Reptiles and Batrachians from the 24: 324–332. Central Sahara. Göteborgs Kungliga Vetenskaps och Brown RP, Znari M. 1998. Geographic variation in Agama Vitterhets-Samhället Handlingar 4: 1–19. impalearis from Morocco: evidence for historical population Anderson J. 1898. Zoology of Egypt, Vol. l. Reptilia and vicariance and current climatic effects. Ecography 21: 605– Batrachia. B. Quaritch, London. 612. Audouin JV. 1827. Explication sommaire des planches de Brygoo ÉR. 1988. Les types d’Agamidés (Reptiles, Sauriens) Reptiles (supplément)...offrantunexposédescaracteres du Muséum national d’Histoire naturelle. Catalogue cri- naturelles des genres, avec la distinction des especes, tique. Bulletin du Muséum National d’Histoire Naturelle 4 Description de l’Égypte, ou Recueil des Observations et des sér. 10: 1–56. Recherches qui ont été faites en Égypte pendant Carranza S, Arnold EN, Geniez P, Roca J, Mateo JA. l’Expedition de l’Armée Française, publie par les Ordres de 2008. Radiation, multiple dispersal and parallelism in the sa Majesté l’Empereur Napoléon le Grand. Histoire skinks, Chalcides and Sphenops (Squamata: Scincidae), Naturelle. Volume 1 (Histoire Naturelle), No. 4. Commision with comments on Scincus and Scincopus and the age of the d’Egypt, Paris, 161–184. Sahara Desert. Molecular Phylogenetics and Evolution 46: Baha el Din S. 2006. A guide to the reptiles and amphibians 1071–1094. of Egypt. Cairo: The American University in Cairo Press. Carranza S, Arnold EN, Pleguezuelos JM. 2006. Phylog- Barts M. 1997. Agaminae. In: Barts M, Wilms TM. eds. eny, biogeography and evolution of the two Mediterranean Catalogue of valid Species and Synonyms. A Bibliographic snakes Malpolon monspessulanus and Hemorrhois hippocre- Reference, Vol. 4, Agamidae, Herpint International, Bredell, pis (Squamata, Colubridae), using mtDNA sequences. South Africa, 416 pp. Molecular Phylogenetics and Evolution 40: 532–546. Bauer AM, Parham JF, Brown RM, Stuart BL, Grismer Cuvier GLCFD. 1817. Le règne animal distribué d’après son L, Papenfuss TJ, Böhme W, Savage JM, Carranza S, organisation, pour servir de base à l’histoire naturelle des Grismer JL, Wagner P, Ananjeva NB, Inger RF. 2010. animaux et d’introduction à l’anatomie comparée. Avec On the availability of new Bayesian-delimited gecko names figures, dessinées d’après nature. Tome II, contenant les and the importance of character-based species descriptions. reptiles, les poissons, les mollusques et les annélides. Paris: Proceedings of the Royal Society of London Series B 278: Deterville. 490–492. doi: 10.1098/rspb.2010.1330. Cuvier GLCFD. 1829. Le Regne Animal Distribué, d’apres Böhme W. 1988. Zur Genitalmorphologie der Sauria: Funk- son Organisation, pur servir de base à l’Histoire naturelle tionelle und stammesgeschichtliche Aspekte. Bonner Zoolo- des Animaux et d’introduction à l’Anatomie Comparé, Nou- gische Monographien 27: 1–176. velle Edition [second edition]. Vol. 2. Les Reptiles. Déter- Böhme W, Klaver CJJ. 1980. The systematic status of ville, Paris, i–xvi, 1–406. Chamaeleo kinetensis Schmidt, 1943 (Sauria: Chamaele- De Jong H. 1998. In search of historical biogeographic pat- onidae) from the Imatong Mountains, Sudan, with com- terns in the western Mediterranean terrestrial fauna. Bio- ments on lung and hemipenial morphology within the logical Journal of the Linnean Society 65: 99–164. C. bitaeniantus-group. Amphibia-Reptilia 1: 3–17. Disi AM, Modrý D, Neças P, Rifai L. 2001. Amphibians Böhme W, Ziegler T. 2008. A review of iguanian and and reptiles of the Hashemite Kingdom of Jordan. Frankfurt anguimorph lizard genitalia (Squamata: Chamaeleonidae; am Main: Edition Chimaira. Varanoidea, Shinisauridae, Xenosauridae, Anguidae) and Doumergue F. 1901. Essai sur la Faune Erpétologique their phylogenetic significance: comparisons with molecular de l’Oranie. Bulletin de la Société de Géographie et data sets. Journal of Zoological Systematics and Evolution- d’Archéologie d’Oran 19-21: 1–404. ary Research 47: 189–202. Dowling HG, Duellman WE. 1978. Systematic herpetology: Boulenger GA. 1885. Catalogue of the Lizards in the British a synopsis of families and higher categories. New York: HISS Museum (Nat. Hist.) I. Geckonidae, Eublepharidae, Uro- Publications. platidae, Pygopodidae, Agamidae. London: British Museum Drummond AJ, Ho SYW, Phillips MJ, Rambaut A. 2006. of Natural History, 450 pp. Relaxed phylogenetics and dating with confidence. PLoS Branch WB. 1981. Hemipenes of the Madagascan boas Acra- Biology 4: e88. nthophis and Sanzinia, with a review of hemipeneal mor- Drummond AJ, Rambaut A. 2003. BEAST v1.0. Available phology in Boidae. Journal of Herpetology 15: 91–99. at http://beast.bio.ed.ac.uk Branch WB. 1998. Field guide to snakes and other reptiles of Dubois A. 2005. Proposed rules for the incorporation of Southern Africa. Cape Town: Struik Publishers. nomina of higher-ranked zoological taxa in the Interna- Brandley MC, Schmitz A, Reeder TW. 2005. Partitioned tional Code of Zoological Nomenclature. 1. Some general Bayesian analyses, partition choice, and the phylogenetic questions, concepts and terms of biological nomenclature. relationships of Scincid lizards. Systematic Biology 54: 373– Zoosystema 27: 365–426. 390. Dubois A. 2006. Naming taxa from cladograms: a cautionary Brown RP, Suárez NM, Pestano J. 2002. The Atlas moun- tale. Molecular Phylogenetics and Evolution 42: 317–330. tains as a biogeographical divide in North-West Africa: Duméril AMC, Bibron G. 1837. Erpétologie Générale ou

Histoire Naturelle Complete des Reptiles. Vol. 4. Paris: Libr. zoologischen Museums der Königliche Universität zu Berlin Encyclopédique Roret, 570 pp. nebst Beschreibung vieler bisher unbekannter Arten von Estes R, Pregill G, eds. 1988. Phylogenetic relationships of Säugethieren, Vögeln, Amphibien und Fischen. Berlin: T. the lizard families. Stanford, CA: Stanford University Press. Trautwein, 118 pp. Evans SE, Prasad GVR, Manhas BK. 2002. Fossil lizards Loveridge A. 1933. Reports on the scientific results of an from the Jurassic Kota Formation of India. Journal of expedition to the southwestern highlands of Tanganika Ter- Vertebrate Paleontology 22: 299–312. ritory. VII Herpetology. Bulletin of the Museum of Compara- Fritz U, Fritzsch G, Lehr E, Ducotterd JM, Müller A. tive Zoolology 74: 197–416. 2005. The Atlas Mountains, not the strait of Gibraltar, as a Macey JR, Schulte JA II, Larson A. 2000. Evaluating biogeographic barrier for Mauremys leprosa (Reptilia: Trans-Tethys Migration: An Example Using Acrodont Lizard Testudines). Salamandra 41: 97–106. Phylogenetics. Systematic Biology 49: 233–256. Geniez P, Arnold EN. 2006. A new species of the Semaphore McLachlan GR. 1981. Taxonomy of Agama hispida (Sauria: gecko Pristurus (Squamata: Gekkonidae) from Mauritania, Agamidae) in southern Africa. Cimbebasia 5: 220–227. represents a 4700 km range extension. Zootaxa 1317: Merrem B. 1820. Versuch eines Systems der Amphibien – 57–68. Tentamen Systematis Amphibiorum. Marburg: J. C. Kriegeri. Geniez P, Mateo JA, Geniez M, Pether J. 2004. The Moody SM. 1980. Phylogenetic and historical relationships of amphibians and reptiles of the Western Sahara. Frankfurt the genera in the family Agamidae (Reptilia: Lacertrilia). am Main: Edition Chimaira. Unpublished PhD thesis, University of Michigan. Geoffroy de Saint-Hilaire E. 1809. Description des reptiles. Moody SM, Böhme W. 1984. Merkmalsvariation und tax- In: Savigny MJCL de, ed. Description d’Égypte. Vol. L. onomische Stellung von Agama doriae Boulenger, 1885 und Édition impériale, 2. Ser., 1. Paris: Nouveau Bulletin des Agama benueensis Monard, 1951 (Reptilia: Agamidae) aus Sciences, Société Philomathique de Paris, 1–366. dem Sudangürtel Afrikas. Bonner Zoologische Beiträge 35: Geoffroy de Saint-Hilaire E. 1827. Description des reptiles. 107–128. In: Savigny MJCL de, ed. Description d’Égypte. Vol. L. Nylander JAA. 2008. MrModeltest v2.3. Program distributed Deuxième édition. Paris: Panckoucke, 121–160 (115– by the author. Available at http://www.ebc.uu.se/systzoo/ 184). staff/nylander.html Goudie AS. 2003. Great warm deserts of the world; land- Padial JM. 2006. Commented distributional list of the scapes and evolution. Oxford: Oxford University Press. reptiles of Mauritania (West Africa). Graellsia 62: 159–178. Grandison AGC. 1968. Nigerian lizards of the genus Agama Palumbi SR, Martin A, Romano S, McMillan WO, Stice (Sauria: Agamidae). Bulletin of the British Museum of L, Grabowski G. 1991. The simple fool’s guide to PCR. Natural History Zoology 17: 67–90. Hawai: Department of Zoology and Kewalo Marine Hall TA. 1999. BioEdit: a user-friendly biological sequence Laboratory. alignment editor and analysis program for Windows 95/98/ Pasteur G, Bons J. 1960. Catalogue des reptiles actuels du NT. Nucleic Acids Symposium Series 41: 95–98. Maroc. Travaux de l’Institute Scientifique Chérifien, Série Ineich I. 2001. Reptiles & Amphibiens de la République de Zoologique 21: 1–132. Djibouti. Internal report to the Ministére de l’habitat, de Pickett KM. 2005a. The new and improved PhyloCode, now l’urbanisme, de l’environment et de l’aménagement du ter- with types, ranks, and even polyphyly: a conference report ritoire bureau national de la diversité biologique, Djibouti. from the First International Phylogenetic Nomenclature International Commission on Zoological Nomenclature Meeting. Cladistics 21: 79–82. (ICZN). 1999. International code of zoological nomencla- Pickett KM. 2005b. Is the PhyloCode now roughly analogous ture, 4th edn. London: The International Trust for Zoological to the actual codes? A reply to Laurin et al. Cladistics 21: Nomenclature. 608–610. Joger U. 1991. A molecular phylogeny of agamid lizards. de Queiroz K. 1998. The general lineage concept of species, Copeia 1991: 616–622. species criteria, and the process of speciation. In: Howard Joger U. 2003. Reptiles and amphibians of southern Tunisia. DJ, Berlocher SH, eds. Endless forms: species and Kaupia 12: 71–88. speciation. New York, NY: Oxford University Press, 57– Joger U, Lambert MRK. 1996. Analysis of the herpetofauna 75. of the Republic of Mali, I. Annotated inventory, with descrip- de Queiroz K. 1999. The general lineage concept of species tionofanewUromastyx (Sauria: Agamidae). Journal of and the defining properties of the species category. In: African Zoology 110: 21–51. Wilson RA, ed. Species: new interdisciplinary essays. Cam- Klaver CJJ, Böhme W. 1986. Phylogeny and classification of bridge, MA: Massachusetts Institute of Technology Press, the Chamaeleonidae (Sauria) with special reference to 49–89. hemipenis morphology. Bonner Zoologische Monographien de Queiroz K. 2007. Species concepts and species delimita- 22: 1–64. tion. Systematic Biology 56: 879–886. Kraus O. 2004. Phylogeny, classification and nomenclature: a Rastegar-Pouyani N. 1998. Systematics and distribution of reply to F. Pleijel and G.W. Rouse. Journal of Zoological the Iranian species of Trapelus (Sauria: Agamidae) a review. Systematics and Evolutionary Research 42: 159–161. Russian Journal of Herpetology 5: 127–146. Lichtenstein MHC. 1823. Verzeichnis der Doubletten des Rastegar-Pouyani N. 2000. Taxonomic status of Trapelus

ruderatus (Olivier) and T. persicus (Blandford), and validity Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, of T. lessonae (De Filippi). Amphibia-Reptilia 21: 91–102. Higgins DG. 1997. The ClustalX windows interface: flex- Rastegar-Pouyani N. 2005. A multivariate analysis of geo- ible strategies for multiple sequence alignment aided by graphic variation in the Trapelus agilis complex (Sauria: quality analysis tools. Nucleic Acids Research 24: 4876– Agamidae). Amphibia-Reptilia 26: 159–173. 4882. Reuss A. 1834. Zoologische Miscellen, Reptilien. Abhandlun- Thys van den Audenaerde DFE. 1963. Les Agamidae du gen aus dem Gebiete der beschreibenden Naturgeschichte. Congo: les espèces et leur distribution géographique. Revue Museum Senckenbergianum 1: 27–62. Zoologie et de Botanique de Africaines 68: 203–250. Rieppel O. 2006. The PhyloCode: a critical discussion of its Townsend TM, Larson A. 2002. Molecular phylogenetics theoretical foundation. Cladistics 22: 186–197. and mitochondrial genomic evolution in the Chamaele- Rieppel O, Walker A, Odhiambo I. 1992. A preliminary onidae (Reptilia, Squamata). Molecular Phylogenetics and report on a fossil chamaeoleonine (Reptilia: Chamaeleoni- Evolution 23: 22–36. nae) skull from the Miocene of Kenya. Journal of Herpetol- Wagner M. 1841. Reisen in die Regentschaft Algier in den ogy 26: 77–80. Jahren 1836, 1837 und 1838. Leipzig: Drei Bände. Robinson MD, Van Devender TR. 1973. Miocene Wagner M. 1889. Die Entstehung der Arten durch räumliche lizards from Wyoming and Nebraska. Copeia 1973: 698–704. Sonderung. Basel. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian Wagner P. 2007. Studies in African Agama I: on the taxo- phylogenetic inference under mixed models. Bioinformatics nomic status of Agama lionotus usambarae Barbour & Lov- 19: 1572–1574. eridge, 1928. Herpetozoa 20: 69–73. Saleh MA. 1997. Amphibians and reptiles of Egypt. Publica- Wagner P, Böhme W. 2007. A new species of the genus tion of the National Biodiversity Unit, no. 6. Cairo: Egyp- Trapelus Cuvier, 1816 (Squamata: Agamidae) from arid tian Environmental Affairs Agency, 283. central Africa. Bonner Zoologische Beiträge 55: 81–87. Schleich HH, Kästle W, Kabisch K. 1996. Amphibians and Wagner P, Burmann A, Böhme W. 2008. Studies on African reptiles of North Africa. Koenigstein: Koeltz Scientific Agama II. Resurrection of Agama agama kaimosae Lover- Books. idge, 1935 (Squamata: Agamidae) from synonymy and its Schmitz A. 2003. Taxonomic and phylogenetic studies on elevation to species rank. Russian Journal of Herpetology scincid lizards (Reptilia: Scincidae). Unpublished PhD 15: 1–7. thesis, University of Bonn. Wagner P, Crochet PA. 2009. The status of the nomina Schmitz A, Brandley MC, Mausfeld P, Vences M, Glaw F, Trapelus savignyi Audouin, 1827 and Agama savignii Nussbaum RA, Reeder TW. 2005b [2004]. Opening the Duméril & Bibron, 1837 and the valid nomen of the black box: phylogenetics and morphological evolution of the Savigny’s Agama (Sauria: Agamidae). Zootaxa 2209: 57– Malagasy fossorial lizards of the subfamily ‘Scincinae’. 64. Molecular Phylogenetics and Evolution 34: 118–133. [DOI Wagner P, Krause P, Böhme W. 2008. Studies on African 10.1016/j.ympev.2004.08.016]. Agama III. Resurrection of Agama agama turuensis Lover- Schmitz A, Ineich I, Chirio L. 2005a. Molecular review of idge, 1932 (Squamata: Agamidae) from synonymy and its the genus Panaspis sensu lato in Cameroon, with special elevation to species rank. Salamandra 44: 35–42. reference to the status of the proposed subgenera. Zootaxa Wagner P, Wilms TM, Schmitz A. 2008. First record of 863: 1–28. Trapelus schmitzi Wagner & Böhme 2007 (Sauria: Agami- Schmitz A, Mausfeld P, Embert D. 2004. Molecular studies dae) from Algeria. Revue Suisse de Zoologique 115: 491– on the genus Eumeces Wiegmann, 1834: phylogenetic rela- 495. tionships and taxonomic implications. Hamadryad 28: Walsh PS, Metzger DA, Higuchi R. 1991. Chelex 100 as a 73–89. medium for simple extraction of DANN for PCR-based Schuster M, Duringer P, Ghienne JF, Vignaud P, typing from forensic material. BioTechniques 10: 506– Mackaye HT, Likius A, Brunet M. 2006. The age of the 513. Sahara desert. Science 311: 821. Wermuth H. 1967. Liste der rezenten Amphibien und Rep- Sindaco R, Jeremcˇenko VK. 2008. The reptiles of the tilien: Agamidae. Das Tierreich 86: 1–127. Western Palearctic. 1. Annotated checklist and distributional Werner F. 1893. Herpetologische Nova. Zoologischer Anzeiger atlas of the turtles, crocodiles, amphisbaenians and lizards 16: 359–363. of Europe, North Africa, Middle East and Central Asia. Werner F. 1929. Beiträge zur Kenntnis der Fauna von Syrien Latina, Italy: Edizioni Belvedere. und Persien. Zoologischer Anzeiger 8: 238–245. Sluys R, Martens K, Schram FR. 2004. The PhyloCode: Werner YL. 1971. Lizards and snakes from Transjordan, naming of biodiversity at a crossroads. Trends in Ecology recently acquired by the British Museum (Natural History). and Evolution 19: 280–281. Bulletin of the British Museum (Natural History) Zoology Spawls S, Howell K, Drewes R, Ashe J. 2002. A field guide 21: 213–256. to the reptiles of East Africa. London: Academic Press. Ziegler T, Böhme W. 1997. Genital structures and mating Swofford DL. 2002. PAUP*: phylogenetic analysis using par- biology in squamate reptiles, especially in platynotans, with simony (*and other methods). Version 4.0b10. Sunderland, remarks on their systematics. Mertensiella 8: 1–207 [in MA: Sinauer Associates. German].