Opening a Box of Cryptic Taxa the First Review of the North African Desert Lizards in the Trapelus Mutabilis Merrem, 1820 Compl
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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. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 884–912. doi: 10.1111/j.1096-3642.2011.00726.x 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: 884 © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 884–912 REVIEW OF TRAPELUS FROM NORTHERN AFRICA 885 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)]. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 163, 884–912 886 P. WAGNER ET AL. 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 recog- nized within T. pallidus, including T. pallidus palli- dus 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 biogeo- graphical 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 descrip- tion. 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