Zootaxa 1363: 23–38 (2006) www.mapress.com/zootaxa/

ISSN 1175-5326 (print edition)

Copyright © 2006 Magnolia Press

ISSN 1175-5334 (online edition)

ZOOTAXA

A review of the systematics of the genus Bradypodion (Sauria: Chamaeleonidae), with the description of two new genera COLIN R. TILBURY 1,4*, KRYSTAL A. TOLLEY 2,4 & WILLIAM R. BRANCH 3 1

No. 2 The Bend, P.O. Box 347, Nottingham Road, 3280, KZN, South Africa. E-mail: [email protected]; [email protected] 2 Molecular Systematics Laboratory, South African National Biodiversity Institute, Kirstenbosch Research Centre, P/Bag X7, Claremont 7735 South Africa. E-mail: [email protected] 3 Port Elizabeth Museum, P.O. Box 13147, Humewood 6013, South Africa. E-mail: [email protected] 4 Evolutionary Genomics Group, Department of Botany and Zoology, University of Stellenbosch, South Africa *Corresponding author

Abstract The taxonomic history and composition of the genus Bradypodion as construed by Klaver & Böhme (1986) and new morphological and molecular data relevant to the taxonomy of the group is reviewed. The combined evidence strongly supports a formal rearrangement of the group into three distinct genera. Bradypodion, type species Chamaeleo pumilus Daudin 1802, is retained for the southern African species. Two new genera are erected to accommodate additional well-diagnosed clades within central and east African species previously referred to Bradypodion. Species of the “fischeri complex” are assigned to Kinyongia gen. nova, whilst the endemic Mulanje chameleon is placed in the monotypic genus Nadzikambia gen. nova. Key words: Chamaeleonidae, Bradypodion, Phylogeny, new genera, mitochondrial and nuclear DNA

Introduction The first species of Bradypodion to be formally described was Chamaeleo pumilus Daudin 1802. Fitzinger (1843) subsequently designated pumilum as the type species for a new genus, Bradypodion. Over the course of the next 133 years, the taxonomy of Bradypodion pumilum and its cogeners underwent a convoluted series of taxonomic shifts including being assigned to two other genera viz: Microsaura and Lophosaura (Grey 1864, Boulenger 1887, Werner 1902, Methuen & Hewitt 1914, Fitzsimons 1943, Loveridge

Accepted by S. Carranza: 5 Oct. 2006; published: 23 Nov. 2006

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1957, Hillenius 1959, Mertens 1966 and Klaver 1973). Raw 1976 and Klaver & Böhme 1997 give good summaries of the taxonomics of the genus. Up until 1976, B. pumilum and all its cogeners were included within the genus Chamaeleo. Finally Raw (1976), citing a number of features purported to be diagnostic for the genus including its unique cranial structure and viviparity, resurrected the genus Bradypodion and assigned all the South African dwarf chameleons to this genus as full species. Klaver & Böhme (1986) after assembling all the currently available information, proposed a systematic revision of the family Chamaeleonidae based largely on hemipenal characteristics, including the available evidence accrued on lung morphology, chromosomal and osteological data. They recognized five genera and two sub-genera, four of these from Africa and three from Madagascar and its adjacent Indian Ocean islands. Although the genus Bradypodion was retained by Klaver & Böhme (1986), they did not consider the diagnostic features of Bradypodion sensu Raw (1976) to be restricted to only South African species. Rather, they expanded the genus to include a group of east and central African chameleons, loosely termed the “fischeri complex” (Hillenius 1959, Böhme & Klaver 1990). This group currently includes Bradypodion fischeri (Reichenow), B. tenue (Matschie), B. uthmoelleri (Müller), B. xenorhinum (Boulenger), B. carpenteri (Parker), B. adolfifriderici (Sternfeld), B. excubitor (Barbour), B. mlanjense (Broadley), B. oxyrhinum Klaver & Böhme, and B. tavetanum (Steindachner). Under this rearrangement, Bradypodion now comprised a morphologically heterogeneous, widespread group of species (Fig. 1) that was acknowledged by Klaver & Böhme (1986) to be undiagnosable by any morphological synapomorphies. Although many authors have adopted the phylogeny of Klaver & Böhme (1986), and most new species descriptions since 1986 by other authors adopted their taxonomic classification (Tilbury 1991, 1998; Lutzmann & Nečas 2002; Nečas et al. 2003; Nečas 2004), the diagnosis and content of Bradypodion remains contested (e.g. Branch 1998). As time has passed and new data has accrued, there is a growing conviction that the inclusion of the central and east African species within an expanded genus Bradypodion is not supported. Whereas in the past the Southern African forms around pumilum were once considered to be at most subspecies of pumilum, there is now good evidence that the genus comprises a monophyletic group of distinct evolutionary taxonomic units (Tolley et al. 2004, 2006; Tolley & Burger 2004).

Evidence Suggesting Nonmonophyly of Bradypodion Some of the morphological attributes of South African Bradypodion are incongruent with northern putative cogeners. All South African Bradypodion have a midline gular crest, usually formed of prominent scaly lobes, whilst none of the described “fischeri complex” possess such ornamentation. Moreover, South African Bradypodion lack rostronasal projections, whilst all except three species of the “fischeri complex” have such features. 24

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The hemipenes of Southern African Bradypodion and the “fischeri complex” essentially display the same plesiomorphic configuration of a calyculate truncus with apical ornamentation based around two pairs of denticulate rotulae. Hemipenial morphology is thus phylogenetically uninformative with respect to relationships between these groups. However, the Mulanje Chameleon, B. mlanjense, the most southerly of the “fischeri complex”, has a unique hemipenal structure (see below).

FIGURE 1. Combined locality map of Bradypodion sensu lato demonstrating geographic distribution patterns of two broad groups within the genus sensu Klaver & Bhme 1986. Red dots indicate records for Southern African Bradypodion and black dots indicate records for the “fischeri complex”. Data locality points are based on specimens from seventeen museum collections.

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Bauer (1997) noted that all species of Southern African Bradypodion have a pigmented parietal peritoneum. He therefore questioned the inclusion of central and east African species, which lack parietal peritoneal pigmentation, within Bradypodion. Furthermore, all South African Bradypodion are viviparous, whilst east and central African species assigned to Bradypodion are oviparous. Although viviparity also exists in several East African chameleons allied to the species around the Chamaeleo (Trioceros) bitaeniatus Fischer and Chamaeleo (Trioceros) werneri Tornier groups (sensu Hillenius 1959), Townsend & Larson (2002) specifically rejected the hypothesis that all viviparous chameleons formed a monophyletic group. Based on mtDNA analysis, they offered strong support for at least two separate origins of viviparity (Townsend & Larson 2002). In all species groups where viviparity occurs (Bradypodion, Chamaeleo (Trioceros) bitaeniatus group, and Chamaeleo (Trioceros) werneri group), or is present in an intermediate phase [e.g. Rhampholeon (Bicuspis) marshalli Boulenger (Humphreys 1990)], this reproductive strategy is always associated with pigmentation of the parietal peritoneum. The internal structure of the lungs of the South African Bradypodion (Type B – Klaver 1981, Klaver & Böhme 1986) is largely similar to that of the east African “fischeri complex”, as well as that of the Malagasy genera Calumma and Furcifer. Essentially the lungs of all these species are small and consist of a relatively simple sac with a varying number of small septae present on the anterior, dorsal, antero-ventral and cephalic walls. The lungs of the South African species, however, lack external appendages or trailing diverticulae, although these are present in most other typical chameleons examined to date. Whilst the presence of a gular pouch has been verified in all species examined of the South African Bradypodion [i.e. damaranum (Boulenger), occidentale (Hewitt), pumilum and ventrale], this accessory respiratory structure is absent in all the species of the “fischeri complex” examined to date (adolfifriderici, fischeri, tenue and xenorhinum; Klaver 1973, 1979, 1981). The marked difference in cranial morphology between the South African Bradypodion and all other typical chameleons has been cited as evidence of a high level of divergence by some authors (Metheun & Hewitt 1914, Raw 1976), but not others (Klaver 1973, Klaver & Böhme 1986). In the South African Bradypodion the lateral crests of the head that extend posteriorly from the supraorbital ridge, form over the lateral edge of the parietal bone, and the temporal crests outline the position of the postfrontal and squamosal bones. In the species of the “fischeri complex”, and as far as can be ascertained in most other species of typical chameleons, the lateral crest of the head is formed along the line of the squamosal bone. As such the lateral crests of the South African Bradypodion are not homologous with the lateral crests of B. fischeri (Reichenow) and other species of typical arboreal chameleons (Raw 1976). The broad parietal bone in South African Bradypodion uniquely recurves posteriorly and on each side has a supra-temporal process which projects inferiorly to make contact with the ascending process of the squamosal bone. In B. fischeri and all other genera of typical chameleons, the parietal bone is narrowed

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posteriorly into a thin sagittal spur that connects at its posterior apex with the squamosal bones. Authors disagree as to whether these cranial features are plesiomorphic (Klaver 1981) or apomorphic (Hillenius 1986, 1988). In iguanids (de Queiroz 1987), e.g. Sphenodon (Rieppel 1992) and Chamaeleo (Rieppel 1993), a broad parietal skull table precedes the ontogenetic development of the narrow parietal condition found in adults, indicating that the broad parietal condition is a plesiomorphic feature and the narrow condition derived. Intergeneric relationships derived from both cladistic analysis of the cranial structure and genetic studies suggest that Brookesia is the sister taxon of all other chameleons. Bradypodion sensu stricto and Brookesia share several cranial features including the broad parietal bearing supratemporal processes and fused nasals (Rieppel 1981, 1987; Rieppel & Crumley 1997). Other observations on the cranial structure of B. pumilum may have taxonomic implications, and include the retention of Jacobsen’s organ (Brock 1941, Malan 1946, Engelbrecht 1950). The dataset for this plesiomorphic character in the Chamaeleonidae is, however, largely incomplete and further discussion is thus deferred. Hofman et al. (1991) examined relationships between purportedly closely related species of chameleons using microcomplement fixation and starch gel electrophoresis of a range of allozymes. They found that the east African taxon B. tavetanum was closer to the Malagasy genus Furcifer than it was to the South African Bradypodion (represented by thamnobates, setaroi (Raw) and melanocephalum) and concluded that there was no support to classify them in the same genus. More recent molecular studies have shown that there are at least two Bradypodion clades that are reciprocally monophyletic and show levels of divergence that are comparable to divergences between other recognised chameleon genera (Townsend & Larson 2002, Tolley et al. 2004.) As the morphological evidence reviewed above does not support the monophyly of Bradypodion, sensu Klaver & Böhme (1986), and since a number of inferences had been made in the literature that the current taxonomy of the genus Bradypodion was flawed, a molecular analysis was conducted with the objective of examining the evolutionary relationships between the East African and South African Bradypodion and all other extant chameleon genera.

Molecular analysis: Materials & methods To determine if taxa currently included within Bradypodion share a close evolutionary history with each other, a phylogenetic analysis of 51 chameleons was run. The analysis included all described forms of east and central African Bradypodion, plus several representatives from each of the other genera of chameleons (Table 1). Sequences from 20 of these individuals have been published previously (Table 1). DNA extraction, PCR amplification, and cycle sequencing of two mitochondrial gene fragments were carried out following standard procedures formerly outlined in Tolley et al. (2004) using the A REVIEW OF BRADYPODION

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following primers for ND2: L4437b (Macey et al. 1997a) and H5934 (Macey et al. 1997b), and 16S: L2510 and H3080 (Palumbi 1996). A 718 bp portion of the nuclear gene RAG1 was amplified and sequenced using primers F118 and R1067 (Matthee et al. 2004). Standard PCR and sequencing were followed for this gene fragment, with PCR annealing temperature at 57°C. All new sequences have been deposited in GenBank (Table 1). Voucher specimens are as listed in Table 1. A Bayesian analysis of 2036 characters from the two mitochondrial genes (ND2, 856 bp and 16S, 462 bp) and the one nuclear gene (RAG1, 718 bp) was run. The outgroup consisted of two other acrodont lizards (Table 1, Agamidae: Leiolepis belliana and Agamidae: Calotes versicolor). The South African Bradypodion have previously been shown to be monophyletic (Tolley et al. 2004) so to reduce computational time, only four representatives from that group were included in the present analysis. Bayesian inference was used to investigate optimal tree space using MrBayes 3.1.0 (Huelsenbeck & Ronquist 2001). Modeltest 3.6 (Posada & Crandall 1998) was run to investigate the evolutionary model that best fits the data set. Both the AIC and LRT test specified the most complex model (GTR+I+G), so MrBayes was run specifying six rate categories with uniform priors for all parameters. Several data partitions were created, and each was allowed to run with separate values for the model parameters. A single data partition was created for 16S, although 24 bases (260–268 and 284–298) were removed due to poor alignment. There were three partitions for ND2: 1st, 2nd, and 3rd codons separately, and three partitions for RAG1: 1st, 2nd, and 3rd codons separately. To ensure the results converged on the same topology, the MCMC was run four times for 5 million generations each, with trees sampled every 100 generations. The first 90k generations (900 trees) were removed as burn-in after examination the average standard deviation of split frequencies (<= 0.004), the convergence diagnostic (PSRF values ~ 1.0) as well as the log-probabilities and the values of each parameter for stabilisation (Ronquist & Huelsenbeck 2005). A 50% majority rule tree was constructed and nodes with > 0.95 posterior probability were considered supported. A parsimony analysis was also run following the procedures outlined in Tolley et al. 2004, and excluded the 24 bases in 16S (as in the Bayesian analysis). One thousand bootstrap replicates were run to evaluate confidence in the nodes. The parsimony analysis (not shown) produced a single tree (5055 steps, CI 0.38, RI 0.55) with the overall same topology and supported nodes (>75% bootstrap) as the Bayesian analysis. Competing phylogenetic hypotheses were tested by comparing the parsimony tree length of the phylogeny presented in this study with 1) the enforced monophyly of the Bradypodion sensu Klaver & Böhme (1986), 2) the enforced monophyly of Bradypodion including only southern and east African taxa, 3) the enforced monophyly of the southern African Bradypodion and the Mulanje taxon. Significance was evaluated with the K-H and S-H tests in PAUP*4.0b10 (Swofford 2002).

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Molecular analysis: Results

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1363 The South African Bradypodion form a strongly supported monophyletic group to the exclusion of all other chameleons, including east and central African Bradypodion (sensu Klaver & Böhme 1986). In addition, the east and central African Bradypodion (sensu Klaver & Böhme 1986) form a monophyletic group with strong support (Fig. 2). This clade includes all species in the “fischeri complex”. A fuller picture of phylogenetic relationships among all known species within this clade utilizing mitochondrial and nuclear genes, will be presented elsewhere (Tolley et al. in prep). Sequence divergences (uncorrected p-distances) between the East and Southern African Bradypodion clades is high for all genes, averaging 20% for ND2, 8% for 16S, and 4% for RAG1 (Table 2). These values of divergence are as high as those found among any other chameleon clades that are currently recognised as genera. Bradypodion mlanjense (sensu Klaver & Böhme 1986) does not fall into either the South African Bradypodion clade, or the east African Bradypodion clade, but forms a separate monotypic clade (Fig. 2). Sequence divergence between it and other clades ranges from 20–27% for ND2, 9 to 15% for 16S, and 4 to 9% for RAG1, which are values as high as those between any other currently established genera. Each of the competing phylogenetic hypotheses enforcing monophyly showed a significantly worse fit (p<0.001 in all cases for both tests) than the topology presented here. Thus the present analysis does not support a monophyletic Bradypodion sensu Klaver & Böhme (1986). There is a basal polytomy for all clades except Brookesia, which is strongly supported as being the sister taxon of the clade comprising this polytomy. This suggests that the relationships among most clades (i.e. genera), excluding Brookesia, are either unresolved at this level of analysis, or that the recognized extant genera radiated within the same time period.

Conclusions The species of the Central and East African Bradypodion “fischeri complex” and the South African Bradypodion form three separate clades based on two mitochondrial and one nuclear gene. They also differ from each other in reproductive physiology, morphologic characters and broad zoogeographical distribution (Fig. 1). To better reflect these evolutionary relationships it is proposed to redefine Bradypodion, type species Chamaeleo pumilus Daudin 1802, and to restrict it to the South African dwarf chameleon clade. Further, to reflect their separate evolutionary lineages, new genera are proposed for species assigned to the East African “fischeri complex” and for the endemic Mulanje chameleon. This division of Bradypodion into three genera (loc hoco) resolves the problem of trying to explain a common recent origin for these groups of chameleons with A REVIEW OF BRADYPODION

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disparate distributions and discordant morphologic and reproductive characters. The marked genetic divergence demonstrated here also underscores the fact that morphologic characters previously used as taxonomic standards, have limited powers of resolution at higher levels of systematics than previously supposed. External morphological synapomorphies for the different genera are still difficult to identify, and for the moment precludes the construction of a Key based on external morphology alone.

FIGURE 2. Bayesian consensus tree for the family Chamaelonidae. The range of posterior probabilites (pp) from 4 independent runs are given on each node (* = 100 pp). Values are not given where nodes are unsupported (<0.95 pp). Sample numbers correspond with Table 1.

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Bradypodion Fitzinger 1843

1363 Type Species: Chamaeleo pumilus Daudin 1802 Composition: B. caffer (Boettger), B. damaranum, B. dracomontanum Raw, B. gutturale (Smith), B. kentanicum (Hewitt), B. melanocephalum, B. nemorale Raw, B. occidentale, B. pumilum, B. setaroi Raw, B. taeniabronchum, B. thamnobates Raw, B. transvaalense (Fitzsimons), B. ventrale, and several as yet undescribed species (Tolley et al. 2005; Branch et al. 2006). Characterization: The monophyly of the South African Bradypodion is established by a suite of nuclear and mitochondrial genes and can also be defined by three characteristics, namely; independently derived viviparity and the associated pigmentation of the parietal peritoneum, and a specific cranial structure with a broad roof-like parietal (interpreted as a retained symplesiomorphy) bearing supra-temporal processes (interpreted as a secondary character reversal Rieppel & Crumley 1997). External morphological features that are common to all Bradypodion include the presence of heterogeneous background scalation, a midline gular crest consisting in most species of composite lobes and cones, and the absence of a ventral crest. Rostronasal processes are absent in all species. The hemipenes are calyculate with a plesiomorphic 4-rotulae apical ornamentation. All species are viviparous. The genus may also be characterized by lung morphology, comprising simple, adiverticulate, sac-like lungs with small ridge-like septae on the cephalic, dorsal and ventral walls and with an accessory gular pouch (Beddard 1997, Klaver 1973, 1881). However, not all Bradypodion species have been assessed. Distribution: Restricted to South Africa, ranging into adjacent Swaziland, and possibly Lesotho and southern Mozambique, with introduced populations in Namibia, and occupying a wide variety of habitats.

Kinyongia genus nova Type Species: Chamaeleo fischeri fischeri Reichenow 1887. Composition: K. adolfifriderici, K. carpenteri, K. excubitor, K. fischeri fischeri, K. fischeri multituberculatum (Nieden), K. fischeri uluguruense (Loveridge), K. tavetanum, K. tavetanum boehmei (Lutzman & Nečas), K. uthmoelleri, K. xenorhinum, K. oxyrhinum, and K. tenue Characterization: The monophyly of Kinyongia is established on the basis of a suite of nuclear and mitochondrial genetic characters. No morphological synapomorphy is known to define all members. Cranial structure has only been studied in K. fischeri (Rieppel & Crumley 1997). The parietal is reduced to a narrow posteriorly projecting sagittal process that meets the ascending squamosal processes at the apex of the casque to completely enclose the temporal fossa. This derived condition is similar to that found in the genera Chamaeleo, Furcifer and Calumma (Rieppel 1981, 1987, Rieppel & Crumley 34

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1997). Scalation is generally of finely heterogeneous granules or flattened polygonal tubercles. In those species that are characterized by a head ornamentation of fused rostronasal projections (carpenteri, xenorhinum, tenue and oxyrhinum), the scalation is generally an unordered heterogeneous mix of tubercles. In species with paired rostronasal projections (fischeri, tavetanum, uthmoelleri) the flanks are adorned with tubercles clustered into “rosettes”, especially on the lower flanks. This rosetting is also seen in the hornless species excubitor. Plantar surfaces are smooth and claws are simple. None of the species have midline gular or ventral crests, occipital lobes, or annulated horns. Cranial ornamentation in some species, e.g. paired rostronasal blade-like horns in fischeri and tavetanum, and fusion of the canthal ridges into a single vertically flattened process in carpenteri, xenorhinum, tenue and oxyrhinum, are similar to features found in the Malagasy genera Calumma and Furcifer. Lung structure is relatively plesiomorphic. They are similar to those of Bradypodion and Malagasy Calumma and Furcifer, being generally simple with a number of small septae on the dorsal, cephalic and ventral walls. The lungs of Kinyongia appear to lack the accessory gular pouch and usually have trailing diverticulae from the posteroinferior surface of the lung (tavetanum, fischeri, tenue, and adolfifriderici) although these are lacking in K. xenorhinum (Klaver 1977, 1981). The lungs in the rest of the species of Kinyongia have not as yet been described. The hemipenes are calyculate with a plesiomorphic 4 rotulae apical ornamentation, and all the species are oviparous. Distribution: Distributed in East Africa with the most westerly species, K. adolfifriderici, extending into the eastern DRC, and K. excubitor reaching as far north as Mount Kenya. They are confined to tropical/sub-tropical forest biomes, often in relict montane or sub-montane forests (Fig. 1). Etymology: This genus is largely confined to the three countries that make up the central east African region namely Kenya, Tanzania and Uganda. The lingua franca for this region is Swahili. The name derives from the generic Swahili name for chameleon “Kinyonga” and identifies it as a genus that is largely confined to Swahili speaking countries. The name is Latinized by terminating the name spelling with the letters ia giving it a feminine gender. Thus the specific names remain unaltered.

Nadzikambia genus nova Type Species: Chamaeleo mlanjensis Broadley 1966 Composition: Nadzikambia mlanjense Characterisation: The monophyly of Nadzikambia is established on the basis of a suite of mitochondrial and nuclear genetic characters and a unique hemipenis. The latter is rather short and stout with a short pedicel and shallow calyces. There are no rotulae on the apex, which are replaced with a pair of large fleshy, papillate lobes with scalloped edges. A REVIEW OF BRADYPODION

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At the sulcal base of each lobe are one or two pedunculated papillae (Klaver & Böhme 1986). The lungs show a structure similar to that of Kinyongia, with two pairs of long diverticulae trailing from the inferior and posterior surfaces of the lung. A series of four small septae alternate with five larger septae across the dorsal wall with several smaller septae arising from the ventral and cephalic walls. There is no gular pouch (Klaver 1977). The parietal peritoneum is unpigmented and reproduction oviparous. The external morphology is largely conservative, and gular and ventral crests are absent. There is a weak dorsal crest, finely heterogeneous scalation that forms rosettes of tubercles on the lower flanks, and a low casque. Although cranial morphology remains undescribed, the external appearance of the cranial crests suggest that the cranium is constructed in the same manner as Kinyongia. Distribution: Only known from sub-montane forest habitats in a few scattered localities on the Mulanje Massif in southern Malawi, Central Africa. Etymology: The name is derived from “Nadzikambe”, the name for chameleon in ChiChewa, the language used by the tribe that lives in the area around Mulanje Mountain in southern Malawi. The name Nadzikambe is Latinised by terminating it with the suffix ia thus giving it a feminine gender.

Acknowledgements The authors would like to acknowledge the significant material contribution and support behind this project of Dr Donald Broadley (Zimbabwe), Professor Kim Howell (University of Dar es Salaam) and Mr Joe Beraducci (Arusha, Tanzania). We would like to thank Laché Rossouw for assistance in the lab, and the South African National Biodiversity Institute for supporting the research. Laboratory support was also given by Conrad Matthee, and additional material was provided by the California Academy of Sciences (USA). The distribution map was kindly provided by Neil Ayres of the De Beers GSC, Johannesburg.

References Bauer, A.M. (1997) Peritoneal pigmentation and generic allocation in the Chamaeleonidae. African Journal of Herpetology, 46, 117–122. Beddard, F.E. (1907) Contributions to the knowledge of the systematic arrangement and anatomy of certain genera and species of Squamata. Proceedings of the Zoological Society of London, 1907, 35–45. Böhme, W. & Klaver, C. J. J. (1990) Zur Kenntnis von Bradypodion uthmoelleri (Mller, 1938). Salamandra, 26, 260–266. Boulenger, G. A. (1887) Catalogue of Lizards in the British Museum (Natural history), III, London.

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Branch, W.R. (1998) Field Guide to the Snakes and other Reptiles of Southern Africa. rev. ed. Struiks Publ., Cape Town, 399pp., 112 col. pls. Branch, W.R., Tolley, K.A., & Tilbury, C.R. (2006) A new Dwarf Chameleon (Sauria: Bradypodion Fitzinger 1843) from the Cape Fold Mountains, South Africa. African Journal of Herpetology, in press. Broadley, D.G. (1965) A new chameleon from Malawi. Arnoldia (Rhod.), 1(32), 1–3. Brock, G.T. (1941) The skull of the chameleon Lophosaura ventralis (Gray): some developmental stages. Proceedings of the Zoological Society (London), 110, 69–137. De Quieroz, K. (1987) Phylogenetic systematics of iguanine lizards. A comparative osteological study. University of California Publication, Zoology, 118, 1–203. Engelbrecht, D.van Z. (1951) Contributions to the cranial morphology of the chameleon Microsaura pumila Daudin. Annals of the University of Stellenbosch, (A), 27, 4–31. FitzSimons, V.F.M. (1943) The Lizards of South Africa, Memoirs of the Transvaal Museum, 1, 1–538. Fitzinger, L.J. (1843) Systema Reptilium Auctore Leopoldo Fitzinger. Vindobonnae (Vienna). Gray, J. E. (1864) Revision of the genera and species of Chamaeleonidae with the description of some new species. Proceedings of the Zoological Society (London), 1864, 465–479. Hillenius, D. (1959) The differentiation within the genus Chamaeleo Laurenti 1768. Beaufortia, 8, 1–92. Hillenius, D. (1986) The relationship of Brookesia, Rhampholeon and Chamaeleo (Chamaeleonidae, Reptilia). Bijdragen tot de dierkunde, 56, 29–38. Hillenius, D. (1988) The skull of Chamaeleo nasutus adds more information to the relationship of Chamaeleo with Rhampholeon and Brookesia (Chamaeleonidae, Reptilia). Bijdragen tot de dierkunde, 58, 7–11. Hofman, A., Maxson, L.R. & Arntzen, J.W. (1991) Biochemical evidence pertaining to the taxonomic relationships within the family Chamaeleonidae. Amphibia-Reptilia, 12, 245–265. Huelsenbeck, J.P. & Ronquist, F. (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics, 17, 754–755. Klaver, C.J.J. (1973) Lung anatomy: aid in chameleon taxonomy. Beaufortia, 20, 155–177. Klaver, C.J.J. (1979) A review of Brookesia systematics with special reference to lung morphology, Bonner zoologische Beitrge, 1–2(30), 163–175. Klaver, C.J.J. (1981) Lung morphology in the Chamaeleonidae (Sauria) and its bearing on phylogeny, systematics and zoogeography. Zeitschrift zoologische Systematic Evolutionforschung, 19, 36–58. Klaver, C.J.J. & Böhme, W. (1988) Systematics of Bradypodion tenue (Matschie, 1892) (Sauria: Chamaeleonidae) with a description of a new species from the Uluguru and Uzungwe mountains, Tanzania. Bonner zoologische Beitrge, 39, 381–393. Klaver, C.J.J. & Böhme, W. (1986) Phylogeny and classification of the Chamaeleonidae (Sauria) with special reference to hemipenis morphology. Bonner zoologische Monographisce 22, 1–64. Laurenti, J.N. (1768). Specimen medicum exhibens Synopsis Reptilium emendatum cum Experimentis circa Venena et Antidota Reptilium Austriacorum. pp. 1–214, 5 pl. Vienna. Loveridge, A. (1957) Checklist of the Reptiles and Amphibians of East Africa (Uganda, Kenya, Tanganyika, Zanzibar), Bulletin of the Museum of Comparative Zoology, 117 153–362. Lutzman, N. & Nečas, P. (2002) Zum Status von Bradypodion tavetanum (Steindachner, 1891) aus den Taita Hills, Kenia, mit Beschreibung einer neuen Unterart (Reptilia: Sauria: Chamaeleonidae). Salamandra, 38, 5–14. Malan, M.E. (1946) Contributions to the comparative anatomy of the nasal capsule and the organ of Jacobsen of the Lacertilia. Annals of the University of Stellenbosch, (A), 24, 69–137. Matthee C.A., Tilbury C.R. & Townsend T. (2004) A phylogenetic review of the African leaf cha-

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meleons: genus Rhampholeon (Chamaeleonidae): the role of vicariance and climate change in speciation. Proceedings of the Royal Society of London, Series B, 271, 1967–1976. Mertens, R. (1966) Chamaeleonidae. Das Tierreich, Berlin , 83, 1–37. Methuen, P.A. & Hewitt, J. (1914) A contribution to our knowledge of the anatomy of chamaeleons. Transactions of the Royal Society of South Africa, 4(2), 89–104. Nečas, P. (2004) Chamaeleo (Trioceros) harennae fitchi (Reptilia: Sauria: Chamaeleonidae), ein neues Chameleon aus dem ethiopischen Hochland, Sauria, 26, 3–9. Nečas, P., Modry, D. & Slapeta, J.R. (2003) Chamaeleo (Trioceros) narraioca n. sp. (Reptilia Chamaeleonidae), a new species from a relict montane forest of Mount Kulal, nothern Kenya. Tropical Zoology, 16, 1–12. Parker, W.K. (1881) On the structure of the skull in chameleons, Transactions of the Royal Society, London, 11, 77–105. Posada, D. & Crandall, K.A. (1998) Modeltest: testing the model of DNA substitution. Bioinformatics, 14, 817–818. Raw, L.R.G. (1976) A survey of the dwarf chameleons of Natal, South Africa, with descriptions of three new species (Sauria: Chamaeleonidae), Durban Museum Novitates, 11, 139–161. Rieppel, O. (1981) The skull and jaw adductor musculature in chameleons, Revue Suisse de Zoologie, 88, 433–445. Rieppel, O. (1987) The phylogenetic relationships within the Chamaeleonidae, with comments on some aspects of cladistic analysis, Zoolological Journal of the Linnean Society, 89, 41–62. Rieppel, O. & Crumley, C. (1997) Paedomorphosis and skull structure in Malagasy chamaeleons (Reptilia: Chamaeleoninae), Journal of Zoology (London), 243, 351–380. Ronquist, F. & Huelsenbeck, J. P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574. Swofford, D.L. (2002) PAUP* Phylogeny analysis using parsimony (*and other methods), version 4.0b10. Sinauer Association, Inc., Sutherland, MA, USA. Tilbury, C.R. (1991) A new species of Chamaeleo Laurenti 1768 (Reptilia Chamaeleonidae) from a relict montane forest in northern Kenya, Tropical Zoology, 4, 159–165. Tilbury, C.R. (1998) Two new chameleons (Sauria: Chamaeleonidae) from isolated Afromontane forests in Sudan and Ethiopia, Bonner zoologische Beitrge, 47, 293–299. Tolley, K.A., Tilbury, C.R., Branch, W.R. & Matthee, C.A. (2004) Phylogenetics of the Southern African dwarf chameleons, Bradypodion (Squamata: Chamaeleonidae), Molecular Phylogenetics and Evolution, 30, 354–365. Tolley, K.A., Tilbury, C.R., Branch, W.R. & Matthee, C.A. (2005) The dwarfs of Africa: taxonomy, distribution and diversity of dwarf chameleons (Bradypodion sensu lato). In Abstracts, Fifth World Conference of Herpetology, Stellenbosch, South Africa, 2005, pp. 156. Tolley, K.A., Burger, M., Turner, A.A. & Matthee, C.A. (2006) Biogeographic patterns and phylogeography of dwarf chameleons (Bradypodion) in an African biodiversity hotspot, Molecular Ecology, 15, 781–793. Townsend, T. & Larson, A. (2002) Molecular phylogenetics and mitochondrial genomic evolution in the Chamaeleonidae (Reptilia, Squamata), Molecular Phylogenetics and Evolution, 23, 22–36. Werner, F. (1902) Prodromus einer Monographie der Chamleonten. Zoologische Jahrbücher, Systematische, 15, 295–460.

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Zootaxa 1426: 68 (2007) www.mapress.com / zootaxa/

ISSN 1175-5326 (print edition)

Correspondence

Copyright © 2007 · Magnolia Press

ZOOTAXA ISSN 1175-5334 (online edition)

Corrections to species names recently placed in Kinyongia and Nadzikambia (Reptilia: Chamaeleonidae) In accordance with the rules of the International Code of Zoological Nomenclature (International Commission on Zoological Nomenclature, 1999) , the gender of the species names must be the same as that of the genus name. In the recently published paper by Tilbury, Tolley and Branch (2006) a number of chameleon species previously placed in the genus Bradypodion Fitzinger 1843 were re-assigned to two new genera, Kinyongia and Nadzikambia. The genus Bradypodion was erroneously considered to be feminine, and in order not to enforce a change in the gender of the species names within the two new genera, they were also specifically nominated as being feminine. However, it has been brought to the author’s attention that in fact the gender of Bradypodion is neuter, and this was accurately reflected in the previous specific names. Unfortunately, as the two new genera were specifically stated to be treated as feminine, the names of the contained species will have to be changed to reflect the nominative feminine gender of the new genera to which they have now been assigned. Although the species names occur regularly in both the popular literature and in East African regional herpetological surveys, the additional amendment of specific ending, given that the generic assignment of the species has also been in flux, is not considered unacceptable. We therefore formally herewith amend the species names accordingly— The genus Kinyongia comprises the following species: Kinyongia fischeri fischeri; K. fischeri multituberculata; K. fischeri uluguruensis; K. tavetana tavetana; K. tavetana boehmei; K. oxyrhina; K. tenuis; K. xenorhina; K. uthmoelleri; K. carpenteri; K. excubitor; K. adolfifriderici. The monotypic genus Nadzikambia comprises the following species: Nadzikambia mlanjensis. We regret any inconvenience that this nomenclatural confusion has occasioned.

COLIN R. TILBURY 1,*, KRYSTAL A. TOLLEY 2 & WILLIAM R. BRANCH 3 1

No. 2 The Bend, Nottingham Road, 3280, KZN, South Africa. E-mail: [email protected]; [email protected] Molecular Systematics Laboratory, South African National Biodiversity Institute, Kirstenbosch Research Centre, P/Bag X7, Claremont 7735 South Africa. E-mail: [email protected] 3 Port Elizabeth Museum, P.O. Box 13147, Humewood 6013, South Africa. E-mail: [email protected] *Corresponding author

2

References International Commission on Zoological Nomenclature (1999) International Code of Zoological Nomenclature. Fourth Edition. The International Trust for Zoological Nomenclature, London, 306 pp. Tilbury C.R., Tolley K.A. & Branch W.R. (2006) A review of the systematics of the genus Bradypodion (Sauria: Chamaeleonidae), with the description of two new genera. Zootaxa, 1363, 23–38.

68 Accepted by S. Carranza: 7 Mar. 2007; published: 15 Mar. 2007