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Pygmy chameleons of the Rhampholeon platyceps compex (Squamata: Chamaeleonidae): Description of four new species from isolated 'sky islands' of northern Mozambique

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The taxonomic status of recently discovered populations of pygmy chameleons (Rhampholeon) from the northern Mozambique montane isolates of Mt. Chiperone, Mt. Mabu, Mt. Inago and Mt. Namuli are assessed, and compared with the closest geographical congeners, including Rhampholeon platyceps Günther 1893 from Mt. Mulanje, and Rh. chapmanorum Tilbury 1992 from the Malawi Hills, both in southern Malawi. Relationships were examined using morphological features and a phylogenetic analysis incorporating two mitochondrial and one nuclear marker. The phylogeny showed that each montane isolate contained a distinct, well-supported clade of chameleons. Chameleons from the Mozambican montane isolates are within a monophyletic clade inclusive of species from southern Malawi (Rh. platyceps and Rh. chapmanorum). Although some relationships are unresolved, the southern Malawi and Mozambican isolates appear to share their most recent common ancestor with species from the Eastern Arc Mountains and Southern Highlands of Tanzania and Malawi (Rh. moyeri, Rh. uluguruesis, Rh. nchisiensis). Along with Rh. beraduccii and Rh. acuminatus, all are included in the subgenus Rhinodigitum. Sister to this larger clade are species from west/central Africa (Rh. temporalis, Rh. spectrum) and the Rh. marshalli-gorongosae complex from southwest Mozambique and adjacent Zimbabwe. Morphological and molecular results confirm that Brookesia platyceps carri Loveridge 1953 is a junior subjective synonym of Rhampholeon platyceps Günther 1892. Historical records of Rh. platyceps from the Shire Highlands (Chiromo) and the Zomba Plateau, are incorrect and the species is now considered endemic to the Mulanje massif. All of the four newly discovered, isolated populations are genetically and morphologically distinct, and we take the opportunity to describe each as a new species. Rhampholeon (Rhinodigitum) maspictus sp. nov. is restricted to Mt. Mabu and distinguished by its large size, well-developed dorsal crenulations, and bright male breeding coloration; Rhampholeon (Rhinodigitum) nebulauctor sp. nov. is restricted to Mt. Chiperone and distinguished by its small size, weakly-developed dorsal crenulations, and a large rostral process in males; Rhampholeon (Rhinodigitum) tilburyi sp. nov. is restricted to Mt. Namuli and distinguished by its small size, weakly-developed dorsal crenulations, and prominent flexure of the snout in males; and Rhampholeon (Rhinodigitum) bruessoworum sp. nov. is restricted to Mt. Inago and distinguished by its small size, weakly-developed dorsal crenulations, large rostral process in males, and relatively long tail in both sexes.
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Accepted by S. Carranza: 27 Feb. 2014; published: 6 Jun. 2014
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Copyright © 2014 Magnolia Press
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http://dx.doi.org/10.11646/zootaxa.3814.1.1
http://zoobank.org/urn:lsid:zoobank.org:pub:A024EBCC-AD60-4104-AD4A-4E4843CE6983
Pygmy chameleons of the Rhampholeon platyceps complex
(Squamata: Chamaeleonidae): Description of four new species
from isolated ‘sky islands’ of northern Mozambique
WILLIAM R. BRANCH
1,2,6
, JULIAN BAYLISS
3
& KRYSTAL A. TOLLEY
4, 5
1
Port Elizabeth Museum, P.O. Box 13147, Humewood 6013, South Africa
2
Department of Zoology, P.O. Box 77000, Nelson Mandela Metropolitan University, Port Elizabeth 6031, South Africa
3
Conservation Science Group, Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK (also Fauna & Flora Inter-
national, Station Road, Cambridge, CB1 2JD, UK)
4
Applied Biodiversity Research Division, South African National Biodiversity Institute, Private Bag X7, Claremont 7735, Cape Town,
South Africa
5
Department of Botany & Zoology, University of Stellenbosch, Private Bag X1, Matieland 7602, Stellenbosch, South Africa
6
Corresponding author. E-mail: billbranch@bayworld.co.za
Abstract
The taxonomic status of recently discovered populations of pygmy chameleons (Rhampholeon) from the northern
Mozambique montane isolates of Mt. Chiperone, Mt. Mabu, Mt. Inago and Mt. Namuli are assessed, and compared with
the closest geographical congeners, including Rhampholeon platyceps Günther 1893 from Mt. Mulanje, and Rh.
chapmanorum Tilbury 1992 from the Malawi Hills, both in southern Malawi. Relationships were examined using
morphological features and a phylogenetic analysis incorporating two mitochondrial and one nuclear marker. The
phylogeny showed that each montane isolate contained a distinct, well-supported clade of chameleons. Chameleons from
the Mozambican montane isolates are within a monophyletic clade inclusive of species from southern Malawi (Rh.
platyceps and Rh. chapmanorum). Although some relationships are unresolved, the southern Malawi and Mozambican
isolates appear to share their most recent common ancestor with species from the Eastern Arc Mountains and Southern
Highlands of Tanzania and Malawi (Rh. moyeri, Rh. uluguruesis, Rh. nchisiensis). Along with Rh. beraduccii and Rh.
acuminatus, all are included in the subgenus Rhinodigitum. Sister to this larger clade are species from west/central Africa
(Rh. temporalis, Rh. spectrum) and the Rh. marshalli-gorongosae complex from southwest Mozambique and adjacent
Zimbabwe. Morphological and molecular results confirm that Brookesia platyceps carri Loveridge 1953 is a junior
subjective synonym of Rhampholeon platyceps Günther 1892. Historical records of Rh. platyceps from the Shire
Highlands (Chiromo) and the Zomba Plateau, are incorrect and the species is now considered endemic to the Mulanje
massif. All of the four newly discovered, isolated populations are genetically and morphologically distinct, and we take
the opportunity to describe each as a new species. Rhampholeon (Rhinodigitum) maspictus sp. nov. is restricted to Mt.
Mabu and distinguished by its large size, well-developed dorsal crenulations, and bright male breeding coloration;
Rhampholeon (Rhinodigitum) nebulauctor sp. nov. is restricted to Mt. Chiperone and distinguished by its small size,
weakly-developed dorsal crenulations, and a large rostral process in males; Rhampholeon (Rhinodigitum) tilburyi sp. nov.
is restricted to Mt. Namuli and distinguished by its small size, weakly-developed dorsal crenulations, and prominent
flexure of the snout in males; and Rhampholeon (Rhinodigitum) bruessoworum sp. nov. is restricted to Mt. Inago and
distinguished by its small size, weakly-developed dorsal crenulations, large rostral process in males, and relatively long
tail in both sexes.
Keywords: Afromontane, Biodiversity, Chamaeleonidae, Rhampholeon, East Africa, new species, reptiles, Southern Af-
rica
Introduction
The Afromontane Archipelago is a series of mountain chains and inselbergs stretching from Ethiopia to South
Africa, characterised by isolated montane forests often with high altitude grassland or heathland habitats. The
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largest and most prominent montane blocks form the Ethiopian and the Kenyan Highlands, the mountain ranges in
the Albertine Rift, the Eastern Arc Mountains of Kenya and Tanzania and the Cape Fold/Drakensberg escarpment
of South Africa. These mountainous regions of Africa are known to harbour rich biological diversity, and
considerable interest in their diversity has resulted in a relative abundance of studies focussing on understanding
biogeography of the region. Indeed, the Cape of South Africa is an extremely well studied system, particularly in
terms of its montane floral endemics (e.g. Linder 2003; Linder 2005; Galley et al. 2006), and the Eastern Arc
Mountains are a well known diversity hotspot across taxa (Burgess et al.1998, 2004; Mittermeier et al. 2004).
Despite the growing wealth of knowledge on the Afromontane system, the montane isolates of Mozambique are a
major gap. Relatively few records exist due to low survey effort, even though this region is an important
connection between the better studied mountains of Tanzania and southern Africa.
The interior of Mozambique, north of the Zambezi River, consists of a relatively level plateau at 700-800m
with numerous, isolated granite massifs, few of which have been thoroughly surveyed. However, even preliminary
surveys have uncovered multiple new species in these mountains. For example, initial survey of Serra Mecula, the
most northerly Mozambique montane isolate (Branch et al. 2005a, b), revealed the endemic girdled lizard Cordylus
merculae Branch, Rödel & Marais 2005, and a number of other species of problematic taxonomic affinities.
However, the other montane inselbergs of northern Mozambique remain largely unstudied, and whilst the early
ornithological survey of Vincent (1933a) gave a general account of the region, it did not discuss the herpetofauna.
Several of these inselbergs in Zambézia Province, including Mt. Chiperone, Mt. Inago, Mt. Mabu, and Mt. Namuli,
(Fig. 1) rise to over 1500 m elevation, and support areas of Afromontane vegetation not found in surrounding
lowlands and are potentially home to numerous endemics (Portik et al. 2013a). By comparison, the nearby Mount
Mulanje in southern Malawi is known to harbour numerous endemic reptiles and amphibians (Loveridge 1953;
Broadley 2001; Branch & Cunningham 2005), including two endemic chameleon species (Tilbury 2010).
During a recent short survey of the avifauna of the Mount Namuli (Ryan et al. 1999), a few lizards were
collected, two of which were provisionally identified as range extensions of species previously considered endemic
to Mt. Mulanje (Branch & Ryan 2001), i.e. Rhampholeon platyceps Günther and Lygodactylus rex.Broadley. Both
specimens, however, showed subtle morphological variation from the Mulanje populations, and it was noted that
further material was required to assess whether these differences were consistent and worthy of taxonomic
recognition. For the dwarf day gecko (Lygodactylus), additional material has allowed genetic analysis and the
description of the new species L. regulus Portik, Travers, Bauer & Branch for the Namuli population, which is
sister to L. rex from Mt. Mulanje (Portik et al. 2013b). The status of the pygmy chameleon (Rhampholeon cf.
platyceps) from Mt. Namuli remained equivocal.
Chameleons form a characteristic and taxonomically diverse component of the African reptile fauna, with at
least 108 species (Krause & Bohme 2009; Barej et al. 2010; Branch & Tolley 2010; Tilbury 2010; Tolley & Herrel
2013) in seven genera. A number of ‘hot spots’ of taxonomic diversity are known, including dwarf chameleons
(Bradypodion) in South Africa (Raw 1976, 1978, 1995; Tolley et al. 2004; Branch et al. 2006; Tolley et al. 2006;
Tolley and Burger 2007; Tilbury and Tolley 2010; Tilbury 2010), and chameleons in the forests (Kinyongia) and/or
grasslands (Trioceros) of East and Central Africa (Tilbury 1991, 1998; Lutzmann & Necas 2002; Necas 2004,
2009; Necas et al. 2003, 2009; Mariaux et al. 2008, Menegon et al. 2009; Tilbury et al. 2006, Tolley et al. 2011;
Tolley & Menegon 2013). Between these two centres of chameleon diversity, localized endemic species are rare.
Broadley (1965) described the enigmatic Chamaeleo mlanjensis from Mt. Mulanje, which was recently placed in a
separate genus (Nadzikambia, Tilbury et al. 2006), and a sister species Nadzikambia baylissi Branch & Tolley was
recently described from Mount Mabu.
African pygmy chameleons, now placed in the genera Rieppeleon and Rhampholeon (Matthee et al. 2004), form a
conspicuous element within montane forest isolates of the Rift area and the Eastern Arc Mountains of East Africa
(Tilbury & Emmrich 1996, Tilbury & Mariaux 2004, Mariaux & Tilbury 2006, Tilbury 2010, Fisseha et al. 2013).
The occurrence of pygmy chameleons in southeast Africa, however, is more sporadic and knowledge of their
distribution somewhat confused. Two closely related species of pygmy chameleon occur on the eastern highlands of
Zimbabwe (Rhampholeon (Bicuspis) marshalli Boulenger) and Gorongoza Mountain (Rhampholeon (Bicuspis)
gorongosae Broadley) with three other species known from the southern Malawi; Rh. platyceps from Mt. Mulanje in
southeast Malawi; Rh. chapmanorum Tilbury from the Malawi Hills at the extreme southern tip of the country; and
Rieppeleon brachyurus (Gűnther) from several localities in Malawi (Blantyre, Mikolongwe, Zomba, Shire Highlands;
Broadley 1966, Tilbury 2010). Records of both Rh. chapmanorum and Ri. brachyurus from “the forests on the slopes
of the Mulanje Massif” (Nečas & Schmidt 2004) are incorrect and likely due to confusion with Rh. platyceps.
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FOUR NEW SPECIES OF RHAMPHOLEON
FIGURE 1. Map showing southern Malawi and Mozambique, with the Rhampholeon localities studied: southern Malawi—Mt.
Mulanje and Malawi Hills; northern Mozambique—Mt. Chiperone, Mt. Mabu, Mt. Namuli and Mt. Inago. Symbols in Key
indicate sampling areas for each species.
Unlike the chameleon fauna in southern Malawi, that of the montane isolates in adjacent northern Mozambique
was poorly known, although there were sporadic records of Ri. brachyurus from Brachysegia savanna in northern
Mozambique (Broadley 1966). This has changed since the formal biodiversity surveys of the Royal Botanic
Gardens Kew Darwin Initiative to montane isolates of central Mozambique (Timberlake et al. 2007, 2009; Bayliss
et al. 2010; Timberlake et al. 2012; Bayliss et al. 2014). Although the herpetofauna was not specifically targeted
during these surveys, and following the discovery of a few unusual lizards on Mt. Namuli during an earlier
ornithological survey (Branch & Ryan 1991), reptiles and amphibians were collected opportunistically. Early
discoveries in the forest on Mt. Mabu included a new species of chameleon (Branch & Tolley 2010), a new species
of bat (Taylor et al. 2012), as well as a new species of forest viper, Atheris mabuensis Branch & Bayliss, a genus
that had never previously been recorded from Mozambique and which, moreover, represented a substantial
southern range extension for the genus (Branch & Bayliss 2009).
During these exploratory surveys of the montane isolates, additional populations of pygmy chameleons were
discovered which could not be assigned to any described taxa. These surveys, together with older material of Rh.
platyceps from Mt. Mulanje (Branch & Cunningham 2005), have allowed a re-assessment of the taxonomic status of
these populations. Rhampholeon are usually restricted to moist evergreen forest, and as a consequence the taxonomic
resolution of allopatric populations associated with ‘sky island’ forest isolates is often problematic. For instance, Rh.
moyeri Menegon, Salvido & Tilbury and Rh. uluguruensis Tilbury & Emmrich can only be distinguished
morphologically by small hemipenial features, and the fragmentation of scales in the interorbital region (Menegon et
al. 2002), which has led to difficulty understanding the taxonomy of some populations. Similarly, two subspecies of the
Mulanje pygmy chameleon (Rh. platyceps) have been recognized by some authors (e.g. Klaver & Böhme 1997, Nečas
& Schmidt 2004), and although these have been rejected by other authors (Broadley 1966, Tilbury 2010), their
taxonomic status has not been formally assessed. The use of molecular phylogenetics, however, has provided a greater
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understanding of the phylogenetic relationships and diversity within pygmy chameleons (Matthee et al. 2004),
including the Rh. moyeri / uluguruensis complex (Fisseha et al. 2013).
In the present study, we assess the evolutionary relationships of Rhampholeon populations in Mozambique in
the context of other adjacent Rhampholeon species known from southern Malawi, including Rh. platyceps on Mt.
Mulanje and Rh. chapmanorum from the Malawi Hills. In addition, we include material from the more southerly
complex from west-central Mozambique and adjacent Zimbabwe (Rh. marshalli and Rh. gorongosae), as well as
the geographically more distant species from southern Tanzania. In particular, we examine populations from the
Mozambican montane isolates of Mt. Chiperone, Mt. Mabu, Mt. Namuli and Mt. Inago to address their taxonomic
status, as well as examining the validity of the problematic subspecies from Mt. Mulanje, Rh. platyceps carri
(Loveridge 1953).
Material and methods
Surveys. Surveys to the montane isolates of northern Mozambique were undertaken as part of ‘Monitoring and
Managing Biodiversity Loss in South-east Africa’s Montane Ecosystems’, a collaborative venture between the
Royal Botanic Gardens, Kew, BirdLife International (United Kingdom), the Instituto de Investigação Agrária de
Moçambique (IIAM) and the Natural History Museum (Mozambique), funded by the UK Government's Darwin
Initiative from 2005 onwards (Smith & Bayliss 2009). A number of Rhampholeon populations were sampled from
forests associated with the montane isolates of Mt. Chiperone (Timberlake et al. 2007), Mt. Namuli (Timberlake et
al. 2009), Mt. Inago (Bayliss et al. 2010) and Mt. Mabu (Timberlake et al. 2012; Bayliss et al. 2014).
Morphological analysis. Specimens examined were housed in the herpetological collections of Bayworld
(formerly Port Elizabeth Museum, PEM) and the Ditsong National Museum of Natural History (formerly the
Northern Flagship Institute and earlier the Transvaal Museum, TM, Pretoria; Appendix 1).
The following measurements were recorded: Snout-Vent Length (SVL)—tip of the snout to the anterior edge of
the cloaca; Tail Length (Tail)—tip of tail to posterior edge of the cloaca; Total Length (TL)—combined SVL and Tail
Length; Head length (HL)—from just behind the tip of the casque to the tip of the snout; Head width
(HW)—maximum width of head (usually in the middle of the casque; Raw 1976); Temporal (TE)—minimum
diagonal distance from posterior edge of orbit to posterior tip of casque; Snout Eye (SE)—from tip of snout to
anterior margin of orbit; Orbit Diameter (OD)—maximum horizontal width of orbit; Inter-orbital distance
(ID)—minimum width between orbits across crown; Rostral Process (RP)—length of soft rostral process (proboscis).
The following scalation details were recorded: Upper labials (UL)—from rostral to (but not including) the
enlarged sub-ocular tubercle; Lateral Crest development (LC)—nature of scales demarcating lateral edge of
casque; Temporal Crest (TC)—number and distribution of enlarged tubercular scales forming a ridge in the
temporal region; Parietal Crest (PC)—enlarged tubercles forming the parietal crest along the longitudinal midline
of the casque top; Supraorbital Ridge (SR)—size and shape of scales forming the ridge above each eye;
Supraorbital Process (SP)—the ‘soft horn’ formed from a cluster of scales in the supraorbital ridge at the junction
of each end of the Interorbital Crest; Interorbital Crest (IC)—number of enlarged and/or raised scales forming a
crest running across the crown between the supraorbital ridges; Inferior Orbital Rim (IOR)—number of enlarged
tubercular scales on the inferio-posterio region of the orbit; Rostral Crests (RC)—the raised ridge of enlarged
scales that demarcate the lateral and upper surface of the snout, and which fuse at the rostrum; Dorsal crenulations
(DC)—number of enlarged clumps of raised tubercles (twice size of intervening granules, and separated by at least
three rows of granules) along top of body and tail; Flank Tubercles (FT): number and distribution of enlarged,
spinose tubercles (at least three times size of surrounding granules) on body between limb insertions. Terminology
of hemipenial morphology follows Klaver & Bohme (1986).
To examine whether Rhampholeon from these mountains show significant morphological differences, eight
morphological measurements were used (Tail, HL, HW, SL, RP, OD, ID, CE). These characters were size corrected
using SVL as a covariate, and the residuals input into a principal components analysis (PCA). Only variables with
communalities > 0.5 were retained in the PCA (Tail, HW, SL, CE). A varimax rotation was used, principal
components (PCs) with eigenvalues >1.0 were extracted, and the resulting PC scores were saved. These PC scores
were then used as input variables for a multivariate analysis of variance (MANOVA) with the species as the fixed
factor. Posthoc pairwise comparisons between were made using Tukey’s HSD test and the Bonferroni test. All
analyses were carried out in SPSS v. 19.
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Phylogenetic analyses. To understand the phylogenetic placement and taxonomy of Rhampholeon from the
inselbergs of Mozambique, a phylogenetic analysis was carried out which included pygmy chameleons from Mts
Inago, Namuli, Chiperone and Mabu plus representatives from other Rhampholeon species, including species
found on nearby inselbergs in Malawi (Rh. platyceps, Rh. chapmanorum), the Zimbabwe Highlands (Rh.
marshalli), Gorongosa Mountain in southern Mozambique (Rh. gorongosae), as well as the nearby Nchisi Plateau
(Rh. nchisiensis Loveridge) in northern Malawi. Multiple individuals from Mt. Mulanje were included in order to
investigate the sub-specific status of Rh. p. platyceps and Rh. p. carri. Specimens from the summit plateau of Mt.
Mulanje were assigned to the race Rh. p. carri, whilst lowland specimens were assigned to the typical race Rh. p.
platyceps.
The resulting dataset consisted of 44 individuals, 21 of which were sequenced for this study and 23 downloaded
from GenBank (Table 1), including the outgroup taxa (Rieppeleon brachyurus, Ri. brevicaudatus (Matchie) and Ri.
kerstenii (Peters)). DNA extraction, PCR amplification, and cycle sequencing of two mitochondrial gene fragments
(ND2 and 16S) were carried out following standard procedures using the following primers for ND2: L4437b
(Macey et al.1997a) and H5934 (Macey et al. 1997b), and 16S: L2510 and H3080 (Palumbi 1996). In addition, a
718 bp portion of the nuclear gene RAG-I 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 were deposited in GenBank or EMBL (Table 1).
TABLE 1. Species name, voucher accession numbers (PEM=Port Elizabeth Museum, CAS = California Academy of
Sciences, Mt.SN = Museo Tridentino di Scienze Naturali, ZMB = Universität Humboldt, Zoologisches Museum) and
GenBank/EMBL accession numbers (16S, ND2, RAG1) for chameleons used in this study. N/A = data, specimen, or
information not available. * indicates new sequence data.
Genus species voucher 16S ND2 RAG1
Rhampholeon platyceps PEM R17136 HG798964* HG798977* HG798991*
Rhampholeon platyceps PEM R17137 HG798965* HG798978* HG798992*
Rhampholeon platyceps PEM R17138 HG798966* HG798979* HG798993*
Rhampholeon platyceps PEM R17139 EF114324* EF114332* EF114340*
Rhampholeon platyceps PEM R17140 EF114325* EF114333* EF114341*
Rhampholeon platyceps (‘carri’) PEM R16290 HG798967* HG798980* HG798994*
Rhampholeon platyceps (‘carri’) PEM R16291 HG798968* HG798981* HG798995*
Rhampholeon platyceps (‘carri’) PEM R16292 HG798969* HG798982* N/A
Rhampholeon platyceps (‘carri’) PEM R16309 HG798970* HG798983* HG798996*
Rhampholeon maspictus sp. nov. (Mabu) PEM R17911 HG798971* HG798984* HG798997*
Rhampholeon maspictus sp. nov. (Mabu) PEM R17912 HG798972* HG798985* HG798998*
Rhampholeon nebulauctor sp. nov.
(Chiperone)
PEM R17278 N/A HG798986* N/A
Rhampholeon nebulauctor sp. nov.
(Chiperone)
PEM R17280 HG798973* HG798987* N/A
Rhampholeon nebulauctor sp. nov.
(Chiperone)
PEM R17281 HG798974* HG798988* N/A
Rhampholeon tilburyi sp. nov. (Namuli) PEM R17131 EF114319* EF114327* EF114335*
Rhampholeon tilburyi sp. nov. (Namuli) PEM R17132 EF114320* EF114328* EF114336*
Rhampholeon tilburyi sp. nov. (Namuli) PEM R17133 EF114321* EF114329* EF114337*
Rhampholeon tilburyi sp. nov. (Namuli) PEM R17134 EF114322* EF114330* EF114338*
Rhampholeon tilburyi sp. nov. (Namuli) PEM R17135 EF114323* EF114331* EF114339*
Rhampholeon bruessoworum sp. nov.
(Inago)
PEM R20374 HG798975* HG798989* HG798999*
......continued on the next page
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Bayesian inference was used to investigate optimal tree space using MrBayes 3.1.2 (Huelsenbeck & Ronquist
2001) on the dataset of 2146 characters, partitioned by marker (ND2, 856 bp; 16S, 469 bp; RAG-I, 821 bp), although
31 bases were excluded for 16S due to ambiguous alignment. To investigate which evolutionary model best fit the
data, jModeltest was used (Posada 2008), and the AIC test indicated the same model for all markers (GTR + G)
was appropriate. Thus, MrBayes was run specifying six rate categories with uniform priors for the gamma
distribution for each of the partitions. To ensure the results were robust, the MCMC was run twice in parallel for 10
million and 20 million generations (four chains in each run), with trees sampled every 1000 generations. Burn-in
was estimated as 2 million generations (2000 trees), as determined by examination the average standard deviation
of split frequencies, the convergence diagnostic (PSRF values ~ 1.0) as well as the log-probabilities and the values
of each parameter for stabilisation (Ronquist & Huelsenbeck 2005). In addition, Tracer v1.4.1 (Rambaut &
Drummond 2007) was used to check that the effective sample size (ESS) of all parameters was greater than 200
after burn-in. A 50% majority rule tree was constructed and nodes with > 0.95 posterior probability considered
supported.
In addition to the Bayesian analysis, a maximum likelihood (ML) search was run using RAxML HPC 7.2.8
(Stamatakis 2006) on the CIPRES Science Gateway (www.phylo.org/sub_sections/portal/) for the combined
dataset. The datasets were partitioned as in the Bayesian analysis, with a GTR+I+G model for all markers and rapid
bootstrapping halted automatically (Stamatakis et al. 2008). This analysis was run three times to ensure that
independent ML searches produced the same topologies. We considered nodes with a bootstrap value of >70% as
supported in this analysis.
TABLE 1. (Continued)
Genus species voucher 16S ND2 RAG1
Rhampholeon bruessoworum sp. nov.
(Inago)
PEM R20375 HG798976* HG798990* HG799000*
Rhampholeon nchisiensis PEM R16247 AY524885 AY524923 AY524960
Rhampholeon nchisiensis PEM R16241 AY524882 AY524920 AY524957
Rhampholeon boulengeri CAS 201682 AY524877 AY524915 N/A
Rhampholeon boulengeri CAS 201681 AY524878 AY524916 AY524953
Rhampholeon chapmanorum PEM R16245 AY524881 AY524919 AY524956
Rhampholeon gorongosae PEM R16252 AY524873 AY524911 AY524949
Rhampholeon gorongosae PEM R16253 AY524874 AY524912 AY524950
Rhampholeon marshalli PEM R16243 AY524870 AY524908 AY524946
Rhampholeon marshalli PEM R16244 AY524871 AY524909 AY524947
Rhampholeon moyeri MTSN002TA AY524875 AY524913 AY524951
Rhampholeon moyeri MTSN001TA AY524876 AY524914 AY524952
Rhampholeon spectrum CAS 207683 AY524863 AY524900 AY524938
Rhampholeon spectrum PEM R16262 AY524865 AY524903 AY524941
Rhampholeon temporalis PEM R16254 AY524866 AY524904 AY524942
Rhampholeon temporalis PEMR 16255 AY524867 AY524905 AY524943
Rhampholeon uluguruensis ZMB 48421 AY524896 AY524934 N/A
Rhampholeon uluguruensis ZMB 48431 AY524897 AY524935 N/A
Rieppeleon brachyurus PEM R16263 AY524898 AY524936 AY524968
Rieppeleon brachyurus PEMR 16264 AY524899 AY524937 N/A
Rieppeleon brevicaudatus PEMR 16257 AY524888 AY524926 AY524963
Rieppeleon brevicaudatus PEM R16256 AY524887 AY524925 AY524962
Rieppeleon kerstenii CAS 169939 AY524890 AY524928 AY524965
Rieppeleon kerstenii N/A AY524892 AY524930 AY524967
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Although the present phylogeny is not dated, it was possible to roughly verify divergence times against dated
divergences for other Rhampholeon species previously estimated in a Bayesian framework using a relaxed clock
(Tolley et al. 2013). Using these already established divergence times together with uncorrected net p-distances
obtained here between Rhampholeon species, a general rate of evolutionary change for the ND2 marker was
estimated. This was then applied to the pairwise p-distances for chameleons from the inselbergs sampled in this
study, which were not included in the Bayesian dating estimates made by Tolley et al. (2013) to examine the
general time frame for divergences.
Results
Morphological analysis. Many scalation features were morphologically conservative, e.g. number of labial scales
and number and distribution of enlarged, spinose tubercles on the flanks, showed little clear demarcation between the
isolated populations. A further complication was that many morphological characters also showed relative degrees of
development, that in some cases were subject to sexual dimorphism whilst others may reflect ontogenetic changes.
Some remain tentative diagnostic features, requiring further sampling for statistical support. The main morphological
features useful in differentiating between the isolated populations are summarized in Table 3.
Analysis of the continuous characters extracted two principal components (PCs) which accounted for 77% of
the variation in the dataset. PC1 loaded highest for HW and CE, whereas the SL and Tail Length (negative) loaded
highest on PC2. The multivariate analysis of variance showed some significant differences between the species for
both PCs (Table 2), although there is a great deal of overlap in general (Fig. 2). Regardless, post hoc pairwise
comparisons (Bonferroni and Tukey’s HSD) showed differences between Rh. platyceps and the Mt Inago
chameleon for PC1 (i.e. HW and CE; p < 0.05), and between the Mt Mabu chameleon with the chameleons from
both Mt Namuli and Mt Chiperone for PC2 (i.e. SL and tail; p < 0.05). Given the small sample sizes, these results
should be considered preliminary, but for the most part there is a great deal of overlap in morphology between
Rhampholeon species suggesting that they are morphologically conservative (Fig. 2). However, there are
potentially minor differences between some species in the dimensions of the head, and the length of the tail.
TABLE 2. Results of principal components analysis and multivariate analysis of variance of morphological characters
for Rhampholeon species. Columns for PC1 and PC2 indicate the loadings of the original variables, % variance of each
PC is given, as are the F and p values of the MANOVA using ‘species’ as the fixed factor.
* p < 0.05, ** p < 0.01
Phylogenetic analyses. The two phylogenetic analyses resulted in similar tree topologies and node support.
The chameleons from the Mozambican inselbergs (Mt Namuli, Mt. Inago, Mt. Mabu, Mt. Chiperone, and Mt.
Mulanje) each formed separate, well-supported monophyletic lineages consistent with species (Fig. 3), and this
was further supported by uncorrected p-distances which are comparable to those observed between other
chameleon species (e.g. Menegon et al. 2009; Tilbury & Tolley 2009; Gehring et al. 2012; Table 4). Rhampholeon
from southern Malawi are within a larger Rhampholeon clade that also includes chameleons from the Mozambican
inselbergs. Despite the close geographic distance between Inago and Namuli (30 km), the lineage from Mt. Inago is
sister to all other Rhampholeon from the region, whereas the lineage from Namuli is more closely related to
lineages from Mt. Mabu (120 km distant), Mt. Chiperone (180 km distant), and Rh. chapmanorum from Malawi
Hills (250 km distant). The two most closely related species are the new species from Mt Chiperone and Rh.
Original variable PC1 PC2
Head width (HW) 0.842 0.133
Tip of casque to eye (CE) 0.840 -0.115
Snout length (SL) 0.495 0.773
Tail length 0.587 -0.876
% var 50.1 27.2
F3.00 4.359
P0.019* 0.002**
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chapmanorum from Malawi Hills (75km apart). Overall, the Mozambican/Malawi clade is most closely related to
species further north in Malawi, Tanzania, and Uganda (i.e. Rh. nchisiensis, Rh. boulengeri Steindachner, Rh.
uluguruensis, Rh. moyeri), although these relationships are not supported in the phylogeny.
The two sub-species recorded from Mt. Mulanje (Rh. p. platyceps and Rh. p. carri) form a single clade, and are
not reciprocally monophyletic. Sequence divergence between these sub-species is low, and is comparable to the
values found within other species both on adjacent montane isolates, and for chameleons from other regions and
genera (Table 4; e.g. Tolley et al. 2011). Indeed, the p-distance within Rh. p. carri (0.009) exceeds the distance
between Rh. p. carri and Rh. p. platyceps (0.004). Given the lack of morphological and genetic differentiation, as
well as a completely overlapping distribution, sub-species status for Rh. p. carri is not supported.
The populations of chameleons on the Mozambican inselbergs are estimated to have been isolated in the
Miocene, based on rough dating of divergence times (Table 5). The chameleons on Mt. Inago appear to have been
isolated longest, probably since the mid-Miocene. Divergence times for the remaining populations are similar, and
are within the late-Miocene. Because of the methodology used, these dates are provisional, but correspond closely
with dates for Rhampholeon divergences dated within a Bayesian framework (Tolley et al. 2013).
FIGURE 2. Scatterplot of the first two principal components extracted of morphological characters for the Rhampholeon
platyceps complex. Individuals from each species are indicated by symbols that correspond with those in Figure 1.
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FIGURE 3. Maximum likelihood topology for the Rhampholeon platyceps complex, and other members of the genus. Nodes
supported by both ML (>70% bootstrap) and Bayesian posterior probabilities (>0.95pp) are denoted with black circles. Nodes
supported by ML only are denoted with white circles. The former sub-species for R. platyceps are denoted with c (‘carri’) and
p (‘platyceps’). Symbols beside each species correspond with those in Figure 1.
Discussion
The phylogenetic analysis and corresponding sequence divergence estimates suggest that there are several
previously unknown, but clearly distinctive species of Rhampholeon in Mozambique, found on each of the four
inselbergs investigated. These species form a clade with described species from Malawi (Malawi Hills and Mt.
Mulanje), which is sister to the Rhampholeon from East Africa, although support for the deeper nodes is lacking.
Many of the inselbergs throughout the region from central Mozambique to the southern highlands of Tanzania have
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not been surveyed, and contain appropriate montane forest habitat. As targeted surveys in both East and southern
Africa montane habitats, more often than not, reveal new species (e.g. Bradypodion: Tilbury and Tolley 2009;
Kinyongia: Menegon et al. 2009; Greenbaum et al. 2012; Rhampholeon: Mariaux and Tilbury 2004; Trioceros:
Stipala et al. 2011, 2012), it is likely that yet other undiscovered taxa are missing from the phylogeny and these
deep relationships may become better resolved with the inclusion of additional new taxa.
Chameleons on these inselbergs probably shared a common ancestor in the mid-Miocene. Chameleons on Mt.
Inago appear to have diverged first (ca. 11-20 Mya), possibly followed by those on Mt. Mulanje and Mt. Namuli
(ca. 6-16 Mya). The remainder of the inselbergs have similar divergence times (ca. 4-12 Mya) although chamelons
from Mt. Mabu, Mt. Chiperone and Malawi Hills (Rh. chapmanorum) appear to have diverged from each other
more recently (4-9 Mya), suggesting these forests remained connected the longest (see also Fig. 3). Although these
dating estimates should be considered tentative, they correspond reasonably well with those obtained using a
Bayesian framework (Tolley et al. 2013). For example, Rh. platyceps and Rh. chapmanorum are thought to have
diverged approximately 9 million years ago (see Fig. 1, Tolley et al. 2013), which corresponds with the rough
dating obtained in the present study (9-16Myr).
Status of Brookesia platyceps carri Loveridge 1953. Rhampholeon platyceps Günther 1893 was based on
material collected by Alexander Whyte (botanist and natural history collector) and sent to the British Museum by Sir
Harry Johnston. The type locality was given as the Shire Highlands, Malawi, with a subsequent record (Günther 1894)
from “Tshiromo” (BM 93.10.26.35). Loveridge (1953) noted that many of the localities of specimens forwarded by
Johnston were incorrect, and he referred the “Tshiromo” record to Chiromo. Stevens (1974), however, noted that Rh.
platyceps did not occur on the Shire Highlands, and that the locality for the Chiromo (“Tshiromo”) record was probably
mislabeled. He therefore recommended that “the type locality should be restricted to Mulanje Mountain” (Stevens
1974, p13), and this was accepted by Klaver & Böhme (1997).
Loveridge (1953) described a new race, Brookesia (= Rhampholeon) platyceps carri, from the Lichenya
Plateau and Ruo Gorge, Mt. Mulanje. His diagnosis of the race was poor (see below), and in an unpublished thesis
Broadley (1966) transferred it to the synonymy of Rh. platyceps. Understandably unaware of this decision, Klaver
& Bohme (1997) continued to recognize both races in their checklist of the Chamaeleonidae. This arrangement was
followed by Nečas & Schmidt (2004), who mistakenly noted that typical Rh. platyceps “has only been recorded
from the Shire Highlands (Chiromo) south of Lake Nyassa and on the Zomba Plateau, whereas a single specimen
of Rh. p. carri is known from the Mulanje Mountains”. This contradicted Loveridge’s (1953) own interpretation,
for he had referred specimens from both Lichenya Plateau and Ruo Gorge on Mt. Mulanje to typical Rh. playceps,
and the type series of Rh. p. carri comprised not one, but four specimens. Stevens (1974) made no comment on the
status of Rh. p. carri, but noted that Rh. platyceps did not occur on the Shire Highlands, and that recent records
were found only on Mt. Mulanje. Broadley (2004) also noted that Rh. platyceps was endemic to the Mulanje
Massif, and reiterated earlier comments (Broadley 1966), that “the subspecies carri Loveridge 1953 (was) not
distinguishable”. Although this arrangement was also followed by Tilbury (2010), the status of Loveridge’s upland
race, Rh. p. carri, had not been formally assessed.
The putatively diagnostic characters of Brookesia platyceps carri include the presence of enlarged spines
associated with crenulations along the vertebral line, and the absence (or greatly reduced nature) of a spine above
the eye on the supraciliary ridge (Loveridge 1953). Recognition of this upland race was a provocative action by
Loveridge (1953). He had little material at hand (4 specimens in the type series, three of which he noted were “in
the nature of intermediates”) and also did not assess potential sexual dimorphism in the expression of these
relatively minor differences in scalation. That his proposed type locality of carri (“Lichenya Plateau, 6000 feet,
Mulanje Mountain, Nyasaland”) clashed with a specimen from the same locality that he referred to typical Rh.
platyceps (BM 33.4.3.4) seems to have unperturbed him, and he resolved the problem by simply arguing that the
latter was probably collected elsewhere on the mountain. Broadley’s (1966) rejection of the race was
understandably brief, given the superficial and conflicting evidence upon which Loveridge’s (1953) description
was based. Unfortunately, Broadley’s action was overlooked by both Klaver & Böhme (1997) and Nečas &
Schmidt (2004), and greater confusion was caused when the latter authors expanded Loveridge’s (1953) diagnosis
of Rh. p. carri by claiming that the subspecies “lacks a nasal process” (more correctly a rostral process). This was
in conflict with Loveridge’s (1953) diagnosis and also with his own picture (pl. 3, fig. 2) of Rh. p. carri
(reproduced in Nečas & Schmidt 2004), which shows a male paratype from Ruo Gorge with a well-developed
rostral process and with relatively weak spines on the vertebral crenulations. The rostral process is not only subject
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to individual variation but also sexual dimorphism in some populations, where it is usually more elongate in males.
Moreover, there may be a distinct ontogenetic change in both the relative size of the rostral process and the degree
of angular flexure of the snout, both of which may be larger in juveniles (see the situation in the Mt. Mabu pygmy
chameleon, Fig. 6C).
Loveridge’s (1953) diagnostic features for Rh. p. carri are both subjective, contrasting the degree of
development between the putative races of spinose scales on the supraorbital crest and on the crenulations of the
dorsal crest. Among a series of 29 specimens examined during the present study, including specimens from
different localities on the summit area (Chambe Hut, Sombani Hut, Lichenya plateau) and lower slopes (Ruo
Gorge, Madzeka River, Chisengoli Forest) of Mt. Mulanje, no consistent geographical pattern of variation in either
the putative diagnostic or other scalation features was evident. In addition, there is a lack of support for the two
sub-species from the phylogenetic analysis, as they form a single polyphyletic clade. Although we cannot
necessarily expect subspecies to form monophyletic clades, the sequence divergence (ND2: 0.9%) within
specimens assigned to Rh. p. carri (i.e. from Lichenya Plateau and other upland locations) exceeds the distance
between Rh. p. carri and lowland locations assigned to Rh. p. platyceps (ND2: 0.04%). Given the lack of
morphological and genetic differentiation, as well as completely overlapping distributions, we concur with the
conclusions of Broadley (1966) and Tilbury (2010) that there is no support for the subspecific status of Brookesia.
platyceps carri Loveridge 1953, which thus become a junior subjective synonym of Rhampholeon platyceps
Günther 1892.
Taxonomic status of Rhampholeon populations from Mt. Chiperone, Mt. Mabu, Mt. Namuli and Mt.
Inago. Pygmy chameleons are considered morphologically conservative, with low vagility and specific habitat
requirements. The multivariate analysis of morphological characteristics does show a great deal of overlap for the
traits analysed (Fig. 2), although this could also be confounded by small sample sizes and the small set of traits
suitable for inclusion. Chameleons however, are known to have morphological features that are adaptive for
specific habitats (e.g. Herrel et al. 2013) and given that Rhampholeon are specialists for the terrestrial forest
habitat, morphological conservatism is expected across the genus. Although Rhampholeon have not yet been
investigated in this specific context, the results of this study are consistent with morphological conservatism as a
result of habitat specialization, but this hypothesis could be further examined by expanding the character set to
include traits ecologically relevant for the terrestrial forest environment, as well as quantitative data on the habitat
characteristics of the forests. Subtle difference in habitat utilization are suggested by apparent differences in perch
height between Rh. chapmanorum (Tilbury 1992), the only chameleon recorded in the evergreen forest of the
Malawi Hills, and also for the Mt. Mabu pygmy chameleon (Branch pers. obs.) which is in sympatry with the
chameleon Nadzikambia baylissi in the Mabu forest (Branch & Tolley 2010).
Although they lack strong morphological differences, some scalation differences are evident among the
chameleons from these mountains (Fig. 2, Table 3). In concert, these morphological features can be used to
diagnose these genetically well-differentiated populations. Our studies have revealed a previously unsuspected
radiation of pygmy chameleons within the Rh. platyceps complex that complements a similar Eastern Arc
radiation. We therefore take this opportunity to describe new species of pygmy chameleons from each of the four
currently explored montane isolates of northern Mozambique, i.e. Mt Mabu, Mt Chiperone, Mt Namuli and Mt
Inago.
Systematics of the Rhampholeon (Rhinodigitum) platyceps complex
Rhampholeon (Rhinodigitum) platyceps Günther, 1892.
Mount Mulanje Pygmy Chameleon
Synonomy: Brookesia platyceps Loveridge 1933
Brookesia platyceps platyceps Loveridge 1953
Brookesia platyceps carri Loveridge 1953
Rhampholeon (Rhinodigitum) platyceps Matthee, Tilbury & Townsend 2004.
Holotype: Adult female (BMNH 1946.8.21.73), collected by A. White. Type locality (by subsequent designation,
Stevens 1974): Mt. Mulanje, southern Malawi.
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Variation in adult coloration of an adult male (Fig. 4A) and adult female (Fig. 4B), and evergreen forest habitat
in the Lichenya plateau region, are shown (Fig. 4C). For full details of morphology, hemipenial structure, biology
and habitat see Tilbury (2010).
FIGURE 4. Rhampholeon platyceps: A—adult male (Lichenya Plateau, PEM R16311, J. Marais, B—adult female (Lichenya
Plateau, PEM R16310, J. Marais); C—Habitat on the Mt Mulanje plateau (J. Marais); R. chapmanorum: D—adult male, PEM
R16245, E—adult female, PEM R16246 (Malawi Hills, C. Tilbury).
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Rhampholeon (Rhinodigitum) chapmanorum Tilbury, 1992
Chapmans’ Pygmy Chameleon
Synonomy: Rhampholeon chapmani Tilbury 1992
Rhampholeon chapmanorum Klaver & Böhme 1997
Rhampholeon (Rhinodigitum) chapmanorum Matthee, Tilbury & Townsend 2004.
Holotype: Adult male (BMNH 1988.399), collected by Colin and Sarah Tilbury. Type locality: in evergreen forest
at 940 m asl., above the Chididi Police post, on top of Malawi Hills, southern Malawi.
Variation in adult coloration in an adult male and an adult female are illustrated in Fig. 4D and Fig. 4E,
respectively. Note also the pronounced nasal and supraorbital processes on the head of the male. For full details of
morphology, hemipenial structure, biology and habitat see Tilbury (2010).
Rhampholeon (Rhinodigitum) maspictus sp. nov.
Mount Mabu Pygmy Chameleon
Synonomy: Rhampholeon (Rhinodigitum) chapmanorum Tilbury 2010, p 179.
Rhampholeon sp. Timberlake et al. 2012, p 45; Bayliss et al. 2014, p 179.
Etymology. The specific epithet derives from a combination of mas (L. = man) and pictus (L. = painted), alluding
to the unusual bright colours of most males, which are often retained for long periods, even when sleeping at night.
Types. The type series comprises ten specimens all preserved in 50% propanol (except for one hatchling in
90% ethanol), including:
Holotype. An adult male (PEM R18072; Fig. 5A, 6A) collected by a W.R. Branch, J. Bayliss & W. Conradie,
27 May 2009, in the vicinity of the main forest base camp, Mt. Mabu, Zambézia Province, Mozambique
(16º17'10.1"S, 36º24'02.2"E; 967 m a.s.l.).
Allotype. An adult female with a small ventral incision (PEM R18061, Fig. 5B, 5A), same collecting details as
holotype.
Paratypes. Eight specimens, comprising four males (PEM R18059, 18073 (Fig. 6B), 18074-75), same
collecting details as holotype; three females (PEM R18069-70, 18076), same collecting details as holotype; and a
hatchling (PEM R18068, Fig. 6C)
Additional material (used in analysis but not forming part of the type series): 13 specimens, all from forest
Camp region, Mt. Mabu, Zambezia Province, Mozambique (16˚17'12"S, 36˚24'14"E; 1000m a.s.l.); PEM R17130
(J. Bayliss, January 2006), PEM R17911-12 (J. Bayliss, 16 April 2009), PEM R18057-58, 18060, 18062-67,
18071, same collecting details as holotype.
Meristics. Measurements for the type series of Rhampholeon maspictus sp. nov. are summarized in Table 6.
Diagnosis. The Mt. Mabu Pygmy Chameleon is referable to the Rhampholeon (subgenus Rhinodigitum
Matthee et al. 2004) by possessing a short hemipenis that is almost bag-like, acalyculate and adorned with a pair of
simple, curved apical “horns” with a variable number of thorn-like papillae arranged on the outer aspect of the
horn; claws that are strongly bicuspid, smooth plantar surfaces, a rostral process, and short tail (<25% of total
length in adult males). It can be distinguished from most other species in Rhampholeon (Rhinodigitum) by having
deep inguinal (absent or indistinct in Rh. boulengeri, Rh. nchisiensis, Rh. uluguruensis, and Rh. moyeri) and
axillary pits (also absent in Rh. nchisiensis). It differs from all other members of the Rh. platyceps complex by the
bright green male breeding coloration, including blue flanks and side of head, and yellow throat, snout and eye ring
(all of which may be retained even at night). It shares with Rh. platyceps, but differs from all other populations of
the complex from Mt Chiperone, Mt Namuli and Mt Inago, its large size (>60 mm SVL) in both sexes, lack of male
dwarfism, well-developed dorsal crenulations, and reduced rostral and supraocular processes; it differs from Rh.
platyceps by its more dorsoventrally flattened habitus (more rounded in Rh. platyceps), and very weak or even
absent accessory plantar spines (present but small in Rh. platyceps). Finally, the species is also genetically well
differentiated from all other Rhampholeon, and all chameleons examined from Mt. Mabu form a monophyletic
clade.
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TABLE 6. Measurements (mm) for the type series of Rhampholeon maspictus sp. nov. from Mount Mabu, Mozambique
(PEM: Port Elizabeth Museum).
TABLE 6. (Continued)
Description of Holotype. Adult male, viscera exposed by a single ventral incision in the chest region; both
hemipenes everted.
Head: Dorsum of head flattened, with no upward flexure of the snout; casque flat with weakly define lateral
crests; temporal crest moderate with a single row of interrupted large tubercles; parietal crest almost absent,
composed of a few enlarged tubercles in the mid-line; supraorbital ridge present but with only few raised conical
tubercles; three enlarged tubercles on inferior orbital rim; supraorbital connected in middle by shallow interorbital
ridge composed of 11 small granular tubercles that demarcate the posterior edge of a prominent frontal depression;
rostral ridge very well marked, forming a small bump over the nostrils and fusing anteriorly and adorned with a
small rostral process (2.1 mm, in fixation flattened against rostrum); rostral process 4 small tubercular scales long
and 4 tubercles wide at base; nares opening posterio-ventrally; no gular or mental appendages; scales on throat
homogenous, more conical than those on crown of head and subequal in size to those on the belly.
Body: Dorsal crest moderately developed, comprised of 9 weak crenulations each comprised of a cluster of
enlarged spinose scales, crenulations most strongly developed over mid-body, reduced over base of neck and tail;
crenulations continue onto tail comprised of 9 small groups that are largest over the distal half of the tail; deep
axillary and inguinal pits are present; flank scalation heterogeneous, composed of small, stellate granules with
scattered, enlarged spinose tubercles, the largest occurring over the shoulder; chest, belly and lower surface of tail
smooth; limb scalation more tubercular, with a few enlarged, spinose tubercles on the forearms; claws strongly
bicuspid; accessory plantar spines very reduced or almost absent.
PEM R18072
Holotype
PEM R18061
Allotype
PEM R18059
Paratype
PEM R18073
Paratype
PEM R18074
Paratype
Sex M F M M M
Snout-vent length 62.0 59.0 56.2 63.4 64.4
Tail length 19.4 13.1 18.1 17.5 19.8
Total length 81.4 72.1 74.3 80.9 84.2
Head length 19.1 18.2 20.0 19.6 20.3
Head width 11.1 9.8 12.3 11.7 12.1
Orbit diameter 5.2 4.3 4.9 5.0 5.4
Snout length 6.0 5.0 6.8 5.9 5.9
Inter-orbital 5.9 4.7 5.4 5.8 5.9
Rostral process 2.1 1.2 2.1 1.9 2.7
Casque to Eye 13.3 8.3 8.9 10.6 9.1
PEM R18075
Paratype
PEM R18069
Paratype
PEM R18070
Paratype
PEM R18076
Paratype
PEM R18068
Paratype
Sex M F F F Hatchling
Snout-vent length 64.0 64.8 61.9 56.8 19.6
Tail length 16.9 15.1 14.0 11.6 4.9
Total length 80.9 79.9 75.9 68.4 24.8
Head length 18.1 19.3 17.8 18.0 6.9
Head width 10.4 11.3 10.9 9.3 4.9
Orbit diameter 4.7 4.4 4.2 3.9 2.1
Snout length 5.5 6.1 5.5 5.4 2.0
Inter-orbital 5.2 5.7 5.7 5.7 3.3
Rostral process 2.5 1.0 2.3 1.0 0.5
Casque to Eye 8.7 9.7 8.7 9.3 2.9
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Colour in Life: Male coloration stunningly beautiful (Figs. 5A); body, tail and limbs leaf green, slightly
mottled and also darker along the dorsal crest of body, tail and upper surfaces of fore- and hindlimbs; central region
of flanks light blue, with two oblique, broad yellow-green stripes; light blue of flanks extends onto the side of head
and around eye, where it becomes darker and more intense; front of chest, throat, labials, rostral process and upper
surface of snout to the level of the orbit, dirty yellow; bright yellow eye ring. When stressed (e.g. in artificially
close proximity to another chameleon) the body coloration changes dramatically, the body darkening to green-
brown, and the blue flank region becomes paler and infused with brown blotches (Fig. 6A); the green orbital
region, yellow eye ring and dirty yellow throat colour are retained, albeit in subdued form.
Colour in preservative: Body dark brown with 3 faint oblique bars of lighter brown on flanks running from
backbone to lower flank; belly, tail and limbs uniform dark brown, except light brown on inner surface of
forelimbs.
Description of Allotype (as for holotype, unless noted): adult female, with viscera exposed by a single, ragged
ventral incision in the belly, and liver tissue excised for DNA analysis.
Head: Temporal crest weakly developed comprised of a disrupted row of slightly enlarge tubercles; parietal
crest absent; subocular ridge weakly pronounced with few enlarged tubercles; interorbital ridge with 13 weakly
enlarged tubercles
Body: Dorsal crest very weakly developed, comprising 7 crenulations of tubercles that are only slightly
enlarged; crenulations most strongly developed over mid-body and almost absent on the tail; flank scalation
heterogeneous, composed of small, stellate granules with very few scattered, enlarged spinose tubercles, the largest
at the shoulder.
Coloration in Life: Less intensely coloured than male holotype (Figs. 5B); sides of body dorsally dull green
with two vague, oblique, dark olive stripes that extend from dorsal crest, where they are broader, onto lower flank;
upper flanks with large, irregular light brown blotches that coalesce and cover upper surface of tail; lower flanks
brighter green with scattered pale blotches, extending as pale green onto lower surface of tail; upper surfaces of
limbs olive, paler green below; upper surface of casque pale brown, extending at a narrow, almost white line along
the dorsal crest; front and sides of snout mottled in light green and brown giving a dull green-brown appearance;
throat cream with numerous light blue tubercles that coalesce to form irregular blotches; orbital area olive green
with scattered pale blue tubercles and a dull red eye ring. When stressed the irregular light brown blotches on the
upper flanks become paler, and the sides of head become blotched, especially in the labial region, giving an
appearance of alternating pale and dark bands radiating from the eye (Fig. 6A).
Colour in preservative: Body and head uniform dark brown above and below.
Paratype variation. All paratype males have well-everted hemipenes. In life the orbital scalation of a male
paratype (R17130) was light green, with a conspicuous yellow ring around the iris; the pale brown body had two
prominent rust red “leaf vein” narrow lines that ran from the dorsal crest obliquely to the lower flank; there is a
prominent enlarged, pale yellow-cream spinose tubercle on the fore-flank in the shoulder region; the crown of the
casque and dorsal crest on the body and tail was medium brown (Fig. 6B). A very small specimen (PEM R18068,
SVL 19.6 mm) has a mottled reddish brown head, body and limbs, with two vague, narrow oblique red-brown
stripes that run from the dorsal crest to the lower flanks; the dorsal crest forms a narrow cream stripe that extends
onto the casque, where it becomes disrupted into small blotches; the limbs are darker brown with scattered bright
yellow tubercles of the upper surfaces; the orbital region is dull brown with scattered small blue tubercles and a
dull red eye ring (Fig. 6C).
Size. Largest male—PEM R18074 (paratype) 65.2 + 20.1 = 85.3 mm; largest female—PEM R18069
(paratype) 64.4 + 16.2 = 80.6 mm. The smallest specimen—PEM R18068 (paratype, unsexed) 19.9 + 4.9 = 24.8
mm) appears to be newly hatched.
Sexual Dimorphism. The average total size of males (65.3 mm, n = 11) and females (64.4 mm, n = 11) is
similar and suggests no sexual size dimorphism. However, males do have proportionately longer tails (TL as = %
of SVL 24.0% in males, but only 18.6% in females). Sexual dichromism in pygmy chameleons remains poorly
known, and has not been studied in the Rh. platyceps complex. Tilbury (1992) noted the emergence of bright
colours (pale powder blue head and neck, and bright white eyelids) in male Rh. chapmanorum in male-male
interactions. The bold colours of large male Rh. maspictus sp. nov. (Fig. 5A) was noted in three different males at
the type locality, including two specimens sleeping at night on low vegetation. No female was observed showing
the bright green body and blue and yellow head of adult males.
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FIGURE 5. Rhampholeon maspictus sp. nov. : A—Holotype, B—Allotype (W.R. Branch)
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FIGURE 6. Rhampholeon maspictus sp. nov. : A—Allotype (left) and Holotype (right); B—Paratype (PEM R17073); C
Paratype (PEM R17068, hatchling); D—Habitat on Mt. Mabu (W.R. Branch).
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Hemipenis. (based on everted hemipenes of five males in the type series). Hemipenis short with unadorned
basal and apical sections, except for a pair of curved horns that form the lateral edges of a prominent, flat-topped
crown; 3-4 weakly-developed spines occur on the upper surfaces of the horns; the folds of the sulcus spermaticus
flare to drain into the flattened apical region.
Distribution. Known only from the type locality; Mt. Mabu, Zambézia Province, central Mozambique, but
expected to occur throughout much of the extensive forest (+7880 ha) remaining on the massif (Bayliss et al.
2014).
Habitat. The Mabu massif is a complex of granitic inselbergs formed of syenite, an igneous intrusion of the
younger Precambrian Namarroi series dating from 850 ‒1100 Mya (Instituto Nacional de Geologia 1987).
Although the Mabu Massif shows vegetational zonation and a significant extent (+7880 ha) of mid-altitudinal
forest, it lacks the large area of upland plateau that occurs on Mt. Namuli. Mt. Mabu is surrounded by Brachystegia
woodland at the base, much of which is replaced to the south by the Cha Madal tea estate. The paratype series were
collected at night on perches from 30-100 cm above ground in forest clearings and adjacent to a mountain stream
(Fig. 6D). No specimens were collected on perches as high as 1.3 m to 5 m noted for Rh. chapmanorum (Tilbury
1992). This may be related to the presence of an additional chameleon (N. baylissi) which utilizes this forest
stratum on Mt. Mabu, and that has not been recorded on Mt. Chiperone.
Reproduction. The female allotype was gravid with seven almost spherical eggs (largest diameter 4.1-4.5 mm,
four in the left oviduct and three in the right oviduct) that lack obvious signs of embryonic development.
Rhampholeon (Rhinodigitum) nebulauctor sp. nov.
Mount Chiperone Pygmy Chameleon
Synonomy: Rhampholeon champmanorum (sic.) Timberlake et al. 2007, p20.
Etymology. The specific epithet is a noun in apposition and derived from nebula (L. = cloud, mist) and auctor (L.
= maker), i.e. ‘cloudmaker’, alluding to the ‘Ciperoni’, the local name for the cold drizzle that comes to the Shire
Highlands of southern Malawi as moist air from the Indian Ocean is forced to rise over Mt. Chiperone.
Types.The type series comprises five specimens, including:
Holotype.- An adult female (PEM R17278) collected by J. Bayliss, 1 December 2008, in the shrub understorey
of evergreen forest on the southeast slopes of Mt. Chiperone Massif, Zambézia Province, Mozambique
(16˚30'25.9”S, 35˚43'33.4”E, ca 1000 m a.s.l.).
Allotype. An adult male (PEM R17281), collected by J. Bayliss on 27 November 2008; same locality details as
holotype.
Paratypes. Three specimens, comprising an adult female (PEM R17277) and two subadult females (PEM
R17279-80), all collected by J. Bayliss between 26 November and 3 December 2008, same locality details as
holotype.
Meristics. Measurements for the type series of Rhampholeon nebulauctor sp. nov. are summarized in Table 7.
Diagnosis. The Chiperone Pygmy Chameleon is referable to the Rhampholeon (subgenus Rhinodigitum
Matthee et al. 2004) by having an unpigmented parietal peritoneum, claws that are strongly bicuspid, smooth
plantar surfaces, a rostral process, and short tail (<27% of total length in adult males). It can be distinguished from
most other species in Rhampholeon (Rhinodigitum) by having deep inguinal (absent or indistinct in Rh. boulengeri,
Rh. nchisiensis, Rh. uluguruensis, and Rh. moyeri) and axillary pits (also absent in Rh. nchisiensis). It is
geographically closest to Rh. chapmanorum, but differs from that species by its smaller size, the presence of a
relatively large rostral process in males, and accessory planter spines that are very poorly developed in both sexes.
It is well differentiated from Rh. platyceps and Rh. maspictus sp. nov. by its smaller size (SVL <53 mm), relatively
larger rostral process, and weakly developed dorsal crest crenulation. It is morphologically closest to the Mt
Namuli chameleon, but has a slightly narrower head and appears to lack the cranial flexure of the head present in
male chameleons from Mt Namuli (further material is required to confirm both these features). The female
holotype also displayed a bright green and orange coloration (Fig. 7A, B), but whether this is diagnostic also awaits
the collection of further material. Finally, the species is genetically well differentiated from all other Rhampholeon,
and all chameleons examined from Mt. Chiperone form a monophyletic clade.
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TAB L E 7. Measurements (mm) for the type series of Rhampholeon nebulauctor sp. nov. from Mount Chiperone,
Mozambique (PEM: Port Elizabeth Museum).
FIGURE 7. Rhampholeon nebulauctor sp. nov. Holotype (PEM R17278): whole body (A) and close-up of head (B);
C—Habitat on Mt. Chiperone (J. Bayliss).
PEM R17278
Holotype
PEM R17281
Allotype
PEM R17277
Paratype
PEM R17279
Paratype
PEM R17280
Paratype
Sex F M F F F
Snout-vent length 44.7 32.3 48.9 41.6 36.3
Tail length 11.3 11.6 13.2 9.1 8.6
Total length 56.0 43.9 62.1 50.6 44.9
Head length 14.4 10.9 14.8 13.4 12.3
Head width 7.4 5.9 8.9 7.2 5.8
Orbit diameter 4.0 3.4 4.4 3.5 3.6
Snout length 4.9 3.1 4.6 4.5 3.9
Inter-orbital 5.3 4.9 5.7 5.1 4.4
Rostral process 1.5 2.2 1.4 1.3 1.1
Casque to Eye 10.2 8.0 10.6 7.2 7.5
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Description of Holotype. Adult female, viscera exposed by a large ventral incision.
Head: Dorsum flattened, with no upward flexure of the snout; casque flat, edged with weakly-defined lateral
crests that are mainly restricted to the posterior region of the casque; temporal crest weakly-developed, comprising
a single, interrupted row of large tubercles; parietal crest almost absent, composed of a few enlarged tubercles in
the mid-line; supraorbital ridges reduced to a few scattered enlarged scales but with a very small multi-scaled
process forming a ‘soft horn’ at each end of the inter-orbital ridge that passes across crown and is composed of 11
small granular tubercles, and that demarcate the posterior edge of a slight frontal depression; inferior orbital rim
with 4 (right) and 4 (left) enlarged tubercles; snout bordered on each side by moderately developed rostral crests,
that fuse together at the tip of the snout which is adorned with a very small, flattened rostral process (1.5 mm), and
is three small tubercular scales long and three tubercular scales wide at its base; nares opening posterio-ventrally;
no gular or mental appendages; scales on throat homogenous, more conical but smaller than those on crown of
head and subequal in size to those on the belly.
Body: Dorsal crest very weakly developed, reduced to 7 crenulations of enlarged, but not obviously spinose
scales; crenulations most strongly developed over mid-body, reduced in size over on neck and tail; crenulations
continue onto tail but in more reduced form; deep axillary and inguinal pits are present; flank scalation
heterogeneous, composed of small, stellate granules with few scattered, enlarged spinose tubercles, the largest at
the shoulder and in a single cluster; chest, belly and lower surface of tail smooth; limb scalation more tubercular,
with a few enlarged, spinose tubercles on the forearms; claws strongly bicuspid; accessory planter spines on the
soles of the fore and hind feet are present, but reduced to a few very small, soft, spinose scales at the base of the
claws; tail flattened laterally, flexing slightly downward on the distal third.
Colour in life (Fig. 7A, B): Mid-body mottled brown with two vague oblique lateral stripes; fore-body, neck,
head and upper surfaces of limbs with extensive bright green tubercles, with scattered light blue tubercles on
temporal region of head and throat and on front of belly; scales around orbit dark blue, with a red rim to the iris; tip
of casque and dorsal crest cream; enlarged scales of the dorsal crest crenulations orange, that is more extensive and
intense along the top of the tail.
Colour in preservative. Body mottled brown with no obvious lateral stripes; lower surface of neck, belly, base
of tail, soles of feet, and lower limbs pale brown, except on throat and sides of head which are dark brown.
Description of Allotype (as for holotype, unless noted): adult male, very large ventral incision; hemipenes not
everted.
Head: Supraorbital ridge reduced to a few scattered enlarged scales but with a distinct multi-scaled process
forming a ‘soft horn’ at the end of the inter-orbital crest that is slightly more pronounced than in female holotype;
interorbital ridge, shallow and composed of 12 small granular tubercles; rostral process six tubercular scales long
and five wide at base.
Body: Dorsal crest very weakly developed, reduced to eight crenulations of enlarged but not obviously spinose
scales, which are subequal in development to those of the female holotype; tail relatively long (26.5% SVL), with a
prominent hemipenal bulge; distal third of tail flexes strongly downward.
Colour in preservative: Body mottled brown with no obvious lateral stripes on the flanks. Pale brown below.
Paratype variation. In the largest female paratype (PEM R17277 ) the ‘horn’ on the supraorbital ridge is
reduced to a very small cluster of about 5 spinose tubercular scales; rostral process is very small, 3 scales long and
4 wide at base.
Size. Presumably a small species, as all except the smallest female were reproductively active. Largest
male—PEM R17281 (allotype) 32.3 + 11.6 = 43.9 mm; largest female—PEM R17277 (paratype) 48.9 + 13.2 =
62.1 mm.
Reproduction. The three adult females contain enlarged ova, albeit without signs of embryonic development:
PEM R17277, Four ova ca. 3.4 mm dia.; PEM R17278, three ova largest measuring 5.0 mm x 3.5 mm; PEM R17279,
two small ova (ca. 3.1 mm dia.). The smallest female, PEM R17280, has small developing follicles. The only male
(PEM R17281) has well-developed testes despite its small size (32.3 mm SVL).
Distribution. Restricted to the type locality; Mt. Chiperone, Zambézia Province, northern Mozambique.
Habitat. The Chiperone Massif shows habitat zonation and is surrounded by Brachystegia woodland at the
base. Chameleons were found on the southeast side of the mountain at 1000 m in wet forest dominated by Khaya
anthotheca, Strombosia schefflerii, Rawsonia burtt-davyi, and Drypetes arguta (Fig. 7C.)
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FOUR NEW SPECIES OF RHAMPHOLEON
Rhampholeon tilburyi sp. nov.
Mount Namuli Pygmy Chameleon
Synonomy: Rhampholeon platyceps Branch & Ryan 2001, p 282.
Rhampholeon tilburyi Timberlake et al. 2010, p57 nomen nudum
Rhampholeon nov. sp. (tilburyi) Timberlake et al. 2010, p61 nomen nudum
Rhampholeon platyceps (tilburyi) Timberlake et al. 2010, p61 nomen nudum
Rhampholeon Portik et al. 2013, p 416.
Etymology. The specific epithet is a patronym for our good friend Dr. Colin Tilbury for his outstanding
contributions to knowledge of African chameleons, most recently exemplified in his magnum opus, the
Chameleons of Africa (Tilbury 2010). For the last 30 years his travels throughout Africa in search of chameleons,
combined with his stunning photography, have been a source of inspiration. His studies have done much to enhance
our understanding of African chameleons, and it is with great pleasure that we name this chameleon in his honour.
Types. The type series comprises eight specimens, including:
Holotype. An adult female (PEM R14921; Fig. 8D) collected by a local guide, 30 November 1998, in the
Ukalini Forest that nestles under the south face of the main Namuli peak, Namuli Massif, Zambézia Province,
Mozambique (15˚22'S 37˚04'E, ca 1550 m a.s.l.).
Allotype. An adult male (PEM R17132 , Fig. 8A) with everted hemipenes, collected by K.A. Tolley and S. van
Noort, 26 May 2006, at night perched on a dead branch 50 cm above ground in a patch of forest dominated by
overgrown tea (Camellia sinensis) on the SDZ Cha Sarl Tea Estate at Gurué, Namuli Massif, Zambézia Province,
Mozambique (15˚26'51.6”S, 37˚00’,32.6”E, ca 839 m a.s.l.).
Paratypes. Six specimens, comprising two females (PEM R17134, Fig. 8B, same collecting details as allotype;
PEM R17135, perched on a tea bush in an overgrown patch of tea, on SDZ Cha Sarl Tea Estate at Gurué,
15˚26'42.8”S, 37˚00’,19.2”E); three males (PEM R17131, SDZ Cha Sarl Tea Estate at Gurué, 15˚26'49”S,
37˚00’,29”E; PEM R17133, same collecting details as allotype; PEM R20372, Muretha Plateau, Namuli Massif,
Zambézia Province, Mozambique (15˚23'26”S, 37˚02’,03”E, ca 1804 m a.s.l.), collected by J. Bayliss 27 May 2007;
and a very small juvenile (PEM R20373, same details as previous specimen).
Meristics. Measurements for the type series of Rhampholeon tilburyi sp. nov. are summarized in Table 8.
TAB L E 8. Measurements (mm) for the type series of Rhampholeon tilburyi sp. nov. from Mount Namuli, Mozambique
(PEM: Port Elizabeth Museum).
Diagnosis. The Mt. Namuli pygmy chameleon is referable to the Rhampholeon (subgenus Rhinodigitum
Matthee et al. 2004) by possessing a short hemipenis that is almost bag-like, acalyculate and adorned with a pair of
simple apical “horns” with a variable number of thorn-like papillae arranged on the outer aspect of the horn; having
an unpigmented parietal peritoneum, claws that are strongly bicuspid, smooth plantar surfaces, a rostral process,
PEM
R14921
Holotype
PEM
R17132
Allotype
PEM
R17131
Paratype
PEM
R17133
Paratype
PEM
R17134
Paratype
PEM
R17135
Paratype
PEM
R20372
Paratype
PEM
R20373
Paratype
Sex F MMMF FMJ
Snout-vent length 55.3 39.6 33.2 34.6 48.8 50 48.8 21.4
Tail length 15.4 12.5 10.5 11.8 10.9 13.8 15.5 7.4
Total length 70.7 52.1 43.7 46.4 59.7 63.8 64.4 28.8
Head length 21.2 12.5 11.0 11.8 15.5 20.8 17.3 8.6
Head width 10.0 7.3 5.5 5.3 9.1 6.4 9.6 4.3
Orbit diameter 5.1 3.2 2.8 3.0 3.9 4.6 4.5 2.4
Snout length 6.4 3.7 3.8 3.9 5.3 5.5 6.0 3.1
Inter-orbital 5.8 4.7 4.5 5.0 5.5 5.8 5.6 3.5
Rostral process 1.8 2.0 1.8 1.9 1.6 1.7 D 0.8
Casque to Eye 10.6 8.1 5.5 7.3 10.5 10.7 10.7 6.5
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and short tail (<27% of total length in adult males). It can be distinguished from most other species in
Rhampholeon (Rhinodigitum) by having deep inguinal (absent or indistinct in Rh. boulengeri, Rh. nchisiensis, Rh.
uluguruensis, and Rh. moyeri) and axillary pits (also absent in Rh. nchisiensis). It differs from Rh. platyceps and
Rh. maspictus sp. nov. by its smaller size (<65mm total length) and weak crenulations of dorsal crest. It differs
from all other members of the Rh. platyceps complex, including the populations from Mt Mabu, Mt Chiperone and
Mt Inago, by retaining in adult males a prominent flexure (>32˚) of the snout in front of the orbit (flat or <10˚ in
adult male Rh. platyceps and Rh. maspictus sp. nov.; <18% in the only known adult males of Rh. nebulauctor sp.
nov. and Rh. bruessoworum sp. nov.), and a narrower head (HW/HL% 49.4%; 53.2–59.8% in all other species).
Finally, the species is also genetically well differentiated from all other Rhampholeon, and all specimens examined
form a monophyletic clade from Mt. Namuli.
Description of Holotype. Adult female, viscera exposed by a single ventral incision and two lateral incisions
on left flank.
Head: Flattened, with only a small upward flexure of the snout at the front of the orbit (angling upwards at
approximately 28˚ from a line between tip of snout and top of casque); casque weak, flat with small, conical
tubercular edges; temporal crest moderate, forming a straight ridge of 7 raised, rounded tubercles, 3
rd
and last
largest; lateral crests weak, composed of small conical tubercles that demarcate the edge of the casque; temporal
crest moderate with a single row of interrupted large tubercles; parietal crest almost absent, composed of a few
enlarged tubercles in the mid-line; supraorbital ridge well marked but without obvious clusters of tubercles
(vaguely present at the posterior edge), and with a very small ‘soft horn’ of enlarged tubercles at the junction with
the shallow interorbital ridge; interorbital ridge composed of 12 small granular tubercles that demarcate the
posterior edge of a prominent frontal depression; two enlarged tubercles on inferior orbital rim; rostral ridges very
well marked, and fusing at tip of the snout which bears a rostral process (1.5 mm, in fixation flattened against
rostrum), about 7 small granules long and 5-6 granules wide at base; nares opening posterio-ventrally; no gular or
mental appendages; scales on throat homogenous, more stellate than those on crown of head and subequal in size to
those on the belly.
Body: Dorsal crest weak, composed of a double row of enlarged, rounded tubercles along the backbone; the
crest undulates between 13 equally spaced clusters of enlarged, spinose tubercles that are largest on the middle of
the body, flatter and smooth over the forelimb and sacral regions, and only vaguely visible on the tail; deep axillary
and inguinal pits are present; flank scalation heterogenous, composed of small, stellate granules with scattered,
enlarged spinose tubercles, the largest occurring over the shoulder; chest, belly and lower surface of tail smooth;
limb scalation more irregular, with numerous larger, spinose tubercles on forearms; soles of feet sub-spinose; claws
strongly bicuspid; accessory planter spines at base of claws very small, almost absent; tail gently tapering,
dorsoventrally flattened, 21.7% of total length, and covered with homogenous conical tubercles.
Colour in preservative: Body mottled brown with reddish brown reticulation on flanks; head darker above,
blotched with dark brown; belly and inner surfaces of limbs paler with darker specking; tail dark brown above and
below.
Description of Allotype (as for holotype, unless noted). Adult male, with everted hemipenes and viscera
exposed by a single, ragged ventral incision and liver tissue excised for DNA analysis.
Head: A very prominent angular flexure of the snout at the front of the orbit (approx 40˚ from line between tip
of snout and casque); supraorbital ridge well marked with clusters of tubercles at posterior and anterior level of
orbit, the latter forming a ‘soft horn’ two scales high; rostral ridge fusing anteriorly with an obvious rostral process
(1.3 mm), that is rounded in profile and composed of about 6 small granules long and 5-6 granules wide at base.
Body: Claws strongly bicuspid; accessory planter spines at the base of claws weakly developed; tail 24.0% of
total length.
Coloration in life (Fig. 8A): Head, body and tail tan to brown with orange flush along midflank and greenish
flush over back and outer surfaces of hind limbs; two prominent diagonal lines on flanks, formed from three
darkish spots joined by grey infusion; belly, throat, inner surfaces of limbs and underside of tail light tan; outer skin
of limbs darker brown; snout with wide orange band running diagonally through nostril; skin of orbit and temporal
region darker brown with scattered, intense green-blue individual tubercles; iris orange-red.
Coloration after preservation: Body very dark, almost blackish; all normal coloration lost due to fixation in
concentrated formalin.
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FIGURE 8. Rhampholeon tiburyi sp. nov. : A—Allotype (PEM R17132, K.A. Tolley); B—Paratype (PEM R17134, K Tolley);
C—Head of male paratype (PEM R20372) showing snout flexure; D—Preserved female holotype (PEM R14921); E—Manho
Forest, Mt. Namuli (J. Bayliss).
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Paratype variation. The tail varies from 18.3–21.7% of total length in females, and from 24.0–25.8% in
males; the rostral process varies from 7.9–10.4% of head length in females, and from 15.9–16.6% in males. In life
the iris of a male paratype (R17131) was reddish and the snout had an indistinct brown stripe rather than the orange
band in the allotype. In addition, a few scattered green-blue tubercles extended onto the snout, as well as on to the
orbit and temporal region. Prominent “leaf vein” dark lines on the flank were also well developed.
Size. Largest male—PEM R17132 (allotype) 39.6 + 12.5 = 52.1 mm; largest female—PEM R14921 (holotype)
55.3 + 15.4 = 70.7 mm. The smallest male (SVL 33.2 mm) still has well-developed hemipenes, indicating that it is
sexually mature (although testicular activity was not determined).
Sexual Dimorphism. Whilst the type series is limited in number, there are indications of sexual dimorphism.
Females grow considerably larger than males, and the three females in the type series have an average SVL of
51.67 mm, compared with only 34.67 mm for the three males. In addition, males have a more angular head shape
(slope 39-45˚, Fig 9B) than females (slope 22-28˚), and also proportionately longer tails and a longer rostral
process (see above). However, the small number of specimens precludes statistical confirmation. More subtle
difference in scalation details cannot be assessed until larger series are available.
Hemipenis. (based on everted hemipenes of all three males in type series). Hemipenis short with unadorned
basal and apical sections, except for a pair of curved horns that emerge prominently from the expanded, flattened
crown, and which bear well developed spines on their upper surfaces; the folds of the sulcus spermaticus flare to
drain into the flattened apical region.
Distribution. Restricted to the type locality; Mt. Namuli, Zambézia Province, northern Mozambique, in both
the evergreen forests on Manho and Ukalini forests on the Muretha Plateau (1804 m a.s.l.) at the base of the main
peaks, respectively, and also in fallow areas of tea plantations at lower elevations (838 m a.s.l).
Habitat. The Namuli Massif shows habitat zonation and is surrounded by Brachystegia woodland at the base.
Grassland and scrub with forested river valleys cover the slopes, with grassy plateaus and patches of dense moist
evergreen forest near the summit (Fig. 8E). The largest surviving blocks include the Manho Forest (c.1,000–1,100
ha) and the Ukalini Forest (c.100 ha), the latter lodged against the base of the Namuli dome. Dominant emergent
trees include Cryptocarya liebertiana, Faurea wentzeliana and Olea capensis (Timberlake et al. 2009). These
forests are under high anthropogenic threat as they are cleared for potato cultivation by surrounding rural
communities.
The allotype and most paratypes were collected at night on perches from 30-50 cm above ground in forest
adjacent to a mountain stream in a fallow areas of an operational tea estate that have overgrown into a forest. Portik
et al. (2013) noted that adults and juveniles were found sheltering on branches of small trees or on the fronds of
epiphytic ferns within Ukalini Forest. This contrasts with perches heights of 1.3–5 m recorded for Rh.
chapmanorum (Tilbury 1992).
Reproduction. The female holotype was gravid with seven almost spherical eggs (largest diameter 4.1-4.5
mm, four in the left oviduct and three in the right oviduct) that lack obvious signs of embryonic development.
Diet. The stomach of the holotype contained insect fragments, including coleopteran elytra.
Predation. A small chameleon, possibly referable to this species, was seen being carried by a Crowned
Hornbill (Tockus alboterminatus) that was flying over the canopy of Ukalini Forest, 29 November 1998 (Branch &
Ryan 2001).
Rhampholeon (Rhinodigitum) bruessoworum sp. nov.
Mount Inago Pygmy Chameleon
Synonymy: Rhampholeon sp. Bayliss et al. 2010, p17. fig. 13.
Etymology. The specific epithet honours the contributions of the brothers Carl and Darren Bruessow to the
protection of wildlife in southern Malawi, particularly via the Mount Mulanje Conservation Trust.
Types.The type series comprises three specimens, including:
Holotype.- An adult female (PEM R20375; Fig. 9A) collected by J. Bayliss, 5 September 2009, in a small
patch of wet forest at the base of a granite inselberg of Mt. Inago, Zambézia Province, Mozambique (15˚04'51”S
37˚23'37”E, ca 1478 m a.s.l.).
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FOUR NEW SPECIES OF RHAMPHOLEON
FIGURE 9. Rhampholeon bruessoworum sp. nov. : A—Holotype; B—Allotype; C—Habitat on Mt. Inago (J. Bayliss).
BRANCH ET AL.
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Allotype. An adult male (PEM R20376, Fig. 9B), same collecting details as holotype.
Paratype. An adult female (PEM R20374), same collecting details as holotype.
Meristics. Measurements of the type series of Rhampholeon bruessoworum sp. nov. are summarized in Table 9.
TAB L E 9 . Measurements (mm) for the type series of Rhampholeon bruessoworum sp. nov. from Mount Inago,
Mozambique (PEM: Port Elizabeth Museum).
Diagnosis. The Mt. Inago Pygmy Chameleon is referable to Rhampholeon (subgenus Rhinodigitum) by
possessing an unpigmented parietal peritoneum, claws that are strongly bicuspid, smooth plantar surfaces, and a
rostral process. It can be distinguished from most other species in Rhampholeon (Rhinodigitum) by having deep
inguinal (absent or indistinct in Rh. boulengeri, Rh. nchisiensis, Rh. uluguruensis, and Rh. moyeri) and axillary pits
(also absent in Rh. nchisiensis). It differs from Rh. platyceps and Rh. maspictus sp. nov. in its small size (<50 mm
SVL), relatively large rostral process in males, and weakly developed crenulations along the dorsal crest. It differs
from Rh. chapmanorum in having a relatively large rostral process in males (small in both sexes in Rh.
chapmanorum), and from all other members of the Rh. platyceps complex in Mozambique (i.e. Rh. maspictus sp.
nov., Rh. nebulauctor sp. nov. and Rh. tilburyi sp. nov.) in having a relatively longer tail in both sexes. From all
other Rhampholeon it is also genetically well differentiated, and all chameleons examined form a monophyletic
clade.
Description of Holotype. Adult female, viscera exposed by a single ventral incision.
Head: Dorsum of head flattened, with no upward flexure of the snout; casque flat, edged with weakly-defined
lateral crests that are mainly restricted to the posterior region of the casque; temporal crest weakly-developed,
comprising a single, interrupted row of large tubercles; parietal crest almost absent, composed of a few enlarged
tubercles in the mid-line; supraorbital ridges reduced to a few scattered enlarged scales but with a very small multi-
scaled process forming a ‘soft horn’ at each end of the inter-orbital ridge that passes across the crown and is
composed of 10 small granular tubercles, and that demarcate the posterior edge of a slight frontal depression;
inferior orbital rim with 4 (right) and 5 (left) enlarged tubercles; snout bordered on each side by moderately
developed rostral crests, that fuse together at the tip of the snout which is adorned with a very small, flattened
rostral process (1.6 mm) which underneath is only slightly free from the rostral, and is four small tubercular scales
long and four tubercular scales wide at its base; nares opening posterio-ventrally; no gular or mental appendages;
scales on throat homogenous, more conical but smaller than those on crown of head and subequal in size to those
on the belly.
Body: Dorsal crest very weakly developed, reduced to 9 crenulations of enlarged, but not obviously spinose
scales; crenulations most strongly developed over mid-body, reduced in size over on neck and which are present on
the tail in more reduced form; deep axillary and inguinal pits are present; flank scalation heterogeneous, composed
of small, stellate granules with few scattered, enlarged spinose tubercles, the largest at the shoulder and in two
clusters; chest, belly and lower surface of tail smooth; limb scalation more tubercular, with a few enlarged, spinose
PEM R20375
Holotype
PEM R20376
Allotype
PEM R20374
Paratype
Sex F M F
Snout-vent length 47.3 39.0 47.5
Tail length 14.8 17.1 15.3
Total length 62.1 56.1 62.7
Head length 15.0 14.5 15.9
Head width 9.2 7.9 9.7
Orbit diameter 4.4 4.1 4.9
Snout length 5.6 4.8 5.6
Inter-orbital 6.3 6.5 6.8
Rostral process 1.6 2.1 1.6
Casque to Eye 10.8 10.4 11.8
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FOUR NEW SPECIES OF RHAMPHOLEON
tubercles on the forearms; claws strongly bicuspid; accessory planter spines on the soles of the fore and hind feet
are present, but reduced to very small, soft, spinose scales at the base of the claws; tail flattened laterally, flexing
downward on the distal third.
Colour in life (based on two images of holotype, JB; Fig. 9A): Mid-body mottled brown with two narrow,
oblique purple-brown lateral stripes; dorsal surface of fore-body, neck, top of head and upper surfaces of limbs
darker brown; Throat lightly mottled cream extending onto chin and labials, which have a light yellow flush; belly
and base of tail pale brown.
Colour in preservative: Body mottled brown with two narrow oblique reddish-brown bars on mid-flanks; lower
surface of neck, belly, base of tail, soles of feet, and lower limbs pale brown.
Description of Allotype (as for holotype, unless noted): Adult male, incision along base of tail with hemipenal
muscle removed; hemipenes not everted.
Head: Parietal crest almost absent, composed of a four enlarged tubercles in the mid-line; five enlarged
tubercles on both sides of the inferior orbital rim; rostral process six small tubercular scales long and four tubercles
wide at base.
Body: Dorsal crest very weakly developed, reduced to nine crenulations of enlarged but not obviously spinose
scales, subequal in development to those of the female holotype; tail relatively long (30.5% SVL), with a
prominent hemipeneal bulge.
Colour in life (based on two images of allotype; Fig. 9B): Mid-body mottled brown with small orange brown
blotches along dorsal crest, separated by 2–3 crenulations; throat, belly and lower surfaces of limbs and tail pale
brown.
Colour in preservative: After preservation body pale brown with vestiges of two narrow oblique stripes on the
flanks; pale brown below.
Paratype variation (as for holotype, unless noted): Adult female with a large ventral incision. The ‘soft horn’
on the supraorbital ridge is very small and hardly protrudes; only four enlarged tubercles on inferior orbital rim;
plantar spines very reduced to small, soft, spinose scales.
Size. Presumably a small species, as all three specimens in the type series were sexually mature, with turgid
testes or developing ova. Largest male - PEM R20376 (allotype) 39.0 + 17.1 = 56.1 mm; largest female—PEM
R20374 (holotype) 47.5 + 15.3 = 62.7 mm.
Distribution. Restricted to the type locality; Mt. Inago, Zambézia Province, northern Mozambique.
Habitat. The Inago Massif shows habitat zonation, and is surrounded by Brachystegia woodland at the base.
The type series were collected at night in mid-altitude (~1500 m) evergreen forest at the base of a granite inselberg
(Fig. 9C). This forest type comprised relatively large trees between 20-30 m high, with the upper canopy layer
composed of species such as Drypetes natalensis, Schefflera umbellifera and Newtonia buchananii, whilst the mid-
canopy layer (< 20 m) was dominated by Chrysophyllum gorungosum, Myrianthus holstii, bridelia sp. and
Garcinia sp. These remnant forest patches are greatly reduced in size (< 10 ha), fragmented, and highly threatened
(Bayliss et al. 2010).
Conservation
Recent surveys of the montane isolates of northern Mozambique have discovered numerous new species and
important range extensions, for groups as diverse as butterflies (Congdon et al. 2010), freshwater crabs (Daniels &
Bayliss 2012), snakes (Branch & Bayliss 2009), lizards (Branch & Ryan 2001, Branch et al. 2005, Branch & Tolley
2010, Portik et al. 2013), birds (Dowsett-LeMaire 2010) and bats (Taylor et al. 2012). Many of these are forest
specialists and their survival dependent on protection of these habitats. All the new species described here are
currently known from very small areas of moist evergreen forest habitat on different montane isolates, and none of
the forests are officially protected. Forest habitats in Mozambique, and throughout most of Africa, are under severe
anthropogenic pressure from threats such as habitat destruction or degradation from mature timber extraction and
encroachment from small-scale agriculture. Forests are destroyed also for commercial agriculture, including tea
and eucalyptus/pine plantations, as well as indigenous farming. In addition to ongoing habitat loss and degradation,
chameleons from all four forest patches could be threatened by local stochastic events. The size of the forest
patches estimated using satellite imagery are: Namuli 13 km
2
; Mabu, 53 km
2
; Chiperone 20 km
2
; Inago 15 km
2
. The
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latter forest appears to be extremely fragmented and the primary habitat is possibly even smaller than estimated
here. On Namuli, chameleons have been recorded in transformed habitats of previously cultivated tea (Camellia
sinensis) gone wild and encroaching on the slopes outside the remaining primary forest. If threats are assessed to be
causing major declines to these forest habitats, the chameleons of Mt. Namuli (Rh. tilburyi sp. nov.) and Mt. Inago
(Rh. bruessoworum sp. nov.) could potentially qualify as threatened, particularly in the case of Rh. bruessoworum
sp. nov. where the forest habitat is reduced to patches < 10ha and the species is probably close to extinction.
Moreover, a number of other species of conservation concern have been discovered on Mt. Inago, including birds
such as the Thyolo Alethe (Alethe choloensis (Sclater). Endangered) and East Coast (or Gunning’s) Akalat
(Sheppardia gunningi (Haagner), Near Threatened), as well as a new species of butterfly (Cymothoe sp.) and a
possible new species of cycad (Encephalartos sp.) (Bayliss et al. 2010). Full IUCN Red List assessments are
required urgently for each new chameleon. The remaining species (e.g. Rh. champanorum and Rh. platyceps) have
been assessed for the IUCN (KAT, unpub. data) and may be listed as threatened, particularly in the case of Rh.
chapmanorum as its primary habitat has already been severely reduced in size (Tilbury 2010) to about 5 small
fragments together totaling just over 1km2 (KAT, unpub. data).
Acknowledgements
We would like to thank Werner Conradie, John Donaldson, Shelley Edwards, Lerina Kaars, Ingrid Nänni, Laché
Rossouw, Peter Ryan, Colin Tilbury, and Simon van Noort for assistance with this work, and Mr. Matthew at the SDZ
Cha Sarl Tea Estate in Gurué. The South African National Science Foundation (WRB) and South African Biodiversity
Institute (KAT) provided funding, and material was collected during the Darwin Initiative (RBG Kew Darwin Initiative
Project 15/0360). We thank Gill Watson (PEM, Bayworld) and Lemmy Mashinini (TM, Ditsong National Museum) for
allowing us to inspect material in their care. Additional support was provided by Carl Breussow (Mulanje Mountain
Conservation Trust), and Johan Marais and Mike Cunningham collected additional high altitude material of Rh.
playceps during the Mt. Mulanje herpetological survey. Our editor Salvador Carranza, and our colleague Colin Tilbury
also made valuable comment on early versions of this paper, and we regret the delayed description of these new species
prevented their incorporation into Tilbury’s monumental Chameleons of Africa, An Atlas including the Chameleons of
Europe, the Middle East and Asia. We hope that naming the Mt. Namuli pygmy chameleon in his honour is some
small recompense for his support of our studies over many years.
Additional material
Rhampholeon (Bicuspis) gorongosae: PEM R16252-53, 16608-10, Forest above Vanduzi (Carvalho), Gorongoza
Mt., Mozambique (18˚25'S, 34˚04'E), C. Tilbury. Rhampholeon Bicuspis) marshalli: PEM R9036-39, Gleneagles,
Nyanga Inyanga, Zimbabwe (18°18'00"S, 32°43'00"E), D.G. Broadley; PEM R9173-74, Mount Selinda, eastern
Zimbabwe (20°24'00"S, 32°46'00"E); PEM R16243-44, near the Vumba Botanical Gardens camp site, eastern
Zimbabwe (1932BA), C. Tilbury. Rhampholeon (Rhampholeon) spectrum: PEM R5355, Rabi Oil site (Shell
Gabon), Gabon, M. Burger; PEM R5841, Moukalaba-Doudou National Park, Gabon (0210CA), OSG Pauwels &
M Burger; PEM R15697-98, R15700-01, camp 3, 25.2km northwest of Doussala (304°), Aire d'Exploitation.
Rationelle de Faune des Monts Doudou, Ogoue-Maritime, Gabon (02°17'00"S, 10°29'00"E), M. Burger; PEM
R16261-62, near Mekambo, Gabon (0113DD), C. Tilbury. Rhampholeon (Rhampholeon) temporalis: PEM
R16254, Monga tea estate, East Usambara, Tanzania (0538BA), C. Tilbury; PEM R16521, 16255, Amani, East
Usambara, Tanzania (05˚06'S, 38˚38'E), C. Tilbury. Rhampholeon (Rhampholeon) viridis: PEM R16259-60,
remnant forest near Shengena Peak, S. Pare Mountains, Tanzania (0437BB), C. Tilbury; R16269-70, R16515-16,
Chome Forest Reserve, S Pare Mountains, Tanzania (0437BB), Joe Beraducci; R16522, 16525, 16528-29, 16712,
Kindoroko forest reserve, North Pare Mountainns, Tanzania (03˚45'S, 37˚38'E, 5750 ft. a.s.l), C. Tilbury.
Rhampholeon (Rhinodigitum) acuminatus: PEM R16265-67, 16271, Nguru Mt.s above Turiani, Tanzania
(0637BA), J. Beraducci. Rhampholeon (Rhinodigitum) boulengeri: PEM R9159-60, Medje, Haut DCR (0227CC),
C. Tilbury; R16517-18, Kalinzu Forest Reserve, Uganda (00˚23'09''S, 30˚06'23''E, 1468 m), C. Tilbury.
Rhampholeon (Rhinodigitum) chapmanorum: PEM R16245-46, Malawi Hill, Malawi (1635CC, 940 m), C.
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FOUR NEW SPECIES OF RHAMPHOLEON
Tilbury. Rhampholeon (Rhinodigitum) nchisiensis: PEM R16241-42, Nchisi Mountain, Malawi (1334AC), C.
Tilbury; R16247-48, Juniper Forest, Nyika Plateau, Malawi (1033DB), C. Tilbury; R16249, Chowo forest, Nyika
Plateau, Zambia (1033DB), C. Tilbury. Rhampholeon (Rhinodigitum) platyceps: PEM R12202, Hydro Station, Ruo
Gorge, Mt. Mulanje, Malawi (15˚58'19''S, 35˚39'18''E), W. R Branch, J. Marais & M. Cunningham; R16250-51,
Madzeka River Basin, Mt. Mlanje, Malawi (15˚45’S, 35˚38'E ; 1535DC), C. Tilbury; R16290-92, Chambe Hut
region, Mt. Mulanje, Malawi (15°54'20"S, 35°32'40"E, 1828 m asl.), W.R. Branch, J. Marais, M. Cunningham;
R16304-05, 16363-65, Cedar forest, NE facing 1.5km East of Sombani Hut, Mt. Mulanje, Malawi (15°53'30"S,
35°42'30"E), W.R. Branch, J. Marais, M. Cunningham; R16309-11, Lichenya plateau, CCAP Hut, Mt. Mulanje,
Malawi (15°58'11"S, 35°32'03"E, 2005 m asl.), W.R. Branch, J. Marais, M. Cunningham; R16312, Chambe Hut,
Mt. Mulanje, Malawi (15°54'20"S, 35°32'40"E, 1828 m asl), W. R. Branch, J. Marais, M. Cunningham; R16327,
200m West of Sombani Hut, north slopes of Mt. Mulanje, Malawi (15°52'59"S, 35°42'05"E), W.R. Branch, J.
Marais, M. Cunningham; R16359-62, Chisengoli Forest, S. slopes Mt. Mulanje, Mulanje, Malawi (15°53'30"S,
35°42'30"E, 2094 m asl.), W.R. Branch, J. Marais & M. Cunningham; R17136-40, Ruo Gorge, Mt. Mulanje (15 15'
36''S, 35 39' 15.3''E), K. Tolley & S. van Noort. Rhampholeon (Rhinodigitum) uluguruensis: PEM R16519, Nguru
Mountains, Tanzania, J.Beraducci. Rieppeleon brachyurus: PEM R9161, Tanzania, Harvey; R16263-64, grasslands
between Tomato & Koradiga, Tanzania (0537DA), J. Beraducci; R16256-57, Teak forest below Amani, E.
Usambara, Tanzania (0538BA), C. Tilbury; R16258, Kjhansi Gorge, Udzungwa Mt.s., Tanzania (0736DB), C.
Tilbury. Rieppeleon kerstenii: PEM R14997, Mavamba School, Kinondo Location, Msabweni Division, Kwale,
Kenya (0439AD), W.R. Branch; R16268, Just S. of Handeni, Tanzania (0538AC), J. Beraducci.
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... One example of this scenario is the Mount Namuli in Mozambique, surveyed repeatedly in 1931Mozambique, surveyed repeatedly in -1932Mozambique, surveyed repeatedly in , 1998Mozambique, surveyed repeatedly in , 2007Mozambique, surveyed repeatedly in , 2011Mozambique, surveyed repeatedly in , 2014Mozambique, surveyed repeatedly in , and 2016 which rendered it considerably better sampled than any surrounding areas (Vincent, 1933;Ryan et al., 1999;Timberlake et al., 2009;Portik et al., 2013;Farooq & Conradie, 2015;Conradie et al., 2016). This repeated sampling resulted in new range expansions (Farooq & Conradie, 2015), new species (Conradie et al., 2018), and a better understanding of the biogeography of the region through phylogenetic studies (Branch et al., 2014;Bittencourt-Silva et al., 2016). ...
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Mt Inago (Serra Inago) is a large granite inselberg situated approximately 50 km north east of the Namuli massif in northern Mozambique, near to the town of Malema (formally known as Entre Rios). As part of the Royal Botanic Gardens, Kew, Darwin Initiative project ‘Monitoring and Managing Biodiversity Loss on South-East Africa's Montane Ecosystems’, it was selected as a site for biological survey as it satisfied the broad selection criteria of being a large mountain inselberg close to Mt Mulanje in southern Malawi and rising to over 1500 m. One of the main aims of the project was to investigate the degree of biological similarity between Mt Mulanje and the neighbouring mountains in northern Mozambique. A 3-day reconnaissance trip was initially undertaken in 27–29 May 2008 in order to assess the overall condition of Mt Inago with a view to a more detailed investigation at a later date. During this initial visit several biological features were identified that merited a return visit. A small expedition was organised over the period 4–13 May 2009, during which the botany, butterflies and birds of the mountain were assessed. Other groups were also opportunistically collected. Mt Inago comprises a mosaic of habitat types ranging from miombo woodland, riverine forests, mid-altitude moist forest, and upland grassland at higher altitudes. During the visits several new species were discovered, notably a new species of pygmy chameleon (Rhampholeon sp.), a new species of butterfly (Cymothoe sp.), a new species of freshwater crab (Potamonautes sp.), and a possible new species of cycad (Encephalartos sp.), along with two globally threatened bird species. However, the area was found to be highly disturbed and the remaining areas of moist forest, where the majority of new species were found, are badly degraded through unsustainable levels of small-holder agriculture. Much of the previous extent of mid-altitude forest has been removed and is now confined to small patches and fringes along the base of the granite domes. Riverine forests, which help protect watercourses supplying the Malema region with good quality water, are also severely threatened. Recommendations for conservation actions are given.
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