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Research Article
The Angolan bushveld lizards, genus Heliobolus Fitzinger, 1843 (Squamata: Lacertidae): Integrative taxonomy and the description of two new species
expand article infoMariana P. Marques§|, Luis M. P. Ceríaco§|, Matthew P. Heinicke, Rachal M. Chehouri, Werner Conradie#¤, Krystal A. Tolley«», Aaron M. Bauer˄
‡ Universidade do Porto, Vairão, Portugal
§ Biodiversity and Land Planning, CIBIO, Vairão, Portugal
| Universidade de Lisboa, Lisboa, Portugal
¶ University of Michigan-Dearborn, Dearborn, United States of America
# Port Elizabeth Museum, Port Elizabeth, South Africa
¤ Nelson Mandela University, George, South Africa
« South African National Biodiversity Institute, Kirstenbosch Research Centre, Cape Town, South Africa
» University of Johannesburg, Johannesburg, South Africa
˄ Villanova University, Villanova, United States of America
Open Access

Abstract

The genus Heliobolus comprises four recognized species, all endemic to sub-Saharan Africa. Of these, only Heliobolus lugubris occurs in southern Africa, its distribution extending from Angola in the west to Mozambique in the east and reaching as far south as parts of northern South Africa. Like many of the reptile species that occur in southern Africa, Heliobolus lugubris is poorly studied, and preliminary investigation suggested that it may contain cryptic diversity. The present work focusses on the Angolan population of H. lugubris and uses an integrative taxonomic approach based on morphological, coloration and DNA sequence data. The results indicate that some of the current and historical specimens of H. lugubris from Angola do not correspond to the nominotypical form, and that differences between specimens suggest the presence of two additional species, described here as Heliobolus bivari sp. nov. from the southernmost xeric/desertic regions and plateau of Namibe Province, southwestern Angola and H. crawfordi sp. nov. from the Serra da Neve inselberg north through the sub-desert coastal regions of northern Namibe, Benguela, and Kwanza Sul provinces. Nominotypical Heliobolus lugubris is confirmed to occur in Cuando Cubango Province, southeastern Angola.

Resumo

O género Heliobolus é atualmente composto por quatro espécies, todas estas endémicas da África Subsariana. Das quatro espécies, apenas uma, o Heliobolus lugubris ocorre na África Austral, estendendo-se de Angola, a oeste, Moçambique, a leste, para sul até partes do norte da África do Sul. Como muitas das espécies de répteis que ocorrem no sul de África, o Heliobolus lugubris têm sido pouco estudado. Uma investigação preliminar recente sugere que pode conter uma diversidade críptica considerável. O presente trabalho foca-se na população angolana de H. lugubris e apresenta uma revisão taxonómica integrativa com base em métodos morfológicos, de coloração e filogenéticos. Os resultados indicam que os registos atuais e históricos dos espécimes de H. lugubris no país não correspondem à forma nominotípica, e as diferenças entre exemplares sugere a presença de duas espécies adicionais, descritas aqui como Heliobolus bivari sp. nov., que ocorre nas partes mais meridionais das regiões xéricas/desérticas e áreas de planalto do sudoeste de Angola e H. crawfordi sp. nov., que ocorre desde o inselberg da Serra da Neve, em direção a norte até às regiões costeiras subdesertas. Confirma-se a ocorrência da espécie nominotipica Heliobolus lugubris na província do Cuando Cubango no sudeste de Angola.

Keywords

Angola, endemism, integrative taxonomy, lizards, reptiles

Palavras-chave

Angola, endemismo, lacertídeos, répteis, taxonomia integrativa

Introduction

In Angola, the family Lacertidae is represented by six genera – Heliobolus Fitzinger, 1843; Holaspis Gray, 1863; Ichnotropis Peters, 1854; Meroles Gray, 1838; Nucras Gray, 1838; and Pedioplanis Fitzinger, 1843 (Marques et al. 2018; Branch et al. 2019a) encompassing seventeen species. Four (three Pedioplanis and one Nucras) of these species have been described in the last decade (Conradie et al. 2012; Branch et al. 2019b; Parrinha et al. 2021). Despite the considerable increase in the number of described taxa, most taxonomic studies incorporating Angolan lacertids suggest that species-level diversity in the country is still underestimated and further taxonomic work is needed to uncover this hidden diversity (Conradie et al. 2012; Branch and Tolley 2017; Marques et al. 2018; Branch et al. 2019a,b; Parrinha et al. 2021). While the Angolan populations of Pedioplanis and Nucras have been the focus of several recent investigations (Conradie et al. 2012; Branch et al. 2019b; Baptista et al. 2020; Parrinha et al. 2021), the country’s populations of Ichnotropis and Heliobolus still lack thorough taxonomic work. Angolan Heliobolus have already been signaled by several authors as potentially comprising undescribed cryptic lineages (Branch and Tolley 2017; Marques et al. 2018; Branch et al. 2019a).

The genus Heliobolus includes four currently recognized species (Dubke et al. 2018; Uetz et al. 2022), namely the bushveld lizard, Heliobolus lugubris (Smith, 1838), Neumann’s Sand Lizard Heliobolus neumanni (Tornier, 1905), the Glittering Sand Lizard, Heliobolus nitidus (Günther, 1872), and Speke’s Sand Lizard, Heliobolus spekii (Günther, 1872). Both H. neumanni and H. spekii are restricted to East Africa, H. nitidus occurs in an extensive area in West and Central Africa, while H. lugubris is the single representative of the genus in southern Africa, being distributed in southwestern Angola, Namibia, Botswana, Zimbabwe, parts of northern South Africa, and Mozambique (Uetz et al. 2022). Heliobolus lugubris was originally described by Smith (1838) as Lacerta lugubris, from the type locality “District immediately beyond the northern frontier of the Colony” (probably referring to what is now the Northern Cape Province of South Africa). In Angola, the species has been recorded in the southwestern region, which includes the low elevation areas of Benguela, Namibe, Cunene and Cuando Cubango provinces (Marques et al. 2018). Despite not having been studied in detail, a preliminary phylogenetic analysis (Branch and Tolley 2017) incorporating Angolan material of H. lugubris sensu lato supported the presence of distinct lineages within Angolan territory.

As part of ongoing research on the Angolan herpetofauna, we collected new specimens of Angolan Heliobolus from several localities across southwestern Angola. With this additional material, it was possible to investigate the taxonomic identity of the H. cf. lugubris population in the country and to assess the diversity and distribution of the genus in Angola. Based on a combination of morphological, meristic, and coloration characters and DNA sequence data, we found evidence that supports the existence of two undescribed species of Heliobolus, closely related to H. lugubris, in Angola. In order to stabilize the taxonomy and to provide an improved estimate of the distribution of the genus in southern Africa, we describe these two lineages as new species.

Materials and methods

Material examined

Specimens collected for this study were euthanized following an approved IACUC protocol (Villanova University #1866), preserved in 10% buffered formalin in the field, and transferred to 70% ethanol for long-term storage at the conclusion of field work. Liver tissue was removed before formalin fixation and preserved in either RNAlater and transferred to 95% ethanol or directly in 95% ethanol for long-term storage (Table 1). For mensural and meristic comparisons, we examined 57 Heliobolus specimens deposited in the American Museum of Natural History (AMNH), New York, U.S.A.; the California Academy of Sciences (CAS), San Francisco, U.S.A.; Museu de História Natural e da Ciência da Universidade do Porto (MHNC-UP), Porto, Portugal; Port Elizabeth Museum (PEM), at Bayworld, Elizabeth to Gqeberha, South Africa. Additional specimens from the Natural History Museum (BMNH), London, England, U.K.; Museu Nacional de Ciencias Naturales (MNCN), Madrid, Spain; Musée d’histoire naturelle de La Chaux-de-Fonds (MHNC), Chaux-de-Fonds, Switzerland; Muséum National d’histoire naturelle de la Ville de Genève (MNHG), Genève, Switzerland; Naturhistorisches Museum Basel (NMBA), Basel, Switzerland; Senckenberg Forschungsinstitut und Naturmuseum [or Senckenberg Research Institute and Natural History Museum] (SMF), Frankfurt am Main, Germany; Museum für Naturkunde (ZMB), Berlin, Germany; Ditsong National Museum of Natural History (TM), Pretoria, Gauteng, South Africa; the Instituto Nacional da Biodiversidade e Áreas de Conservação (INBAC), Kilamba-Kiaxi, Angola; and the National Museum of Namibia (NMNW), Windhoek, Namibia, were also consulted. All specimens examined in this study are listed in the taxonomic accounts below. Information on morphological characters of species that could not be examined, as well as supplemental data, was acquired from the literature (e.g., FitzSimons 1943; Szczerbak 1975; Auerbach 1987; Branch 1998; Dubke et al. 2018).

Locality data are presented in decimal degrees and use the WGS 84 datum. Older records (non-GPS) were mostly derived from Marques et al. (2018) and georeferenced using the GEOLocate web application (https://www.geo-locate.org), elevation is reported in meters above sea level.

Table 1.

Specimens used for genetic analysis and corresponding GenBank accession numbers for genes used in the study. Locality data are reported in the form of decimal degrees and use the WGS 84 map datum. See Materials and Methods section for collection abbreviations. Institution and field number acronyms not cited in the Material and Methods section as follows: MCZ, Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts, U.S.A.; AMB, Aaron M. Bauer field numbers; FP/KTH/RSP/WP, Krystal Tolley field numbers; MBUR/MB: Marius Burger field numbers; SVN, Stuart V. Nielsen field numbers; WRB/AG, William R. Branch field numbers. All genotyped specimens of Heliobolus bivari sp. nov. and H. crawfordi sp. nov. are part of the type series.

Specimen ID Locality Genbank Accession Number
Species Field No. Museum No. 16S CO1 ND4 RAG-1
Australolacerta australis (Hewitt, 1926) KTH-569
n/a SA: Western Cape, Goedemoed-Langeberg DQ871151 MN015100 HF547725 DQ871208
AG142 PEM R24128 Angola: Namibe, 1 km SE of Farm Mucongo OP055968 OP057322 OP057281
AG143 PEM R24129 Angola: Namibe, 1 km SE of Farm Mucongo OP055969 OP057323 OP057282
AMB10595 CAS 266276 Angola: Namibe, Virei-Chipumpo OP055982 OP053373 OP057334 OP057295
AMB10596 CAS 266277 Angola: Namibe, Virei-Chipumpo OP055983 OP053374 OP057335 OP057296
AMB10597 CAS 266278 Angola: Namibe, Virei-Chipumpo OP055984 OP053375 OP057336 OP057297
AMB10598 CAS 266279 Angola: Namibe, Virei-Chipumpo OP055985 OP053376 OP057337 OP057298
AMB10599 CAS 266280 Angola: Namibe, Virei-Chipumpo OP055986 OP053377 OP057338 OP057299
Heliobolus bivari sp. nov. AMB10600 CAS 266281 Angola: Namibe, Virei-Chipumpo OP055987 OP053378 OP057339 OP057300
AMB10601 CAS 266282 Angola: Namibe, Virei-Chipumpo OP055988 OP053379 OP057340 OP057301
AMB10602 CAS 266283 Angola: Namibe, Virei-Chipumpo OP055989 OP053380 OP057341 OP057302
AMB10603 CAS 266284 Angola: Namibe, Virei-Chipumpo OP055990 OP053381 OP057342 OP057303
AMB10604 CAS 266285 Angola: Namibe, Virei-Chipumpo OP055991 OP053382 OP057343 OP057304
AMB10631 CAS 266286 Angola: Namibe, Virulundo OP055992 OP053383 OP057344 OP057305
AMB10633 CAS 266287 Angola: Namibe, Virulundo OP055993 OP053384 OP057345 OP057306
KTH09-265 PEM R17965 Angola: Huila, along Humpata-Namibe Rd OP055998 OP057349
KTH09-266 PEM R17966 Angola: Namibe, road to Espiheira OP055999 OP057350 OP057308
WRB937 PEM R21626 Angola: Namibe, road to Leba OP056018
WRB938 PEM R21630 Angola: Namibe, Leba Pass road OP056019 OP057367 OP057321
AG11 PEM R24019 Angola: Namibe, road north of Bibala OP055967 OP057280
AG17 PEM R24024 Angola: Namibe, road north of Bibala, towards Lola OP055970 OP057283
AG24 PEM R24004 Angola: Namibe, 10 km W Lola OP055971 OP057284
AMB10285 CAS 266267 Angola: Namibe, Dolondolo OP055972 OP053363 OP057324 OP057285
Heliobolus crawfordi sp. nov. AMB10286 CAS 266268 Angola: Namibe, Dolondolo OP055973 OP053364 OP057325 OP057286
AMB10287 CAS 266269 Angola: Namibe, Dolondolo OP055974 OP053365 OP057326 OP057287
AMB10289 CAS 266271 Angola: Namibe, Dolondolo OP055975 OP053366 OP057327 OP057288
AMB10333 CAS 266273 Angola: Namibe, Dolondolo OP055976 OP053367 OP057328 OP057289
AMB10348 CAS 266275 Angola: Namibe, Dolondolo OP055977 OP053368 OP057329 OP057290
WRB935 PEM R24025 Angola: Namibe, road north of Bibala towards Lola OP056017 OP057366 OP057320
ABB20 n/a Namibia: Hardap, Haruchas JX962910 EF632216
AMB6975 n/a Namibia: Kunene, Sesfontein OP055994
FP271A n/a SA: Kruger National Park OP055995 OP057346
FP291 n/a SA: Kruger National Park OP055996 OP057347 OP057307
FP295 n/a SA: Kruger National Park OP055997 OP057348
MB20857 n/a SA: Northern Cape, Farm Boseekoebaard (SE of Groblershoop) OP056000 OP057351
MB20860 n/a SA: Northern Cape, Farm Panheuwel, E of Langberge, ENE of Groblershoop OP056001 OP057352
MB20901 n/a SA: Northern Cape, Farm Boseekoebaard (SE of Groblershoop) OP056002 OP057353 OP057309
MB20940 n/a SA: Northern Cape, 36 km NE of Groblershoop OP056003 OP057354
MB21313 PEM R20956 SA: Northern Cape, Red Sands Country Lodge (14 km SW of Kuruman) OP056004 OP057355 OP057310
MB21691 n/a SA: Mpumalanga, Frischgewaagd (Bobididi) Resettlement, about 20 km S of Steelpoort OP056005 OP057356
Heliobolus lugubris (Smith, 1838) MBUR00377 n/a SA: Limpopo, Makgabeng area, W of Senwabawana (Bochum) OP056006 OP057357
MCZ A28701 MCZ R 193176 Namibia: Erongo, Farm Omandumba OP056007 MW823306
MCZ Z37870 MCZ R 184277 Namibia: Kunene, Kamanjab Rest Camp DQ871141 HF547729 DQ871199
MCZ Z37893 MCZ R 184282 Namibia: Kunene, Kamanjab Rest Camp OP056008 OP057358 OP057311
MCZ Z37894 NMNW 11134 Namibia: Kunene, Kamanjab Rest Camp DQ871142 HF547730 DQ871200
MCZ 38795 CAS 234140 SA: Limpopo, Farm Pylkop OP056009 OP057359 OP057312
MCZ 38796 CAS 234141 SA: Limpopo, Farm Pylkop OP056010 OP057313
RSP275 n/a SA: Northern Cape, Tswalu Kalahari Reserve OP056011 OP057360 OP057314
RSP285 PEM R18582 SA: Northern Cape, Tswalu Kalahari Reserve OP056012 OP057361
RSP339 PEM R18603 SA: Northern Cape, Tswalu Kalahari Reserve OP056013 OP057362 OP057315
RSP482 PEM R18642 SA: Limpopo, Venetia Limpopo Nature Reserve OP057363 OP057316
SVN364 PEM R19599 SA: Limpopo, Lapalala Reserve OP056014 OP057364 OP057317
SVN365 PEM R19562 SA: Limpopo, Lapalala Reserve OP056015 OP057365 OP057318
WP037 n/a Namibia: Sandveld Agricultural Station, 40 km N of Gobabis Omaheke OP056016 OP057319
Heliobolus spekii (Günther, 1872) n/a CAS 198923 Kenya: Rift Valley Province, Kajiado District AF206608 AF206583 EF632217
Ichnotropis capensis (Smith, 1838) AMB6007 CAS 209602 SA: KwaZulu-Natal, Kosi Bay DQ871149 MN015099 MN030223 DQ871206
Lacerta agilis Linnaeus, 1758 n/a n/a n/a DQ494823 MN015108 MN030232 EF632222
Latastia longicaudata (Reuss, 1834) n/a n/a n/a JX962911 MG700025 EF632229
AMB10374 CAS 264771 Angola: Namibe, Amélia Beach OP055978 OP053369 OP057330 OP057291
Meroles reticulatus (Bocage, 1867) AMB10375 CAS 264772 Angola: Namibe, Amélia Beach OP055979 OP053370 OP057331 OP057292
AMB10376 CAS 264773 Angola: Namibe, Amélia Beach OP055980 OP053371 OP057332 OP057293
AMB10421 CAS 264782 Angola: Namibe, Curoca River OP055981 OP053372 OP057333 OP057294
Nucras tessellata (Smith, 1838) AMB5582 CAS 206723 SA: Northern Cape, Groenriviermond DQ871143 AF206565 MG846565 HG005257
Pedioplanis namaquensis (Duméril & Bibron, 1839) AMB7577 n/a Namibia: 17 km E of Ugab crossing DQ871098 AF206566 HF547767 DQ871156
Poromera fordii (Hallowell, 1857) n/a USNM-Herp: 584231
Republic of the Congo: Lekoumou, Bambama village AF080370 MH274569 EF632240

Phylogenetic methods

We constructed a DNA sequence dataset to estimate phylogenetic relationships among Heliobolus cf. lugubris samples from Angola, Namibia, and South Africa. The dataset includes 54 ingroup samples: 28 from Angola and 26 from Namibia and South Africa, plus nine lacertid outgroup taxa Heliobolus spekii, Australolacerta australis (Hewitt, 1926), Ichnotropis capensis (Smith, 1838), Lacerta agilis Linnaeus, 1758, Latastia longicaudata (Reuss, 1834), Meroles reticulatus (Bocage, 1867), Nucras tessellata (Smith, 1838), Pedioplanis namaquensis (Duméril and Bibron, 1839), and Poromera fordii (Hallowell, 1857) (Table 1), chosen for broad phylogenetic coverage based on previous phylogenetic analyses of African lacertids (Mayer and Pavlicev 2007; Greenbaum et al. 2011; Edwards et al. 2013). Heliobolus neumanni and H. nitidus were not available for inclusion in the phylogenetic analysis. Fragments of four mitochondrial and nuclear genes were targeted for sequencing and analysis: 16S (561 bp), CO1 (665 bp), ND4 plus adjacent tRNAs (882 bp) and RAG-1 (1347 bp).

We extracted DNA from ethanol-preserved tissue samples using Qiagen DNeasy tissue kits following the manufacturer’s protocol. PCR amplification of target genes was performed using the primers listed in Table 2 and the following standard cycling conditions: 95°C initial denaturation (150 s), followed by 40 cycles of denaturation at 95°C (30 s), annealing at 46–55°C (30 s) and extension at 72°C (60 s), with a 72°C final extension (150 s). Amplified DNA was purified using either agarose gel extraction or Axygen AxyPrep magnetic beads and sequenced at the University of Michigan Advanced Genomics Core or at Macrogen (Amsterdam). Resulting sequences were assembled using MEGA X v.10.0.5 (Kumar et al. 2018), and individual gene alignments were produced using CLUSTALX v.2.1 (Larkin et al. 2007).

Table 2.

List of primers used for PCR in this study.

Gene Primer Sequence Direction Source
16S 16S-A 5’-CGCCTGTTTATCAAAAACAT-3’ Forward Palumbi (1996)
16S 16S-B 5’-CCGGTCTGAACTCAGATCACGT-3’ Reverse Palumbi (1996)
CO1 RepCO1F 5’-TNTTMTCAACNAACCACAAAGA-3’ Forward Nagy et al. (2012)
CO1 RepCO1R1 5’-ACTTCTGGRTGKCCAAARAATCA-3’ Reverse Nagy et al. (2012)
ND4 ND4-F 5’-CACCTATGACTACCAAAAGCTCATGTAGAAGC-3’ Forward Arévalo et al. (1994)
ND4 LeuR1 5’-CATTACTTTTACTTGGATTTGCACCA-3’ Reverse Arévalo et al. (1994)
RAG-1 R13 5’-TCTGAATGGAAATTCAAGCTGTT-3’ Forward Groth and Barrowclough (1999)
RAG-1 RAG-1-PedF2 5’-GGYGAYRTTGACACAATCCATCCTAT-3’ Forward Parrinha et al. (2021)
RAG-1 RAG-1-PedR1 5’-GTACTGAGGTGTATCTTGTTGCA-3’ Reverse Parrinha et al. (2021)
RAG-1 RAG-1-PedR2 5’-CAGCAAAAGCTTTCACTTGAAGT-3’ Reverse Parrinha et al. (2021)

The primary phylogenetic analysis used a concatenated alignment including all available genetic data. PartitionFinder v.2.1.1 (Lanfear et al. 2017) was used to identify the best-fitting partitioning scheme and models of evolution under the Akaike Information Criterion (AIC). A total of 11 potential partitions were considered, including 16S, tRNAs, and each codon position for the three protein-coding genes. The best scheme under the AIC used the following subdivisions and models of evolution, which were applied to subsequent analyses: 16S (GTR+I+G), tRNAs (HKY+G), CO1 position 1 (SYM+I), CO1 position 2 (TVM+I), CO1 position 3 (TrN+G), ND4 position 1 (GTR+I+G), ND4 position 2 (TVM+G), ND4 position 3 (TIM+G), RAG-1 position 1 (HKY+I), RAG-1 position 2 (HKY+I), RAG-1 position 3 (SYM+G). Using these partitions, a maximum likelihood (ML) phylogenetic analysis was run using IQ-TREE v.2.1.2 (Nguyen et al. 2014). The primary analysis used all partitions, with branch support assessed using 1000 ultrafast bootstrap replicates (Hoang et al. 2018). Strongly supported nodes were defined as those with bootstrap support (BS) > 95%, with moderately supported nodes from 70–90%. Single-gene trees were constructed separately from each alignment (16S, CO1, ND4 + tRNA, and RAG-1) and compared to one another and the concatenated phylogeny to confirm there was no significant discordance in phylogenetic tree topologies. The quality control analyses of each single gene retained the relevant partitions and models used in the primary analysis. We also used MEGA X to calculate uncorrected p-distances for ND4 to provide an estimate of sequence divergence among Heliobolus specimens. Pairwise comparisons were made between all pairs of individuals in the dataset.

Morphological methods

Specimens were measured with a digital caliper, and pholidosis was observed through a stereomicroscope. Scale nomenclature, scale counts, and measurements used in the descriptions follow Conradie et al. (2012). We recorded the following 27 characters: snout-vent length (SVL), from the snout to the vent; tail length (TL), from cloaca to tip of tail, measured only in specimens with complete original tails; head length (HL), from tip of snout to anterior tympanum border; head width (HW), from the lateral edge of the left parietal to the lateral edge of the right parietal, above the eyes; length of the forelimb (LFL), from the elbow to the wrist; length of the hindlimb (LHL), measured from knee to heel; inter-limb distance (ILD), corresponding to the distance between axillary and inguinal region; body length (BL), from the median collar plate to the cloaca; collar-snout distance (CS), from the median collar plate to the tip of the snout; number of nasal scales (NS); number of collar plates (CPL); number of gular scales (GS), in a straight line from the symphysis of the chin shields to the median collar plate; number of femoral pores (FP); number of midbody scale rows (MSR); ventral longitudinal rows (LVSR), counted from the axilla to the groin; ventral transverse rows (TVSR), counted midway between fore- and hind limbs; number of subdigital lamellae under the fourth toe (LUFT); number of supralabials anterior to the subocular (SL); number of infralabials (IL); number of supraciliaries (SC); number of supraoculares (SO); number of small granules in front of supraoculars touching frontal and prefrontal (GrSO); number of rows of granules between supraoculars and supraciliaries (GrRows); contact between parietals (CPT); contact between frontoparietals (CFP); contact between supranasals (CSN); contact between prefrontals (CPF).

Results

Phylogenetic relationships

The concatenated phylogeny (Fig. 1) recovers strongly supported relationships at basal nodes within sampled Heliobolus. Clades recovered with moderate to strong support in the single gene analyses matched those observed in the concatenated dataset, indicating no significant discordance in the data. Heliobolus cf. lugubris samples (hereafter referred to as the “H. lugubris complex”) comprise a strongly supported (BS=99%) monophyletic group sister to H. spekii (BS=100%), the only other Heliobolus species in the dataset. The H. lugubris complex itself includes three strongly supported monophyletic and geographically discrete clades (BS=100% for each clade).

One of these clades includes samples from widespread localities scattered across South Africa and Namibia. There is limited structure within this clade, with one subgroup consisting of a single specimen from Sesfontein in northwestern Namibia, one subgroup consisting of specimens from across Namibia and South Africa (BS=99%), and one subgroup containing individuals from northeastern South Africa (BS=97%). As the type locality of H. lugubris is within the central core of the distribution of this clade, we consider it representative of true H. lugubris.

Figure 1.

Maximum likelihood phylogeny of the Heliobolus lugubris complex based on a concatenated dataset of 16S, CO1, ND4, and RAG-1 sequences. The tree is rooted with exemplar African and Eurasian lacertid taxa. Bootstrap support values are provided at key nodes.

The two other clades in the H. lugubris complex are endemic to Angola but have allopatric ranges, with one occurring in far southwestern Angola and the other farther north. These two Angolan clades have previously been identified as H. lugubris (Branch and Tolley 2017; Marques et al. 2018; Branch et al. 2019a). The northern Angolan clade is recovered as sister to true H. lugubris (BS=94%), with the southern Angola clade in turn sister to this grouping. Although there are records from inland areas of southern Angola (Huíla, Cunene, and Cuando Cubango provinces) (Marques et al. 2018), there was no genetic material available from these populations for inclusion in the phylogenetic analysis. Based on the identity of geographically adjacent populations for which we do have genetic data, it is likely that the specimens from Huíla and Cunene provinces represent the southwestern Angolan lineage while the specimen from Cuando Cubango represents true H. lugubris [after the acceptance of this manuscript, the Cuando Cubango specimen was genetically confirmed to belong to true H. lugubris; W. Conradie, unpubl. data].

The three clades within the H. lugubris complex show high sequence divergence between them with uncorrected p-distances for ND4 ranging from 10.2–14.0% when comparing individuals between clades. In contrast, intra-clade values are from 0–4.6%. The inter-clade sequence divergences are comparable to species level divergence values observed between species of African Lacertidae from other genera (Mayer and Pavlicev 2007; Conradie et al. 2012; Edwards et al. 2013; Branch et al. 2019b; Parrinha et al. 2021). As our results suggest that the three major clades in the H. lugubris complex form separate genetically distinct and geographically discrete evolutionary lineages, and that each clade possesses diagnostic morphological features as described below, we recognize them herein as distinct species.

Morphology

Mensural and meristic data for the studied species are presented in Table 3. The two new Heliobolus species occurring in Angola differ from each other and from Heliobolus lugubris from southern Africa most noticeably in coloration patterns, but present very conservative external morphological characters.

One characteristic that can easily differentiate the two new Angolan species and the nominotypical H. lugubris is the coloration pattern of juveniles (Fig. 2). In H. lugubris the pale vertebral stripe is usually discontinuous (in slightly older specimens it becomes continuous but bears clear evidence that it was originally discontinuous when younger), while in the two new taxa this stripe is always continuous. This coloration pattern is, however, common to both new Angolan species and therefore is not diagnostic between them.

Detailed diagnoses for each species are provided in the taxonomic accounts section.

Table 3.

Morphometric and meristic comparisons between Heliobolus bivari sp. nov., Heliobolus crawfordi sp. nov. and Heliobolus lugubris. Data presented as “mean [minimum–maximum]”, measurements are presented in millimeters (mm). Abbreviations are those described in the Materials and Methods section.

H. bivari sp. nov. (n=22) H. crawfordi sp. nov. (n=18) H. lugubris (n=17)
SVL 54.8 [47.6–62.2] 52.2 [48.2–57.9] 52.3 [45.5–56.9]
TL 125.7 [100.7–162] 121.9 [6–19] 122.2 [106–139]
TL/SVL 2.3 [1.6–2.8] 2.3 [1.7–2.8] 2.3 [2–3]
ILL 27.7 [21.3–32.7] 26 [20.1–32.9] 25.9 [21.8–28.4]
BL 37.6 [31.1–42.9] 36.1 [23.8–42.3] 33 [22.9–36.8]
CSL 19.1 [16.3–22.7] 17.8 [15.7–20.3] 19.1 [16.6–21]
HL 12.8 [10.5–14] 11.8 [10–13.5] 12.7 [10.9–14]
HW 8.6 [7.4–11.9] 7.8 [6–19] 7.7 [4.5–9.2]
LFL 6.6 [5–8.9] 6.1 [5–7.4] 7 [6.3–7.9]
LHL 12.1 [9.8–14.1] 11.8 [10–13.2] 12 [10.7–13.2]
SL 5.5 [4–9] 4.7 [4–8] 5 [4–6]
IL 6.4 [5–7] 6.2 [5–7] 6 [5–8]
NS 3 [3–3] 3 [3–3] 3.7 [3–4]
SC 4.8 [3–7] 4.8 [4–6] 5.7 [5–7]
GrSO 8 [7–10] 15.1 [7–28] 8.3 [5–14]
GrRows 1.3 [1–3] 1.9 [1–3] 1 [1–1]
LVSR 6 [6–6] 6.1 [6–7] 6 [6–6]
TVSR 27 [25–30] 25.4 [24–27] 26.1 [23–28]
MSR 71.5 [64–82] 78 [70–90] 75.3 [64–85]
CP 6.7 [6–8] 7.1 [6–14] 8.5 [6–11]
GS 24.3 [19–29] 21.8 [18–27] 23.1 [19–27]
FP 15.3 [13–19] 13.3 [11–17] 14.3 [12–17]
LUFT 26.6 [21–34] 22 [16–26] 25.3 [23–28]
CPT Usually in contact (n=16), or in a single point (n=6); rarely without contact (n=3) Usually without contact (n=15); rarely in contact (n=3) Usually in contact (n=12); occasionally without contact (n=5)
CFP Always in contact (n=25) Always in contact (n=18) Always in contact (n=17)
CSPN Always in contact (n=25) Always in contact (n=18) Always in contact (n=17)
CPF Always in contact (n=25) Always in contact (n=18) Always in contact (n=17)

Systematics

Heliobolus bivari sp. nov.

Figs 2, 3, 4, 5, 6, 7; Tables 3, 4

Eremias lugubris [part]: Bocage 1895: 31; Boulenger 1921: 243.

Heliobolus lugubris [part]: Branch 1998: 161; Ceríaco et al. 2016: 56; Marques et al. 2018: 213; Branch et al. 2019a: 317.

Comment

The first records attributable to Heliobolus bivari sp. nov. are those provided by Bocage (1895) from Capangombe and Maconjo, followed by those of Boulenger (1921) from “Konondoto, Mossamedes”. After decades without published records, Ceríaco et al. (2016) and Branch and Tolley (2017) provided additional localities for the species in the Namibe Province. All these records were originally identified as H. lugubris. Branch and Tolley (2017) presented the first evidence that the Angolan populations of Heliobolus, namely those in Namibe, western Huíla and Benguela provinces, corresponded to two putative new taxa: Heliobolus sp. 1 and Heliobolus sp. 2, the first of which is referable to Heliobolus bivari sp. nov.

Diagnosis (adults)

A medium-sized lizard, identified to genus by the following combination of characters: well-developed limbs, slender body, elongated snout, long tail, and a distinct collar on ventral region (FitzSimons 1943; Branch 1998). Heliobolus bivari sp. nov. can be distinguished from other members of its genus by the following combination of characteristics: (1) stout medium-size body (mean SVL 54.6 mm); (2) long-tailed (mean 123.7 mm), tail more than twice the body length; (3) midbody scale rows 64–82 (mean: 71.5); (4) higher number of subdigital lamellae under the fourth toe (mean: 26.6); (5) parietals usually in contact, rarely separated; (6) cranial shields not ornamented and temporal shield smooth; (7) lateral dark marking through the ear to the posterior margin of the eye faded or totally absent; (8) absence of bright yellow dots ventrolaterally.

Comparison with other Heliobolus species

Heliobolus bivari sp. nov. is distinguished from H. neumanni by possessing a higher number of midbody scale rows (64–82 vs. 40–42). It is distinguished from H. nitidus by possessing a higher number of midbody scale rows (64–82 vs. 52–64) and by color pattern (background light-brown to orange-brown above vs. background greenish, especially on the flanks). Heliobolus bivari sp. nov. is distinguished from H. spekii by having the cranial shields not ornamented and temporal shield smooth (vs. cranial shields ornamented and temporal shield keeled). The morphological differences between H. bivari sp. nov. and H. lugubris are more subtle, possibly corresponding to the close phylogenetic relationship between the two species. Molecular phylogenetics and the interpreted distribution (H. bivari sp. nov. in southwestern Angola vs. H. lugubris in eastern Angola, Namibia, Botswana, Zimbabwe, South Africa, and Mozambique) are the best proxies for identification. However, H. bivari sp. nov. can be distinguished from H. lugubris by the presence of 1–3 rows of granules between the supraoculars and supraciliaries (vs. only one row), on average a lower number of collar plates (6.7 [6–8] vs. 8.5 [6–11]), and, on average, a higher number of subdigital lamellae under the fourth toe (26.6 [21–34] vs. 25.3 [23–28]).

Holotype

An adult female (CAS 266287, field number AMB 10633; Fig. 3), collected in Virulundo [-16.2852°, 12.9419°, 718 m a.s.l.], Namibe Province, Angola, by Luis M.P. Ceríaco, Suzana A. Bandeira, and Ishan Agarwal on 2 December 2016.

Figure 2.

Comparison of the juvenile dorsal pattern between individuals of Heliobolus bivari sp. nov., H. crawfordi sp. nov. and H. lugubris. Photos by Werner Conradie and Luis M.P. Ceríaco.

Figure 3.

Dorsal and ventral whole-body views (left) and dorsal, lateral, and ventral views of the head (right) of the holotype of Heliobolus bivari sp. nov. (CAS 266287). Photo by Luis M.P. Ceríaco.

Paratypes

All specimens from Angola. 16 specimens. Huíla Province: An adult female (PEM R17965, field number MBUR 02130), collected at an outcrop by the side of the road at the bottom of the escarpment between Humpata and the limits of Namibe Province [-15.0447°, 13.1594°, 642 m a.s.l.], by William R. Branch, Werner Conradie, John Measey and Krystal A. Tolley on 16 January 2009. Namibe Province: Ten adults, both females and males (CAS 266276–266285, field numbers AMB 10595–10604), collected at Virei-Chipumpo [-16.2793°, 12.9584°, 742 m a.s.l.], by Luis M.P. Ceríaco, Suzana A. Bandeira, and Ishan Agarwal, on 1 December 2016; an adult female (CAS 266286, field number AMB 10631), collected at the same locality as the holotype, by same collectors and date; an adult female (PEM R17966, field number MBUR 02299), collected on road from Lake Arco to Espinheira rocky valley [-15.9136°, 12.3952°, 319 m a.s.l.], by William R. Branch, Werner Conradie, John Measey and Krystal A. Tolley, on 23 January 2009; an adult male (PEM R21626, field number ANG 0296), collected 50 km E of Namibe [=Moçâmedes] on main road to Leba [-15.0156°, 12.5550°, 516 m a.s.l.], by William R. Branch, Johan Marais, James Titus-McQuillan, Ninda Baptista, and Pedro Vaz Pinto, on 8 December 2012; an adult male (PEM R21630, field number ANG 0287), collected 7.8 km from the bottom of Leba Pass [-15.0447°, 13.1595°, 642 m a.s.l.], by William R. Branch, Johan Marais, James Titus-McQuillan, Ninda Baptista, and Pedro Vaz Pinto on 8 December 2012; an adult female (PEM R24128, field number AG 142) and an adult male (PEM R24129, field number AG 143), collected 1 km SE of Farm Mucongo [-14.7867°, 12.4961°, 303 m a.s.l.], by William R. Branch, Pedro Vaz Pinto and Ninda Baptista, on 7 November 2015.

Table 4.

Mensural (in mm) and meristic counts of the holotype and paratypes of Heliobolus bivari sp. nov. Abbreviations are the same as those described in the Materials and Methods section.

CAS 266287 CAS 266276 CAS 266277 CAS 266278 CAS 266279 CAS 266280 CAS 266281 CAS 266282 CAS 266283 CAS 266284 CAS 266285 CAS 266286 PEM R 17965 PEM R 17966 PEM R 24128 PEM R 24129 PEM R 21630
Holotype Paratype Paratype Paratype Paratype Paratype Paratype Paratype Paratype Paratype Paratype Paratype Paratype Paratype Paratype Paratype Paratype
Sex
SVL 57.9 56.1 55.7 52.6 57.1 54 57.4 50.6 47.8 47.7 47.6 53.9 53.6 62.2 58.7 56.0 51.2
TL 162 133 129 141 111 121.0 126 126 108 121 111 133 115.7 100.7 147.1
TL/SVL 2.8 2.4 2.3 2.7 1.9 2.2 2.2 2.5 2.3 2.5 2.3 2.5 2.2 1.6 2.6
HL 13.5 13.3 13.5 11.8 13.0 11.0 13.2 11.0 10.5 14.0 11.0 13.7 12.1 14.0 12.7 13.9 13.6
HL/SVL 0.2 0.2 0.2 0.2 0.2 0.2 0.2 0.2 0.2 0.3 0.2 0.3 0.2 0.2 0.2 0.2 0.3
SVL/HL 4.2 4.2 4.1 4.5 4.4 4.9 4.3 4.6 4.5 3.4 4.3 3.9 4.4 4.4 4.6 4.0 3.7
HW 11.9 8.4 9.4 9.7 9.3 8.5 8.9 8.5 7.6 9.4 9.4 8.6 7.5 8.5 7.4 8.0 7.6
ILL 30.6 28.9 30.8 24.6 30.0 23.4 26.9 26.1 30.6 21.3 23.6 25.8 25.5 31.2 32.1 27.8 26.5
BL 42.9 41.0 42.5 38.2 40.0 34.8 39.0 36.3 42.9 31.1 32.5 34.9 35.9 42.9 40.1 35.0 32.5
CSL 22.7 18.0 19.0 21.8 18.2 17.1 18.2 19.5 22.7 18.5 21.8 19.2 17.2 20.2 17.6 20.3 18.4
LFL 6.5 6.8 5.6 8.9 7.2 6.5 7.3 7.5 7.0 7.1 5.0 6.7 5.7 6.5 6.2 6.4 6.0
LHL 9.8 11.2 13.3 13.4 13.1 11.0 10.2 11.4 11.1 11.4 10.0 13.3 11.8 12.8 12.2 12.7 12.9
SL 6 | 6 5 | 5 5 | 5 5 | 5 5 | 4 5 | 4 5 | 4 5 | 9 6 | 7 4 | 5 6 | 5 5 | 7 5 | 5 5 | 5 7 | 5 5 | 5 5 | 4
IL 7 | 7 7 | 7 6 | 7 6 | 7 7 | 6 7 | 6 6 | 6 7 | 7 6 | 7 6 | 6 7 | 7 6 | 7 6 | 6 6 | 6 7 | 7 6 | 6 6 | 6
SC 4 | 5 4 6 | 5 4 4 4 | 4 4 | 5 5 | 5 5 | 5 4 | 5 6 | 5 4 | 5 5 | 5 6 | 6 5 | 5 5 | 5 6 | 5
GrSO 8 | 8 7 | 7 7 | 6 7 | 8 9 | 8 8 | 8 8 | 8 8 | 8 7 | 6 10 | 9 7 | 7 8 | 7 10 | 10 8 | 7 7 | 8 5 | 6 10 | 9
GrRows 1 1 1–2 1 1 1 1 1 1 1 1 1 1 1–2 1–2 1–2 1
MSR 66 64 72 70 82 79 69 64 78 72 70 73 87 78 79 81
LVRS 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6
TVRS 25 28 27 25 30 26 28 27 27 26 27 28 25 27 25 24 25
CP 7 8 8 6 7 6 7 8 6 6 10 7 6 7 6 5 7
GS 24 19 23 23 25 23 26 29 20 27 27 26 25 26 28 23 23
FP 15 | 16 14 | 14 13 | 14 14 | 12 13 | 13 13 | 15 16 | 16 16 | 16 19 | 19 15 | 15 14 | 18 13 | 14 16 | 13 17 | 16 14 | 16 17 | 17 18 | 17
LUFT 24 27 27 27 27 33 34 26 27 23 27 27 25

Additional material

Huíla Province: Gambos Foster’s farm [-15.8500°, 14.6833°, 1189 m a.s.l.] (PEM R22039); Capelongo [-14.4667°, 16.3000°, 1453 m a.s.l.] (AMNH R47034–47036); Mulondo [-15.6500°, 15.2000°, 1156 m a.s.l.] (MNHG 1545.018). Namibe Province: Namibe-Lubango road, 2 km E of Mangueiras, south side of the road [-15.0436°, 13.1600°, 622 m a.s.l.] (CAS 254885); on main road to Leba [-15.0156°, 12.5550°, 516 m a.s.l.] (PEM R21626–21627); 7.8 km from bottom of Leba Pass [-15.0447°, 13.1595°, 642 m a.s.l.] (PEM R21628, 21629, 21631); Konondoto, Mossamedes [=Moçâmedes] [undetermined] (BMNH 1907.6.29.27–31); Caraculo [-15.0167°, 12.6667°, 463 m a.s.l.] (TM 40252–40253); Maconjo [-15.01667°, 13.2°, 865 m a.s.l.] (ZMB 7774). Cunene Province: Ponang Kuma (currently Donguena) [-17.0167°, 14.7167°, 1109 m a.s.l.] (BMNH 1907.6.29.19–26); Mupanda [-17.1333°, 15.7667°, 1114 m a.s.l.] (MHNC 91.0518, MNHG 858.098, NMBA 13357–13358); Calueque [-17.2583°, 14.5750°, 1453 m a.s.l.] (PEM R22038).

Historical localities (no extant specimens)

Namibe Province: Maconjo [-15.0167°, 13.2000°, 865 m a.s.l.] (Bocage 1895); Capangombe [-15.1000°, 13.1500°, 553 m a.s.l.] (Bocage 1895). Unknown Locality: Kuangu (BMNH 1905.5.29.15–16).

Unassigned records (records that could represent H. bivari sp. nov.)

Angola [undetermined] (MHNC 91.0515–17, 91.0519–23) – presumably a part of Mulondo specimens (Monard 1937).

Description of the Holotype

Individual in good condition. Adult female with a complete original tail (Fig. 3). Body cylindrical (SVL 57.9 mm, TL 162 mm, HL 13.5 mm), relatively stout (SVL/HL 4.3) with robust limbs. Well-defined neck and moderately sized head (HL/SVL 0.23); tail length greater than two and a half times the SVL length (TL/SVL 2.8). Additional measurements are presented in Table 5. Rostral wider than long, visible from above. Nostril pierced between three scales; supranasals in broad contact with each other behind rostral; infranasal in contact with rostral, anterior-most supralabial and anterior loreal; postnasal medium and subquadrangular, placed between the supranasal, infranasal, loreal and frontonasal. Upper head shields flat and smooth. Frontonasal hexagonal, wider than long. Prefrontals in broad contact with each other, the loreals, frontonasal and frontal. Frontal longer than wide, narrower posteriorly, in broad contact with prefrontals anteriorly and frontoparietals posteriorly; separated from supraoculars laterally by a single row of small scales. Paired frontoparietals in broad median contact, touching frontal anteriorly and the parietals and interparietal posteriorly; separated from the posterior supraocular by a single row of small granular scales. Interparietal longer than wide, arrow-shaped. Occipital round. Parietals almost as long as wide, in contact with frontoparietals and interparietal. Two rounded supraoculars in contact with each other, bordered by a group of 13 (right side) and 12 (left side) small granules which are in contact with the prefrontal, frontal, frontoparietals and parietal. One row of small granules between anterior supraocular and supraciliaries, increasing to two rows posterior to supraocular suture. Supraciliaries five, the first longest. Temporal scales irregular, small and granular. One elongated, narrow tympanic shield present on the anterior-dorsal edge of the ear opening. Subocular bordering lip, upper margin much wider than lower. Six supralabials anterior to subocular and two posterior to subocular. Infralabials seven. Lower eyelid scaly with an elongated median transparent patch that is dark-edged. Mental wider than long, in contact with first pair of chin shields and infralabials. Four pairs of chin shields, anterior three pairs in broad medial contact, fourth largest. Gular scales 24 in a straight line between symphysis of the chin shields and median collar plate. Collar free, comprising seven enlarged plates. Ventral scales smooth, in six longitudinal and 25 transverse rows. Precloacal scales homogenous and subequal, with two scales in the center. Femoral pores 15 on right leg and 16 on left leg. Lamellae under fourth toe 24. Dorsal scales small and granular. Upper forelimb and anterior hindlimb covered above by large hexagonal plates; forearm covered above by slightly imbricate and keeled scales, larger than dorsal scales, and below by enlarged plates. Hindlimbs covered above by slightly imbricate and keeled scales, larger than dorsal scales, and below by enlarged plates. Scales on tail diagonally keeled, except for those on ventral side, which are smooth.

Coloration in life

Background coloration was light brown to orange-brown, with three visible and continuous light-yellow to beige dorsal stripes, and a series of transverse dark brown markings between these stripes. Dorsolateral dark brown markings from each side of the flanks through the ear to the posterior margin of the eye faded, more visible between limbs. An interrupted whitish band is visible ventrolaterally. Yellow vertebral stripe dividing on the neck (in a Y-shape) that continues anteriorly to the posterior borders of the parietals and extends posteriorly to the base of the tail, continuous, fading on the proximal portion of the tail. Head uniformly light brown to orange-brown with white labials, with darker speckles on the supralabials which become more pronounced posteriorly. The limbs are also light brown to orange-brown, speckled with a series of yellow to white dots on their dorsal surfaces, these being most noticeable on the hindlimbs. Venter homogeneous dirty white, except the palms and soles, which are orangish; darker speckling is present laterally on the outer row of ventral scales.

Coloration in ethanol

Background color in preserved specimens is light brown to orange-brown on dorsum of head, trunk, legs and tail (Fig. 3). The dorsum presents the same pattern of coloration as in live specimens, with three continuous pale cream stripes between transverse dark markings, with the median pale stripe bifurcating (Y-shape) on the neck and extending posteriorly as a single stripe to the base of the tail. A continuous light to dark brown band extends from the flanks through the ear to the posterior margin of the eye, being most noticeable just in front of the hindlimbs. An interrupted cream band is present on the flanks between the limbs. Cream spots on limbs. Venter cream to dirty white with darker speckling present on the outermost row of ventral scales.

Variation

Variation in scalation and body measurements of the type series is reported in Table 5. The paratypes agree almost entirely with the holotype description, although in six of the paratypes (CAS 266281–266286) the subocular does not reach the lip and, therefore, does not separate the anterior and posterior supralabials. Labial markings are more faded on paratypes. Background colouration varies from orange-brown to light brown, with pale median and dorsolateral stripes. In some specimens, the pale vertebral stripe is bordered laterally by a dark brown longitudinal stripe. Some specimens have a faint to distinct darker brown dorsolateral patch, which extends from the flanks through the ear to the posterior margin of the eye. The yellow vertebral stripe divides on the neck (in a Y-shape) that continues anteriorly to the posterior borders of the parietals and extends posteriorly to the base of the tail, either continuously or interrupted (Fig. 4). Juveniles black above and below, with a continuous yellow vertebral stripe and two broken white-yellow dorsolateral stripes above the arms; tail yellow-orange; symmetrically arranged yellow to orange spots and markings on the top of the head and snout; labials present some white markings (Figs 2, 4, 5).

Figure 4.

Heliobolus bivari sp. nov. in life (CAS 266276). In a sandy riverbed between Virei and Chipumpo, Namibe Province, Angola. Photo by Ishan Agarwal.

Table 5.

Mensural (in mm) and meristic counts of the holotype and paratypes of Heliobolus crawfordi sp. nov. Abbreviations are the same as those described in the Materials and Methods section.

CAS
266269
CAS 266267 CAS 266268 CAS 266271 CAS 266273 CAS 266275 AMNH-R 41567 AMNH-R 41570 AMNH-R 41587 PEM R 21625 PEM R 22058 PEM R 22059 PEM R 24004 PEM R 24019 PEM R 24024 PEM R 24025 PEM R 24168
Holotype Paratype Paratype Paratype Paratype Paratype Paratype Paratype Paratype Paratype Paratype Paratype Paratype Paratype Paratype Paratype Paratype
Sex
SVL 51.7 50.9 51.1 49.5 53.3 53.0 53.3 53.1 48.2 53.4 53.9 51.1 57.9 49.5 53.2 49.2 52.8
TL 123 128 127 105 144 152 110.2 92.2 116
TL/SVL 2.3 2.5 2.5 2.1 2.7 2.8 2.1 1.7 2.4
HL 13.5 11 12 12.2 11.6 10.7 10 11.2 11.3 12.2 11.5 11.5 13.4 12.2 12.4 11.4 12.4
HL/SVL 0.3 0.2 0.2 0.2 0.2 0.2 0.1 0.2 0.2 0.2 0.2 0.2 0.2 0.2 0.2 0.3 0.2
SVL/HL 3.8 4.6 4.2 4.1 4.6 4.9 5.3 4.7 4.2 4.3 4.7 4.4 4.3 4.1 4.3 4.3 4.3
HW 9.5 7.4 8.7 7.8 9.6 9.1 6.5 6.5 6.0 7.3 7.4 7.1 8.1 8.1 8.1 7.6 7.4
ILL 24.9 29.8 28.7 32.9 23.2 24.7 25.5 23.2 20.1 27.6 30.3 25.5 30.0 22.3 28.2 25.0 29.5
BL 37.3 40.8 42.3 40.0 35.0 37.0 37.0 36.2 29.7 36.1 36.7 36.6 40.9 23.8 35.1 33.3 34.9
CSL 15.7 16.4 18.4 18.4 17.6 20.2 18.3 20.3 18.1 18 17.9 16.0 15.8 17.0 19.0 16.7 17.7
LFL 5.8 6.6 6.0 6.6 5.1 7.4 5.1 5.0 5.1 6.8 6.2 6.3 6.2 6.5 6.5 5.9 6.0
LHL 11.6 12.3 10.0 12.2 13.1 11.6 12 11.0 10.0 12.4 12.2 11.9 12.3 11.5 12.2 11.8 11.7
SL 4 | 4 4 | 5 4 | 5 5 | 4 4 | 5 5 | 5 4 | 4 5 | 5 4 | 4 4 | 4 5 | 5 5 | 5 5 | 5 5 | 5 5 | 5 8 | 5 5 | 5
IL 7 | 7 6 | 7 6 | 5 7 | 6 6 | 6 6 | 6 5 | 5 7 | 7 5 | 5 6 | 6 6 | 6 6 | 6 7 | 6 7 | 7 7 | 6 6 | 6 5 | 5
SC 5 | 5 5 5 | 5 5 | 5 5 | 5 6 | 6 5 | 5 4 | 4 4 | 4 5 | 4 6 | 6 5 | 5 6 | 5 5 | 6 5 | 5 5 | 5 5 | 5
GrSO 8 | 8 9 | 9 8 | 8 9 | 8 8 | 9 9 | 9 8 | 8 7 | 7 9 | 10 8 | 9 23| 22 12 | 11 12 | 10 11 | 9 12 | 11 8 | 9 10 | 8
GrRows 1 1–2 1 1 1 1 1 1–2 1 1–2 2 2 1–2 1 1 1 1
MSR 70 77 80 90 70 75 76 88 72 69 84 77 77 74 78 67 80
LVRS 6 6 7 6 6 6 6 6 6 6 6 6 6 6 6 6 6
TVRS 24 25 24 26 25 24 27 27 27 24 25 25 27 24 25 24 24
CP 6 8 6 7 7 11 7 5 6 8 6 6 11 8 8 9 6
GS 19 19 18 23 20 21 21 20 20 19 25 25 21 22 26 22 27
FP 14 | 15 16 | 16 13 | 14 13 | 12 16 | 16 16 | 15 15| 17 17 | 17 14 | 14 14 | 14 16 | 18 15 | 17 14 | 14 16 | 17 14 | 14 17 | 16 17 | 17
LUFT 20 16 19 24 20 19 24 26 20 25 25 27 23 25 24 27

Distribution, habitat and natural history notes

Heliobolus bivari sp. nov. appears to be restricted to southwestern Angola, occurring in the southernmost parts of the region in the xeric/desertic lowlands (Fig. 6). The presences of records close to Namibia’s border might indicate that the species is more widespread in similar habitats and could extend into neighboring Namibia, although this hypothesis requires confirmation. Individuals have been observed basking during daytime on sandy substrate, usually where there is sparse vegetation (e.g., shrubs) or on open sandy plains (Fig. 7). Little is known about the natural history of this species, but its ecological habits and behavior are expected to be similar to other Heliobolus species, therefore being oviparous and insectivorous. As commonly observed in juvenile H. lugubris individuals, we assume that juveniles of H. bivari sp. nov. mimic Anthia (Carabidae) ground beetles (Huey and Pianka 1977; Schmidt 2004), both through their iconic white and yellow markings on a black body, and by adopting an “arched” position when walking, imitating the general shape of a beetle.

Figure 5.

Juvenile Heliobolus bivari sp. nov. in life (specimen not collected) from Bibala [-15.0726°, 13.1128°, 501 m a.s.l.], Namibe Province, Angola. Photo by Rogério Ferreira.

Figure 6.

Distribution of Heliobolus species in Angola. Blue circles: H. crawfordi sp. nov.; dotted blue circles: historical records of H. crawfordi sp. nov.; red triangles: H. bivari sp. nov.; dotted red triangles: historical records of H. bivari sp. nov.; white stars: type localities for both species; green pentagon: H. lugubris. Colour palate represents elevation as depicted in the legend.

Figure 7.

Typical habitat of Heliobolus bivari sp. nov. Virei, Namibe Province, Angola. Photo by Ishan Agarwal.

Etymology

The species is named after the Portuguese entomologist António Bivar de Sousa (Lisbon, 1946–), a researcher at the recently defunct Instituto de Investigação Científica Tropical (IICT), Lisbon, Portugal. António Bivar de Sousa has had an important role in entomological research in Angola, being one of the main authorities on the country’s Lepidoptera. The specific epithet is a patronym in the masculine genitive singular. We propose the English common name of Bivar’s bushveld lizard, and the Portuguese common name of lagartixa de Bivar.

Heliobolus crawfordi sp. nov.

Figs 2, 6, 8, 9, 10, 11; Table 3, 5

Eremias lugubris [part]: Bocage 1867: 221; 1895: 31; Boulenger 1921: 239; Monard 1937: 75; Mertens 1938: 437.

Lamperemias lugubris [part]: Szczerbak 1975: 33.

Heliobolus lugubris [part]: Branch 1998: 161; Marques et al. 2018: 213; Branch et al. 2019a: 317.

Comment

Historical records of H. lugubris from Benguela Province (Bocage 1867, 1895; Boulenger 1921; Monard 1937; Mertens 1938; Szczerbak 1975) are all referable to H. crawfordi sp. nov. Since then, new records have expanded its known distribution to the neighboring province of Kwanza Sul and south into northern Namibe Province.

Diagnosis (adults)

A medium-sized lizard, identified to genus by the following combination of characters: well-developed limbs, slender body, elongated snout, long tail, and a distinct collar on ventral region of neck (FitzSimons 1943; Branch 1998). Heliobolus crawfordi sp. nov. can be distinguished from other members of its genus by the following combination of characteristics: (1) slender body of medium-size, mean SVL 52.2 mm; (2) long-tailed (mean 121.9 mm), tail more than twice body length; (3) midbody scale rows 70–90 (mean: 78); (4) low number of subdigital lamellae under the fourth toe (mean: 22); (5) parietals usually separated; (6) cranial shields not ornamented and temporal shield smooth; (7) lateral dark marking extending through the ear to the posterior margin of the eye; (8) presence of bright yellow dots ventrolaterally.

Comparison with other Heliobolus species

Heliobolus crawfordi sp. nov. is distinguished from H. neumanni by possessing a higher number of midbody scale rows (70–90 vs. 40–42). Heliobolus crawfordi sp. nov. is distinguished from H. nitidus by possessing a higher number of midbody scale rows (70–90 vs. 52–64) and by color pattern (background light brown to orange-brown above versus background greenish, especially on the flanks). Heliobolus crawfordi sp. nov. is distinguished from H. spekii by having the cranial shields not ornamented and temporal shield smooth (versus cranial shields ornamented and temporal shield keeled). The morphological differences between H. crawfordi sp. nov. and H. lugubris are much more subtle, indicative of the close phylogenetic relationship between the two species. Molecular data and distribution (H. crawfordi sp. nov. in western Angola versus H. lugubris in south-eastern Angola, Namibia, Botswana, Zimbabwe, South Africa, and Mozambique) are the best proxies for its identification, as is the presence of bright yellow spots ventrolaterally (absent in H. lugubris). Heliobolus crawfordi sp. nov. can potentially also be distinguished from H. lugubris by the presence of 1–3 rows of granules between the supraoculars and supraciliaries (versus only one row), by having a lower average number of collar plates (7.1 [6–14] vs. 8.5 [6–11]), a lower number of subdigital lamellae under the fourth toe (22 [16–26] vs. 25.3 [23–28]) and having the parietal scales usually separated (versus usually in contact). Juveniles of H. crawfordi sp. nov. can be distinguished from H. lugubris by the presence of a continuous white-yellow vertebral stripe (vs. a discontinuous vertebral stripe). Heliobolus crawfordi sp. nov. can be distinguished from H. bivari sp. nov. by having, on average, a lower number of subdigital lamellae under the fourth toe (22 [16–26] vs. 26.6 [21–34]), parietal scales usually separated (vs. usually in contact), a lateral dark marking through the ear to the posterior margin of the eye (vs. faded or totally absent), and presence of bright yellow spots ventrolaterally (vs. absent).

Holotype

An adult male (CAS 266269, field number AMB 10287; Fig. 8), collected in N’Dolondolo (-13.8133°, 13.1362°, 681 m a.s.l.), Namibe Province, Angola, by Luis Ceríaco, Suzana Bandeira, and Ishan Agarwal on 21 November 2016.

Figure 8.

Dorsal and ventral whole-body views (left) and dorsal, lateral and ventral views of the head (right) of the holotype of Heliobolus crawfordi sp. nov. (CAS 266269). Photos by Aaron M. Bauer.

Paratypes

All specimens from Angola. 16 specimens. Kwanza Sul Province: An adult male (PEM R24168, field number AG 16.02), collected 2–3 km W of Sumbe-Gabela road [-11.1239°, 13.9406°, 160 m a.s.l.], by William R. Branch, Pedro Vaz Pinto and Ninda Baptista, on 30 October 2015. Benguela Province: Three adult females (AMNH-R 41567, 41570, 41587), collected at Hanha [-11.5167°, 14.8167°, 1397 m a.s.l.], by Herbert Lang and Rudyerd Boulton, on 14 May 1925; an adult female (PEM R21625, field number WC-1881), collected 7 km E of Catengue on road to Cubal [-12.9994°, 13.7986°, 814 m a.s.l.], by William R. Branch, Johan Marais, James Titus-McQuillan, Ninda Baptista, and Pedro Vaz Pinto, on 3 December 2012; two adult females (PEM R22058–22059, field numbers PVP 062–063), collected 30 km NE of Lobito [-12.3411°, 13.8408°, 274 m a.s.l.], by Pedro Vaz Pinto, on 23 October 2013. Namibe Province: Five adults (females and males) (CAS 266267–266268, 266271, 266273, 266275, field numbers AMB 10285–10286, 10289, 10333, 10348), collected at same locality by same collectors as the holotype, on 21 and 23 November 2016; an adult female (PEM R24004, field number AG 024), collected 10 km W of Lola, edge of Bentiaba River, road northwest to Camacuio [-14.2903°, 13.5306°, 802 m a.s.l.], by William R. Branch, Pedro Vaz Pinto and Ninda Baptista, on 2 November 2015; an adult male (PEM R24019, field number AG 011), collected on the road north of Bibala [-14.6708°, 13.3717°, 793 m a.s.l.], by William R. Branch, Pedro Vaz Pinto and Ninda Baptista, on 2 November 2012; two adult males (PEM R24024–24025, field numbers AG 016–017), collected on the road N of Bibala towards Lola [-14.4161°, 13.5647°, 920 m a.s.l.], by William R. Branch, Pedro Vaz Pinto and Ninda Baptista, on 2 November 2015.

Additional material

Benguela Province: Huxe [-12.7167°, 13.2000°, 65 m a.s.l.] (BMNH 1906.8.24.44–45); Benguela [-12.5833°, 13.4167°, 15 m a.s.l.] (MNCN 7946); Catengue [-13.0622°, 13.7561°, 586 m a.s.l.] (PEM R26335); Cubal [-13.0333°, 14.2500°, 921 m a.s.l.] (SMF 25388). Namibe Province: base of Serra da Neve, near Malowe village [-13.8113°, 13.3322°, 879 m a.s.l.] (CAS 266120–266121, 266146; INBAC/LMPC 1221; MHNC-UP/REP 869–871).

Historical localities (no extant specimens)

Benguela Province: Benguela [-12.5833°, 13.4167°, 15 m a.s.l.] (Bocage 1867); Catumbela [-12.4333°, 13.5500°, 15 m a.s.l.] (Bocage 1895); Quissange [-12.4333°, 14.0500°, 870 m a.s.l.] (Bocage 1895); Dombe [-12.9500°, 13.1000°, 50 m a.s.l.] (Bocage 1895).

Description of the Holotype

Individual in good condition. Adult male with a complete original tail (Fig. 8). Body cylindrical (SVL 51.7 mm, TL 123 mm, HL 13.5 mm), and relatively elegant (SVL/HL 3.8), with a well-defined neck and moderately sized head (HL/SVL 0.26) and robust limbs; tail length almost two and a half times greater than SVL length (TL/SVL 2.4). Additional measurements are presented in Table 5. Rostral wider than long, visible from above. Nostril pierced between three scales; supranasals in broad contact with each other behind rostral; infranasal in contact with rostral, anterior-most supralabial and anterior loreal; postnasal medium-sized and subquadrangular, placed between the supranasal, infranasal, anterior loreal and frontonasal. Frontonasal hexagonal, wider than long. Prefrontals in broad contact with each other, the anterior loreals, frontonasal and frontal. Frontal longer than wide, narrower posteriorly, in broad contact with prefrontals anteriorly, and frontoparietals posteriorly. Paired frontoparietals in broad contact, touching frontal anteriorly and the parietals and interparietal posteriorly. Interparietal slightly longer than wide. Occipital round. Parietals in narrow contact behind the interparietal, as long as wide, in contact with frontoparietals and interparietal. Two rounded supraoculars in contact with each other, bordered by a group of 14 (right side) and 15 (left side) small granules, which separate the supraoculars from the prefrontal, frontal, frontoparietals and parietals. One row of small granules between anterior supraocular and supraciliaries, increasing to two rows posterior to supraocular suture. Supraciliaries five, the first longest. Temporal scales irregular, small and granular. One elongated tympanic shield present on the antero-dorsal margin of the ear opening. Subocular bordering lip, upper margin much wider than lower. Four supralabials anterior to subocular and two posterior to subocular. Infralabials seven. Lower eyelid scaly with a median transparent patch that is black-edged. Mental wider than long, in contact with first pair of chin shields and infralabials. Four pairs of chin shields, the first three in broad median contact, fourth pair largest. Gular scales 19 in a straight line between symphysis of the chin shields and median collar plate. Collar free, comprising six enlarged plates. Ventral scales smooth, in six longitudinal and 24 transverse rows. Precloacal scales homogeneous and subequal, with two scales in the center. Femoral pores 14 on right leg and 15 on left leg. Lamellae under fourth toe 20. Dorsal scales small and granular. Upper forelimb and anterior of hindlimb covered above by large hexagonal plates; forearm covered above by slightly imbricate and keeled scales, larger than dorsal scales, and below by enlarged plates. Hindlimbs covered above by slightly imbricate and keeled scales, larger than dorsal scales, and below by enlarged plates. Scales on tail diagonally keeled, except for those on ventral side, which are smooth or slightly keeled.

Coloration in life

Background coloration is brown to orange-brown with three continuous beige dorsal stripes, with a series of fairly broad transverse dark brown markings between stripes (Fig. 9). Dorsolateral dark brown markings continue through the ear to the posterior margin of the eye. Bright yellow spots present ventrolaterally. Vertebral stripe dividing on the neck (in a Y-shape), extending anteriorly to the posterior margins of the parietals, and extending posteriorly to the lower back, where it fades out. Lower back uniform light orange; tail orange-grey dorsally. A pale ventrolateral band arises on the posterior margin of the subocular, extending posteriorly through the ear to the hindlimb insertion; pale yellow anteriorly, becoming beige posteriorly. Head uniformly light brown. Supralabials yellow with some dark infusions; dark infusions becoming more prominent on subocular and posterior supralabials, forming a narrow dark brown stripe that continues posteriorly to the ear opening. Limbs light brown to orange-brown, speckled with large pale spots dorsally. The venter is homogeneous dirty white, except for the orangish palmar regions of the hands and feet.

Figure 9.

Heliobolus crawfordi sp. nov. in life. A Male holotype (CAS 266269); B Female (PEM R21625), from 7 km E of Catengue on road to Cubal [-12.9994°, 13.7986°, 814 m a.s.l.], Benguela Province, Angola. Photos by Luis M.P. Ceríaco (A) and William R. Branch (B).

Coloration in ethanol

Background color of preserved specimens brown to orange-brown above on dorsum of head, trunk, legs and tail (Fig. 8). The dorsum presents the same pattern of coloration as in live specimens, with three continuous pale cream stripes with short, dark lateral stripes in between, with the median pale stripe bifurcating (Y-shape) on the neck and extending posteriorly as a single stripe to the base of the tail. Dorsolateral dark brown marking continues anteriorly through the ear to the posterior margin of the eye. A beige stripe and yellow blotches are visible ventrolaterally. Cream spots on limbs. Venter cream to dirty white with no markings or speckling.

Variation

Variation in scalation and body measurements of the type series is reported in Table 6. The paratypes agree almost entirely with the holotype description. The presence of the ventrolateral yellow spots is variable from being obvious to faded in some individuals. Juveniles black above and below with a continuous yellow vertebral stripe on the dorsum and two broken stripes above the arms; tail sandy-orange; symmetrically arranged yellow to orange spots and markings on the top of the head and snout, labials present some white markings (Figs 2, 10).

Distribution, habitat and natural history notes

Heliobolus crawfordi sp. nov. seems to be restricted to the central coastal regions of Angola (Fig. 5). The species is distributed from central Namibe Province to southern Kwanza Sul Province and is widespread in Benguela Province. Similar to Heliobolus bivari sp. nov. this species is usually observed basking during daytime on the sandy ground, commonly in areas with sparse vegetation (e.g., shrubs) or on open sandy plains (Fig. 11). Little is known about the natural history of this species, but its ecological habits and behavior are expected to be similar to other Heliobolus species, being oviparous and insectivorous. As commonly observed in juvenile H. lugubris individuals, the juveniles of H. crawfordi sp. nov. also seem to imitate Anthia (Carabidae) ground beetles through their iconic white and yellow markings on a black body, their adopting an “arched” position when walking, and imitating the general shape of a beetle (MPM pers. obs.).

Figure 10.

Subadult Heliobolus crawfordi sp. nov. (CAS 266146) in life, from a sandy road to Quilengues, base of Serra da Neve [-13.8113°, 13.3322°, 587 m a.s.l.], Namibe Province, Angola. Photo by Luis M.P. Ceríaco.

Figure 11.

Type locality habitat of Heliobolus crawfordi sp. nov. on N’Dolondolo, base of Serra da Neve Inselberg, Namibe Province, Angola. Photo by Luis M.P. Ceríaco.

Etymology

The species is named after the Portuguese mammalogist João Crawford-Cabral (Funchal, 1929–2020), a researcher at the former Instituto de Investigação Científica de Angola (IICA), Sá da Bandeira [currently Lubango], Huíla Province, Angola, and the recently defunct Instituto de Investigação Científica Tropical (IICT), Lisbon, Portugal. João Crawford-Cabral played a pivotal role in the establishment and development of the zoological collections of IICA, currently housed at the Instituto Superior de Ciências de Educação (ISCED) in Lubango, Huíla Province, Angola, as well as in the publication of several important syntheses of biogeographic analyses on Angolan vertebrates. The specific epithet is a patronym in the masculine genitive singular. We propose the English common name of Crawford-Cabral’s bushveld lizard, and the Portuguese common name of lagartixa de Crawford-Cabral.

Heliobolus lugubris (Smith, 1838)

Figs 5, 12, 13, 14

Lacerta lugubris (Smith 1838: 93)

Heliobolus lugubris [part]: Branch 1998: 161; Conradie et al. 2016: 24; Marques et al. 2018: 213.

Comment

This species was described by Smith (1838) based on specimens from “District immediately beyond the northern frontier of the Colony”, probably referring to what is now the Northern Cape Province of South Africa. While the species has historically been recorded in Angola (see previous accounts), our current data indicates that the species has a much narrower distribution in the country than previously believed. The first confirmed records of the species in the country are those presented by Conradie et al. (2016) from Dirico region, Cuando Cubango Province, near the Namibian border, although it is possible that the species may occur in other areas in the southeastern part of the country.

Material examined

Cuando Cubango Province: East of Dirico Camp 7 [-17.9361°, 21.1027°, 1018 m a.s.l.] (PEM R21500).

Distribution, habitat and natural history notes

Heliobolus lugubris occurs from southeastern Angola, where it has been confirmed only from the extreme southernmost part of Cuando Cubango Province, eastwards to Mozambique, reaching as far south as parts of northern South Africa.

Figure 12.

Dorsal and ventral whole-body views (left) and dorsal, lateral and ventral views of the head (right) of Heliobolus lugubris (PEM R21500). Photos by Werner Conradie.

Figure 13.

Heliobolus lugubris in life. A Adult female (PEM R21783) from Alicedale Citrus Estate, Tshipise [-22.5716°, 30.1128°, 586 m a.s.l.], Limpopo Province, South Africa. Photo by William R. Branch. B Juvenile Heliobolus lugubris (specimen not collected) in life, from Rogella pan, Tswalu Kalahari Reserve [-27.3000°, 22.2296°, 1031 m a.s.l.], Northern Cape Province, South Africa. Photos by Werner Conradie.

Figure 14.

Habitat of Heliobolus lugubris, west of Dirico, Cuando Cubango Province, Angola. Photo by Werner Conradie.

Discussion

Southwestern Angola represents a hotspot of diversity (Ceríaco et al. 2016; Marques et al. 2018; Lobón-Rovira et al. 2022) with a high number of new reptile species described from here in the last decade (Conradie et al. 2012; Stanley et al. 2016; Ceríaco et al. 2018, 2020; Branch et al. 2019a, 2019b, 2021; Marques et al. 2019, 2020; Parrinha et al. 2021). There are still, however, several areas in the southwest that remain largely undocumented in terms of biodiversity and that require further surveys and research focus. In the last few years, the Angolan lacertids have been the subject of attention, resulting in the description of four new species (Conradie et al. 2012; Branch et al. 2019b; Baptista et al. 2020; Parrinha et al. 2021). The description of Heliobolus bivari sp. nov. and H. crawfordi sp. nov. add to this regional lacertid diversity.

The taxonomy of the genus Heliobolus has been stable since the late 19th century. The addition of these two new Angolan species raises the currently known number of bushveld lizards to six, which highlights the importance of new data from field surveys and integrative taxonomic studies, especially for such a morphologically conservative group. Heliobolus bivari sp. nov. and H. crawfordi sp. nov., despite morphological similarity, exhibit a set of subtle morphological characters that can distinguish them, and there is clear ND4 sequence divergence exceeding 10% which easily separates both lineages. It is interesting to note that one of the few consistent physical features differentiating the three Angolan Heliobolus species is their coloration patterns, not only of the adults but also of the juveniles. Although coloration in lacertids has traditionally been disregarded as a good diagnostic character for closely related taxa, especially due to the high prevalence of color polymorphism in the family Lacertidae (see Brock et al. 2022) and for the difficulty of objectively differentiating between subtle coloration differences, most recent descriptions of southern African lacertids (all backed by molecular phylogenies) have relied on coloration differences to diagnose the newly described species (Conradie et al. 2012; Branch et al. 2019b; Childers et al. 2021; Parrinha et al. 2021). This situation agrees with the results of Brock et al. (2022) that color polymorphism can be a driver of speciation. More interestingly in this case is the fact that we report here for the first time a clear and diagnostic difference in the coloration of the juvenile specimens. Juvenile H. lugubris are known to mimic noxious, acid-spraying carabid beetles of the genus Anthia in order to reduce predation (Huey and Pianka 1977) – the juveniles present a dark coloration pattern that strongly resembles the pattern of the beetles and even actively forage with arched backs, mimicking the movement of a beetle. We observed juveniles of H. crawfordi sp. nov. adopting the same movement “style” and given its close phylogenetic position, it is safe to assume that H. bivari sp. nov, juveniles also adopt this strategy. Therefore, the coloration differences of the juveniles of H. bivari sp. nov. and H. crawfordi sp. nov. against those of H. lugubris may (or may not) represent adaptive mimicry of the local colour variation between populations of Anthia beetles. It would be interesting to assess whether the juvenile color patterns of the three Heliobolus species correspond to differences in coloration of sympatric taxa and/or populations of these beetles.

Given their interpreted distributions, it appears that the two new species may be allopatric, with H. bivari sp. nov. restricted to the xeric/desertic lowlands of the southernmost parts of Namibe Province, and H. crawfordi sp. nov. limited to the arid habitats of central coastal regions of the country, from Namibe to Benguela provinces and extending to the southern areas of Kwanza Sul Province.

The ecology, natural history and behavior of the newly described species are expected to be similar to other Heliobolus species, being diurnal, oviparous and insectivorous. Despite the lack of detailed information regarding the natural history and ecology for both species, the typical habitat for both species does not appear to be threatened at present, and both are considerably widespread. Following the IUCN Red List guidelines (IUCN Standards and Petitions Committee 2019), both H. bivari sp. nov. and H. crawfordi sp. nov. would most likely be considered Least Concern. Despite this, further studies are needed to better assess their distributions, population trends, and conservation status.

Acknowledgments

This work is dedicated to all the naturalists of the defunct Instituto de Investigação Científica Tropical (IICT), Lisbon, an important institution for the study of African fauna, to which both António Bivar de Sousa and João Crawford-Cabral were affiliated. William (Bill) R. Branch, who provided the first evidence of the presence of the two undescribed Angolan lineages, is kindly acknowledged here. The present work is a result of the ongoing collaboration between the Instituto Nacional de Biodiversidade e Áreas de Conservação (INBAC) from the Ministry of Environment of Angola and its international partners. Angolan specimens were collected and exported under permits issued by the Angolan Biodiversity Assessment and Capacity Building Project (SANBI/ISCED/UAN 2009) and INBAC (155/INBAC.MINAMB/2017; 28/INBAC.MINAMB/2019). Besides these two institutions, research in Angola has been supported and fostered by the collaboration between the Southern Africa Regional Environmental Program (SAREP), the Angolan Ministry of Environment’s Institute of Biodiversity (MINAMB) and the Angola Ministry of Agriculture’s National Institute of Fish Research (INIP). Additional non-Angolan material used in this study were collected under permission of the following institutions and permit numbers: Department of Economic Development, Environment and Tourism, Limpopo Province, South Africa (018-CPM403-00001; CPM/20884/2006); Department of Tourism, Environment and Conservation, Northern Cape Province, South Africa (FAUNA 1243/2008; FAUNA 717/2009); Ministry of Environment and Tourism, Namibia (459/2001; 906/2005; 1504/2010; 1894/2014); CapeNature, Western Cape Province, South Africa (0045-AAA004-00052); Kruger National Park, South Africa (SANParks TOLKA976).

We also thank the provincial and local authorities for their support and cooperation during our fieldwork. We thank William R. Branch, Ishan Agarwal, Suzana Bandeira, Joyce Janota, James Titus-McQuillan, Pedro Vaz Pinto, Ninda Baptista and Johan Marais for their support during field work and collecting valuable material, and Shelley Edwards and interns at the South African National Biodiversity Institute for assistance in the lab. The following collection managers and curators are thanked for their support during the COVID pandemic by helping with data from the collections under their care: Lauren Scheinberg and Erica Ely from the California Academy of Sciences (CAS); David Kizirian and Lauren Vonnahme (AMNH). Special thanks to Álvaro (“Varito”) Baptista and his team from Omahua Lodge, for all the assistance, great support, and friendship during the field work. We thank Rogério Fernando for the use of his photo. We also want to thank the three anonymous reviewers that provided important comments to improve the manuscript.

This work was funded by U.S.A. National Science Foundation grants (DEB 1556255, 1556585, 1556559, 1657527), a grant from J.R.S. Biodiversity Foundation to A.M.B., M.P.H. and David C. Blackburn, the South African National Biodiversity Institute, and the National Research Foundation of South Africa (South African Biosystematics Initiative # FA2007022700016, Key International Science Capacity fund #69817 and Incentive Funding for Rated Researchers #85413), the National Geographic Okavango Wilderness Project, and the National Geographic Society Explorer Grant (NGS-73084R-20). M.P.M. was supported by Fundação para a Ciência e Tecnologia (FCT) grants (SFRH/BD/129924/2017, COVID/BD/152155/2022). Work co-funded by the project NORTE-01-0246-FEDER-000063, supported by Norte Portugal Regional Operational Programme (NORTE2020), under the PORTUGAL 2020 Partnership Agreement, through the European Regional Development Fund (ERDF).

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