Wednesday, October 28, 2020

[Herpetology • 2020] Breviceps ombelanonga • A New Species of Rain Frog (Brevicipitidae, Breviceps) endemic to Angola

Breviceps ombelanonga 
 Nielsen, Conradie, Ceríaco, Bauer, Heinicke, Stanley & Blackburn, 2020

Recent molecular phylogenetic work has found that Breviceps Merrem, 1820 comprises two major clades, one of which, the B. mossambicus group, is widely distributed across southern sub-Saharan Africa. This group is notable for harboring abundant cryptic diversity. Of the four most recently described Breviceps species, three are members of this group, and at least five additional lineages await formal description. Although Breviceps has long been known to occur in Angola, no contemporary material has been collected until recently. The three most widespread taxa, B. adspersus, B. mossambicus, and B. poweri, may all occur in Angola, but accurate species assignment remains challenging given the rampant morphological similarity between these taxa, and, until recently, the lack of genetic resources. Phylogenetic, morphological, and acoustic analyses of recently collected samples from disparate localities within Angola provide evidence for an undescribed species that is sister to B. poweri. The new species can be diagnosed from its sister taxon by lacking pale spots along the flanks, a pale patch above the vent, and a short, dark band below the nares (all present in B. poweri). Additionally, the male advertisement call differs from the three other Breviceps that might occur in Angola in having both a longer interval between consecutive calls and a higher average dominant frequency. We here describe this lineage as a distinct species, currently only known from Angola, and discuss the presence of other Breviceps taxa within Angola.

Keywords: Afrobatrachia, Anura, Breviceps ombelanonga sp. nov., cryptic species, multilocus, novel species, Sub-Saharan Africa

Figure 1. Geographic distribution and phylogenetic relationships of Breviceps spp. included in this study. 
A Map of Angola and surrounding countries with all known Breviceps spp. sampling localities indicated on legend. The proposed distributions of B. adspersus and B. poweri (blue and red polygons, respectively) are from IUCN (2013a, b), but should be considered tentative and worthy of reevaluation in light of recent studies. Furthermore, B. mossambicus is not mapped as no samples of certain identification occur west of Malawi (see Nielsen et al. 2018). 
B Multi-locus phylogeny of Breviceps, with select clades collapsed that are not relevant directly to the B. mossambicus group. The backbone is from the likelihood analysis, although Bayesian analyses produced a nearly identical topology (with any topological differences subtended by poor support). A black dot at each node indicates high support (e.g., Bayesian posterior probability > 0.95, Maximum Likelihood bootstrap > 90), while values below that cutoff are indicated for deep nodes only. Tapered bars to the right of voucher IDs indicate from which Angolan locality they were collected. 
C Median-joining networks for the two nuclear loci indicating a lack of shared haplotypes between candidate and recognized species. Hash marks indicate unique sequence differences between lineages, and black circles are hypothetical intermediate haplotypes.

Breviceps ombelanonga sp. nov.
 Suggested common names: Angolan Rain Frog (English), 
Sapinho das Chuvas de Angola (Português).
Breviceps gibbosus: Bocage (1870: 68).
Breviceps gibbosus: Bocage (1873: 227).
Breviceps mossambicus: Bocage (1895: 182); Parker (1934: 194); Monard (1937: 29, 1938: 56); Laurent (1964: 156); Cei (1977: 17, 18); Ruas (1996: 23).
Rana mossambicus: Hellmich (1957: 30).
Breviceps mossambicus-adspersus” complex: Poynton (1982: 67); Ruas (2002: 142).
Breviceps adspersus [part]: Poynton and Broadley (1985: 52).
Breviceps sp.: Marques et al. (2018: 81); Ceríaco et al. (2020: 63).
Breviceps cf. adspersus: Baptista et al. (2019: 270).

Diagnosis: A species referable to Breviceps due to the following characteristics (Poynton 1964; Minter et al. 2017): snout extremely abbreviated; mouth narrow and downturned near jaw joint; short limbs which, at rest in life, are held close to the body, not projecting beyond the body outline; digits I and V short or rudimentary; inner metatarsal tubercle well developed and notably longer than pedal digit III, narrowly separated from a prominent conical outer metatarsal tubercle. Additionally, the results of the molecular phylogenetic analyses support this species as embedded within the diversity of Breviceps, specifically within the B. mossambicus group (Fig. 1B). Breviceps ombelanonga can be diagnosed from other species of Breviceps and especially those in the B. mossambicus group by the combination of lacking a visible tympanum, males having a single, uniformly dark gular patch that is continuous with the mask extending from the eye, having generally smooth dorsal skin, lacking many small tubercles on the palmar surfaces (as in, e.g., B. branchi and B. sylvestris; FitzSimons 1930; Channing 2012), lacking pale spots along flanks and a pale patch above the vent (both present in B. poweri; Parker 1934; du Preez and Carruthers 2017), lacking short dark band below nares (as in B. poweri; du Preez and Carruthers 2017), lacking confluent inner and outer metatarsal tubercles, having a relatively narrower head, shorter thigh, and shorter manual digit III (Fig. 2; Table 4), and having an advertisement call with both a longer interval between consecutive calls and a higher average dominant frequency (Fig. 3).

Figure 4. Breviceps ombelanonga sp. nov. holotype male (UF Herp 187172): 
A in life photo B dorsal and ventral aspects C additional views of the holotype, including the left pes, frontal, right lateral, and left manus and mental.
Scale bar: 10 mm. 
Photographs by J. Cavagnaro (A) and SVN (B, C).

Figure 5. Variation in color and pattern within living paratypes of Breviceps ombelanonga sp. nov.
A, B sub-adult (of unknown sex) from Embala Seque (14 km N of Cassumbi village), Bié Province (MHNCUP_ANF 0320)
C juvenile male, Cuito River source lake, Moxico Province (PEM A12537) D adult female, Cuando River source, Moxico Province (PEM A12770)
E adult male, Quembo River source lake, Moxico Province (PEM A12787) F adult male, Cuanavale River source lake, Moxico Province (PEM A12800).
Photographs by LMPC (A, B) and WC (C–F).

Distribution: Based on our phylogenetic analysis, this species is currently confirmed from three widely separated localities and elevations ranging from near sea level to > 1400 m: i) Kissama National Park, on the outskirts of Angola’s capital city, Luanda, in coastal western Angola (Luanda Province); ii) central Angola (Bié Province); and iii) the source of the Cuanavale, Cuito, Cuando and Quembo rivers (Moxico Province). The identity of other known Angolan localities for Breviceps (black diamonds) remain uncertain without additional sampling and genetic data (Fig. 1, Appendix 1; see Marques et al. 2018).

Figure 7. Photos of typical habitat of Breviceps ombelanonga sp. nov.
A a view of the Kwanza River and bordering savannah, near the type locality, in Kissama National Park, Luanda Province
 B savannah near Embala Seque (14 km N of Cassumbi village), Bié Province 
C Cuanavale River source lake and associated miombo savannah woodland. 
Photographs by LMPC (A, B) and WC (C).

Habitat and natural history notes: 
The preferred habitat for B. ombelanonga ranges from typical western Angolan savannah, with sandy soils and vegetation dominated by Adansonia digitata, Euphorbia conspicua, Acacia welwitschii and Combretum sp., together with a good grass coverage (Grandvaux-Barbosa 1970), to dense Angolan wet miombo woodland in the east (Fig. 7). The type series was collected after gentle rains, either by hand or in traps. The holotype was first observed feeding on small, unidentified ants (family Formicidae). No information is available on egg deposit sites and clutch sizes. One of us (WC) has discovered remains of B. ombelanonga in the stomach contents of two snake species, Kladirostratus acutus (Psammophiidae; PEM R23450) and Causus bilineatus (Viperidae; PEM R23321) from the Cuando and Cuito River sources, respectively.

Etymology: The name ombelanonga is a derived combination of two words in Umbundu, a native Angolan language, for rain (ombela) and frog (anonga). The species epithet is used as an invariable noun in apposition to the generic name.

Conservation status: Given that it appears widely distributed, we suggest that B. ombelanonga be included in the IUCN category of Least Concern. The type locality lies within Kissama National Park, which grants some legal protection from major habitat degradation and loss, though the park has recently experienced significant wildfires. Additionally, the paratype localities in southeastern Angola (visited during field activities related to the National Geographic Okavango Wilderness Project 2017) are relatively pristine and ecologically intact miombo savannah that comprise an area recently proposed for formal protection.

 Stuart V. Nielsen, Werner Conradie, Luis M. P. Ceríaco, Aaron M. Bauer, Matthew P. Heinicke, Edward L. Stanley and David C. Blackburn. 2020. A New Species of Rain Frog (Brevicipitidae, Breviceps) endemic to Angola. ZooKeys. 979: 133-160. DOI: 10.3897/zookeys.979.56863

Resumo: Investigações moleculares recentes revelaram que o género Breviceps Merrem, 1820, é composto por duas linhagens principais, uma das quais, o grupo B. mossambicus, é amplamente distribuído na região sul da África subsaariana. Este grupo é notável por albergar uma abundante diversidade críptica. Das quatro espécies de Breviceps recentemente descritas, três pertencem a este grupo, e pelo menos outras cinco linhagens adicionais aguardam a sua descrição formal. Apesar de o género ser conhecido de Angola desde há muito tempo, só muito recentemente foram colhidos novos espécimes. Os três taxa mais amplamente distribuídos, B. adspersus, B. mossambicus e B. poweri podem todos, porventura, ocorrer em Angola, no entanto a correta identificação destas espécies têm sido problemática devido às semelhanças morfológicas extremas entre este taxa, e, até muito recente, a completa ausência de material genético. Análises filogenéticas, morfológicas e acústicas dos espécimes recentemente colhidos em diferentes locais de Angola apontam para a existência de uma espécie nova para a ciência, irmã de B. poweri. A nova espécie pode ser diferenciada do seu táxon irmão pela falta de marcas pálidas nos flancos, mancha pálida acima do ventre e pequena banda negra abaixo do nariz (presentes em B. poweri). Para além destas características, o chamamento dos machos difere das outras três espécies de Breviceps que podem ocorrer em Angola por ter um maior intervalo entre chamamentos consecutivos e uma maior frequência média dominante. Descrevemos aqui esta linhagem como uma espécie distinta, atualmente apenas conhecida de Angola, e discutimos a presença de outras espécies de Breviceps em Angola.

Palavras Chave: África Subsahariana, Afrobatrachia, Anura, Breviceps ombelanonga sp. nov., espécies crípticas, espécies novas, multilocus