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

Nielsen, Stuart V., Conradie, Werner, Ceriaco, Luis M. P., Bauer, Aaron M., Heinicke, Matthew P., Stanley, Edward L. & Blackburn, David C., 2020, A new species of Rain Frog (Brevicipitidae, Breviceps) endemic to Angola, ZooKeys 979, pp. 133-160 : 133

Breviceps ombelanonga sp. nov. Figs 4 , 5 , 6 , 7 Suggested common names: Angolan Rain Frog (English), Sapinho das Chuvas de Angola ( Português).

Chresonymy.1

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).

Material examined.

Holotype. UF Herp 187172 (field number MCZ A-36476), an adult male, Kawa Camp Headquarters, 1 km south of the Kwanza River, Kissama National Park (-9.183068, 13.369314, WGS-84, elevation 151 m above sea level), Luanda Province, Angola, collected by LMPC, Mariana P. Marques, Philip Pastor, and John Cavagnaro on 2 June 2016 at approx. 22:00. Paratypes (5 males, 1 female, 1 sex unknown) UF Herp 187173 (field number MCZ A-36495), an adult male, Kawa Camp Headquarters, 1 km south of the Kwanza River, Kissama National Park (-9.183068, 13.369314, WGS-84, elevation 151 m above sea level), Luanda Province, Angola, collected by LMPC, Mariana P. Marques, Philip Pastor, and John Cavagnaro on 8 June 2016; MHNCUP/ANF 320 (field number AMB 11736), sub-adult (sex unknown), Embala Seque, 14 km N of Cassumbi village (-11.083845, 16.66741), Bié Province, Angola, collected by LMPC, Mariana P. Marques, and Adam Ferguson on 16 June 2019; PEM A12800 (field number WC-4591), adult male, Cuanavale River source lake (-13.089343, 18.89485, 1396 m above sea level), Moxico Province, Angola, collected by Werner Conradie and Luke Verburgt on 24 October 2016; PEM A12537 (field number WC-3924), juvenile male, Cuito River source lake (-12.68935, 18.36012, 1435 m above sea level), Moxico Province, Angola, collected by Werner Conradie and Ninda Baptista on 18 February 2016 October; PEM A12787 (field number WC-4756), adult male, Quembo River source lake (-13.13544, 19.04397, 1375 m above sea level), Moxico Province, Angola collected by Werner Conradie on 11 November 2016; PEM A12770 (field number WC-4827), adult female, Cuando River source (-13.00334, 19.13564, 1364 m above sea level), Moxico Province, Angola, collected by Werner Conradie and James Harvey on 22 November 2016; SAIAB 204537 (field number Ang16-RB12), adult male, Quembo River source lake (-13.13583, 19.04528), Moxico Province, Angola, collected by Roger Bills on 9 November 2016.

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 ).

The new species can be distinguished from other species of Breviceps occurring in the region by the following: pale paravertebral and dorsolateral patches are lacking, although a fine dorsolateral band may be present (versus no pale paravertebral or dorsolateral spots or patches in B. mossambicus ; series of both paravertebral and dorsolateral pale spots and patches present in B. adspersus , a series of pale dorsolateral spots or patches present in B. poweri ); no conspicuous light patch above vent (present in B. poweri ); manual digit IV reaching approximately midway between the proximal and distal subarticular tubercles of manual digit III (versus nearly reaching distal subarticular tubercle of manual digit III in B. mossambicus ; not reaching or barely passing the proximal subarticular tubercle of the manual digit III in B. poweri ; similar to B. adspersus in usually not reaching the distal subarticular of manual digit III); gular region with a single uniformly dark patch (versus a pair of marbled to freckled patches in B. adspersus ).

The advertisement call of the new species (Table 5 , Fig. 3 ) can be differentiated from other potential Angolan congeners by its duration (0.175 ± 0.083 s; shorter than in B. adspersus 0.196 ± 0.047 s and B. mossambicus , 0.500 ± 0.070 s, and longer than in B. poweri , 0.140 ± 0.012 s), longer interval between consecutive calls (0.996 ± 0.133 s; B. adspersus , 0.745 ± 0.636 s; B. mossambicus , 0.710 ± 0.168 s; B. poweri , 0.743 ± 0.166 s), and a higher dominant frequency (2156 Hz; B. adspersus , 1742 ± 100 Hz; B. mossambicus , 1835 ± 107 Hz; B. poweri , 1728 ± 83 Hz). The number of pulses per call (28-34) are similar to B. adspersus (14-31), B. mossambicus (7-31), and B. poweri (10-74).

Description of the holotype.

Adult male (SUL 30.5 mm), with globular body and well-developed short limbs with medialmost and lateralmost digits reduced (Fig. 4 ; Table 3 ); snout abbreviated, protruding and angular in lateral profile, blunt and rectangular in dorsal view; eyes projecting beyond profile of head in both dorsal and ventral views; pupils horizontally elliptical; nares small oval slits, directed horizontally and visible in dorsal and lateral views; mouth narrow and directed ventrally near jaw joint; choana largely obscured by maxillae in ventral view; well-developed gland at midline of palate between choana; tongue ovoid and filling floor of mouth, and lacking median papilla; single medial bony point on lower jaw at symphysis; tympana not distinguishable; teeth absent on premaxilla, maxilla, and vomer.

Skin of dorsum and head smooth, and weakly glandular with irregular folds; skin of ventrum smooth; skin folds overlying vent creating triangular shape.

Limbs short with digits I and V short or rudimentary; webbing absent on manus and pes; nuptial pads absent and adhesive glands not discernable; relative manual digit lengths when adpressed: III>II>I>IV; only tip of first pedal digit extending beyond fleshy webbing and sole; fourth (outer) manual digit reaches midway between the large tubercle at metacarpophalangeal joint and subarticular tubercle at most proximal interphalangeal joint; finger tips conical, not expanded; several small globular palmar tubercles; single subarticular tubercles present on pedal digits II, III, and IV; pedal digit V very short, falling short of most proximal subarticular tubercle of pedal digit IV; well-developed (though not keratinized) inner metatarsal tubercle visibly longer than pedal digit III, separated from conical outer metatarsal tubercle by deep cleft.

Coloration.

In life, dorsum of body mottled dark brown on pale tan base, transitioning to golden yellow on the lateral aspects, before stark transition to solid dark brown flanks with a dark boundary becoming paler ventrally (Fig. 4 ); limbs dark grayish brown dorsally; plantar and palmar surfaces pale grayish brown; subarticular, palmar, and inner and outer metatarsal tubercles pale gray; posterior dorsum dark gray-brown with scattered pale gray spots; bold facial mask composed of broad dark brown stripe running obliquely downwards, from margin of lower eyelid towards base of arm (but not attaining it) and joining dorsolateral aspect of gular patch, giving appearance of a large dark bib; region below nares generally same coloration as dorsal and lateral rostrum, and not more darkly pigmented; lower eyelid with white opaque patch at anterior margin; margins of mouth and lateral angle of mouth off-white to cream; gular patch uniformly dark anteriorly, becoming mottled posteriorly and merging with ventral coloration; pectoral region and ventrum creamy pale gray with scattered punctate gray dots sometimes coalescing into larger spots in the gular region and laterally; iris bright orange, scattered with dark brown flecks (dark brown in preservative), with black pupil (pale gray in preservative; no mid-vertebral line; faint pale line extending across posterior hindlimbs extending between heels.

In preservative, coloration is largely similar but more muted and overall darker (Fig. 4 ).

Measurements.

Measurements of the type series are shown in Table 3 .

Variations.

All specimens resemble the holotype in the absence of a visible tympanum, and skin that is densely granular dorsally and laterally and smooth ventrally (Figs 5 - 6 ). The distal tip of manual digit IV reaches well past the proximal subarticular tubercle of manual digit III in all specimens. PEM A12770 have both manual digit II and III proximal subarticular tubercles divided. Inner and outer metatarsal tubercles not separated by a deep cleft in paratypes PEM A12800, PEM A12537, PEM A12787, PEM A12770 and SAIAB 204537.

Color and pattern in UF Herp 187173 is very similar to the holotype. Dorsum gray with scattered black spots (MHNCUP/ANF 320); red with scattered black blotches in two specimens (PEM A12537 and PEM A12770), dark brown to black with red spots and markings (PEM A12787 and PEM A12800), light brown with red spots and darker black blotches (SAIAB 204537). Interocular bar visible in all paratypes, except PEM A12537, PEM A12770 and SAIAB 204537. Light dorsolateral patches present in PEM A12878, absent in PEM A12770, dark black band present in PEM A12537. Mid-vertebral line present in most paratypes, but very faint in PEM A12537 and PEM A12770, and absent in SAIAB 204537 and MHNCUP/ANF 320. Heel-to-heel line present in all specimens, but faint in UF Herp 187173, PEM A12537, and PEM A12770. A broad, black stripe runs obliquely downwards from margin of lower eyelid towards base of arm, not reaching the shoulder in all specimens. Dark orbital band partly reaching the gular patch in all specimens, falling short in PEM A12770 (female). Anterior to the orbital bar, a broad white stripe runs down to angle of mouth and onto upper and lower lips in all individuals. Gular patch uniform dark brown to black in all paratypes, except PEM A12537 in which it is dark brown with scattered darker blotches. Pectoral region white, with scattered spots in all specimens. Ventrum white with scattered darker spots in all paratypes.

Advertisement call.

The following call description is based on a recording of a paratype male (PEM A12800) from the source lake of the Cuanavale River recorded on 24 October 2016 at 8:50 in the morning. Ambient temperature was not recorded. Frogs began calling during the daytime following heavy rains, and stopped after sunset. Call sites were among leaf litter in dense miombo woodland. The call can be described as a short whistle with a call duration of 0.064-0.342 seconds and call interval of 0.742-1.190 seconds. Each call consists of about 28-34 pulses and a dominant frequency of 2156 Hz (Table 4 , Fig. 2 ). The small number of calls from a geographically restricted sample does not allow for further statistical analysis.

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).

Genetic divergence.

Breviceps ombelanonga differs from other species within the B. mossambicus group by net uncorrected mitochondrial p -distances of at least 9% (12S) and 11% (16S; Table 2 ), as well as unique nuclear haplotypes for both RAG1 and BDNF (Fig. 1B ).

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.

Figures

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 (2013 a, 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.

Figure 2. PCA plots of ten size-corrected morphological characters from specimens of B. adspersus (n = 24), B. mossambicus (n = 9), B. poweri (n = 8), and the putative new Angolan species (n = 6) (Suppl. material 1: Table S 1), illustrating the PC 1 and PC 2 (A) and PC 2 and PC 3 (B) axes of variation, which combined represent ~ 70 % of the total variation (Table 4).

Figure 3. Spectrograms and oscillograms showing a series of notes of the putatively novel Angolan Breviceps taxon compared to three closely related congeners.

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 B. ombelanonga sp. nov.: A, B sub-adult (of unknown sex) from Embala Seque (14 km N of Cassumbi village), Bie Province (MHNCUP _ ANF 0320) C juvenile male, Cuito River source lake, Moxico Province (PEM A 12537) D adult female, Cuando River source, Moxico Province (PEM A 12770) E adult male, Quembo River source lake, Moxico Province (PEM A 12787) F adult male, Cuanavale River source lake, Moxico Province (PEM A 12800). Photographs by LMPC (A, B) and WC (C-F).

Figure 6. Variation in color and pattern within preserved paratypes of B. ombelanonga sp. nov.: A an adult male from Kawa Camp Headquarters, Luanda Province (UF Herp 187173) B sub-adult (of unknown sex) from Embala Seque, Bie Province (MHNCUPANF 320) C adult male from Cuanavale River source lake, Moxico Province (PEM A 12800) D juvenile male from Cuito River source lake, Moxico Province (PEM A 12537) E adult male from Quembo River source lake, Moxico Province (PEM A 12787) F adult female from Cuando River source, Moxico Province (PEM A 12770); and G adult male from Quembo River source lake, Moxico Province (SAIAB 204537). Photographs by SVN (A), LMPC (B), and WC (C-G).

Figure 7. Photos of typical habitat of B. 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), Bie Province C Cuanavale River source lake and associated miombo savannah woodland. Photographs by LMPC (A, B) and WC (C).