Poyntonophrynus nambensis, Baptista & Vaz Pinto & Keates & Lobón-Rovira & Edwards & Rödel, 2023

Baptista, Ninda L., Vaz Pinto, Pedro, Keates, Chad, Lobon-Rovira, Javier, Edwards, Shelley & Roedel, Mark-Oliver, 2023, Two new Poyntonophrynus species (Anura: Bufonidae) highlight the importance of Angolan centers of endemism, Vertebrate Zoology 73, pp. 991-1031 : 991

Poyntonophrynus nambensis sp. nov.

Figures 5 , 6 , 7 , 15 , 16 , 17

Holotype.

ZMB 91787, adult female, collected in granite bedrock 200 m S of old farm paddock, in Fazenda Namba, Cuanza-Sul Province, -11.914167°, 14.820556°, 1840 m a.s.l., 03 November 2016, by Ninda L. Baptista, Pedro Vaz Pinto and William R. Branch (Figs 5 - 7 , 15 - 17 ).

Paratypes.

CHL 0326, BMNH 2021.7538, BMNH 2021.7539, 3 females, same data as holotype; BMNH 2021.7540, ZMB 91788, two males, same data as holotype; FKH-0378, FKH-0379, FKH-0380, FKH-0381, four males, collected at night on bedrock near forested stream, in Missão da Namba, Cuanza-Sul Province, -11.922078°, 14.835542°, 1740 m a.s.l., 11 February 2020, by Pedro Vaz Pinto and Javier Lóbon-Rovira; FKH-0377 unconfirmed sex, same data as FKH-0378-0381; FKH-0457, FKH-0458, FKH-0462, ZMB 91789, four females, collected approximately 12 km W of Missão da Namba, Chinhundo, Cuanza-Sul Province, -11.914685°, 14.740552°, 1730 m a.s.l, 16 October 2020, by Pedro Vaz Pinto; CHL 0472, eggs, same data as holotype.

Definition.

A medium-sized pygmy toad with females larger and rougher than males. No tarsal fold. Subarticular tubercles at the base of fingers and toes usually single, remaining ones, located at the joint between phalanges, usually double. Tympanum varies between visible and not visible. Conspicuous protuberant parotoid glands, with curved outer edge. Very conspicuous dorsal glandular warts. Usually 1.75 phalanges of toes III and V free of web, webbing between toes III and IV vestigial, not serrated. Two enlarged well-developed palmar tubercles: large, rounded to triangular-shaped outer metacarpal tubercle, and smaller oval inner metacarpal tubercle. Typical Poyntonophrynus dorsal coloration: one pale occipital blotch, one mid-dorsal blotch, one sacral blotch, and one pale blotch over arm insertion. In most individuals, the occipital and mid-dorsal pale blotches are connected in the vertebral area, resembling an hourglass shape only observed in this species. Dorsal coloration identical in both sexes, generally dull, varying in shades of grey, beige and brown with some traces of brick orange and dark brown. Dark cross-bands on limbs around the same width as pale interspaces.

Diagnosis.

Poyntonophrynus nambensis sp. nov. differs from P. pachnodes and P. fernandae sp. nov. sensu lato in having a columella. It differs from P. pachnodes in having a better-developed neopalatine. Differs from P. fernandae sp. nov. sensu lato in ventral patterning (few speckles along midline of chest, and dark line in front of arm insertion vs. scattered speckles at least on the chest), and dorsal coloration (dorsal pale hourglass-shaped blotch almost always present vs. absent), and breeding male coloration (dulls, similar to females vs. partially or completely bright yellow). It differs from P. beiranus in parotoid glands conspicuousness (conspicuous, elevated, with clearly demarcated margins vs. inconspicuous), and dorsal patterning (vertebral line absent vs. present). It differs from P. damaranus in ventral patterning (few dark speckles along midline of chest, and dark line in front of arm insertion vs. immaculate). It differs from P. dombensis in tympanum size (when visible, between 0.5 and 0.6 times internarial distance, vs. conspicuous and around 0.7 times internarial distance), and ventral patterning (few speckles along midline of chest, and dark line in front of arm insertion vs. immaculate). It differs from P. fenoulheti in parotoid glands width (thinner or around same width of eye diameter vs. wider than eye diameter). It differs from P. grandisonae in tympanum size (when visible, between 0.5 and 0.6 times internarial distance, vs. same width or wider than internarial distance) and skin texture (rough vs. leathery). It differs from P. grindleyi in pale occipital and sacral patches (present vs. absent), dorsal spines (small vs. large), and ventral coloration (few dark speckles along midline of chest, and dark line in front of arm insertion vs. dark thick ventral marbling). It differs from P. hoeschi in ventral patterning (few speckles along midline of chest, and dark line in front of arm insertion vs. immaculate). It differs from P. jordani in shape of parotoid glands (kidney-shaped vs. a cluster of glands) and pale occipital patch (present vs. absent). It differs from P. lughensis in conspicuousness of parotoid glands (conspicuous vs. inconspicuous). It differs from P. kavangensis in foot webbing (non-serrated vs. serrated), dorsal patterning (absent vertebral line vs. present), and ventral patterning (few speckles along midline of chest, and dark line in front of arm insertion vs. immaculate). It differs from P. parkeri in development of parotoid glands (elevated vs. flattened). It differs from P. vertebralis in dorsal patterning (absent vertebral line vs. present), ventral patterning (few speckles along midline of chest, and dark line in front of arm insertion vs. distinct thick dark blotches), and conspicuousness of parotoid glands (conspicuous vs. inconspicuous).

Holotype description.

External morphology. Small (SVL 31.9 mm), robust gravid female (Fig. 15 , Fig. 16B, C , all measurements in Table 7 ). SVL approximately 2.9 times head width, 3.9 times head length, 2.8 times thigh length, 2.9 times tibiofibula length, and 4.8 times forearm length. Head rounded in dorsal view. Head length approximately 0.7 head width. Snout profile rounded, snout projecting slightly beyond upper jaw. Rostral tip rounded in dorsal, ventral and lateral views. Eyes projecting laterally just beyond eyelids and not beyond margins of head in dorsal view. Around a third of the eye projecting above dorsal margin of head in lateral view. Interorbital distance approximately 0.9 times eye diameter and 1.4 times internarial distance. Eye diameter approximately 0.9 times eye-nostril distance, and 2.7 times naris to rostral tip distance. Naris small, oval, directed dorsolaterally. Tympanum visible under dissecting microscope, approximately 0.3 times eye diameter. Canthus rostralis sharp. Loreal region concave. Limbs and digits robust and well-developed. Tarsal fold absent. Digits of manus and pes elongated. Finger III length approximately 0.5 times hand length. Relative length of fingers: III> I> IV = II. Finger tips rounded, not expanded to discs. Fingers with prominent subarticular tubercles that are single at the base of fingers II, III and IV, double at the base of finger I, and bilobate under fingers III and IV, on the right hand; and always double or bilobate, except at the base of fingers III and IV, which are single, on the left hand. Plants of hands beset with supernumerary tubercles. Digits with subdigital tubercles, often double. Inner and outer metacarpal tubercles very well developed (Fig. 15C ), approximately oval in shape, the first being around twice as long as the latter. Webbing between manual digits absent. Toe IV length approximately 0.6 times foot length. Relative length of toes IV> III> V> II> I. Toe tips rounded, not expanded to discs. Prominent subarticular tubercles that are single at toe bases, the remaining being double. Double subdigital tubercles. Toes without a margin of web. Webbing between toes vestigial, only at the base of toes, webbing margin not serrated. Prominent oval inner and outer metatarsal tubercles, the first around twice longer than the latter. Inner metatarsal tubercle around half the length of toe I.

Dorsal skin rough, with brown-tipped conical spines on dorsum, arms, legs, dorsal and lateral surface of snout, top of head, and outer ring of tympanum. Ventral, gular skin, and ventral surface of limbs granular with no spines. Dorsum with very prominent rounded glandular warts, located mostly around pale mid-dorsal and sacral blotches, and dorsolaterally towards the flanks (Fig. 16B ). Parotoid glands elongated, elevated, with clearly discernible margins, with a curved outer margin, placed dorsolaterally and extending from behind the eye to slightly beyond the forearm insertion. Both kidney-shaped, but the right one consisting of a single mass, and the left broken in the middle, consisting of a junction of two masses.

Color. In life, dorsal coloration consists of a set of pale beige blotches distributed along the vertebral region, forming a symmetrical pattern (Fig. 16B ). These include a thick conspicuous chevron-shaped occipital blotch extending between eyes and directed posteriorly, connected to a mid-dorsal roundish blotch (the connection between these two blotches resembling an hourglass shape), and a small rounded sacral blotch. Rest of the dorsum with dark-, coppery- and orangey-brown mottling. Dark brown glandular warts located around the mid-dorsal blotch and towards the flanks. A thin dark brown interorbital bar, forming the anterior border of the beige occipital patch. Anterior to it, one continuous interorbital brown thin chevron directed posteriorly. Brown dorsum of head and snout. A dark brown line extending from anterior corner of eye to tip of snout. A pale beige blotch under both eyes. Conspicuous beige blotch above arm insertion. Parotoid glands brown. Eyelid brick orange. Iris olden. Pupil black ellipsoid. Flanks with dark brown (corresponding to glandular warts) and coppery markings on a pale grey background, becoming faint towards the venter. Dorsal surface of forelimbs and fingers III and IV pale beige, with dark brown cross-bands thinner than the beige inter-spaces. Dorsal surface of fingers I and II pale grey. Dorsal surface of hindlimbs (thighs and crus) beige with two dark brown cross-bands thinner than the beige inter-spaces. Dark cross-bands on thigh, crus and feet touching when legs flexed. Ventral skin almost immaculate white, with dark spots placed in midline of pectoral region, and a dark line curving down in front of insertion of arm (Fig. 16C ). Plantar surface of manus and pes grey with white tubercles. Preserved specimen, after six years in ethanol, pale beige and grey blotches turned pale grey, and dark blotches (shades of brown) turned dark grey (Fig. 15 ). A large grey blotch on mid chest corresponding to area where formalin was injected for preservation, unrelated to natural pigmentation (Fig. 15B ).

Osteology (Fig. 17 ). Skull wider than long, without ornamentation on dermal roofing bones. Jaw joint anterior to otic region. Parotic plate incompletely ossified but synostosed to frontoparietal. Premaxillae lacking teeth, with robust pars dentalis and robust alary process that is taller than wide, and widely separated from nasals. Maxillae and mandibles without teeth. Quadratojugals thin and elongate with broad articulation with maxillae. Pterygoids slender, with long medially curved anterior ramus with broad articulation with adjacent maxilla, short posterior ramus approaching jaw joint, and short medial ramus approaching prootic. Vomers large and plate-like, without teeth, with short and pointy mediolateral processes, and reduced anterior processes. Neopalatines thin flat rods, approaching but not in contact with edges of sphenethmoid, maxillae, and anterior ramus of pterygoid distally. Septomaxillae present at anterior margin of nasal capsule. Prominent sphenethmoid co-ossified across midline and visible in dorsal view between nasals and frontoparietals. Parasphenoid narrowing anteriorly and exhibiting a small bifurcation at its anterior extent. Squamosals reduced, with dorsalmost otic region, reduced zygomatic ramus present, and vestigial ventral ramus separate from main bone. Prootic poorly ossified. Columella well ossified, with pars interna plectri developed as an expanded knob on medial end of pars media plectri, which is antero-posteriorly compressed. Posteromedial processes of hyoid ossified and slender.

Eight distinct, procoelous, non-imbricating, not synostosed presacral vertebrae. Atlas without transverse processes, with widely separated cotyles. Sacrum procoelous with laterally expanded transverse processes, bearing expanded diapophyses. Urostyle long and thin with weakly developed dorsal ridge on proximal half, a small pointy posteriorly directed protrusion on the right side of its right cotyle, and bicondylar articulation with sacrum. Pectoral girdle firmisternal, with widely spaced and slender coracoids. Clavicles slender, nearly reaching one another. Scapulae are stout, directed laterally but strongly curving dorsally at lateral extent. No visible ossified sternum or omosternum. Pelvic girdle comprising ilium, pubis, and ischium. Shaft of ilium long and slender, lacking a dorsal crest. Radioulna shorter than humerus. Humerus bearing a ventral crest on proximal half, and without medial and lateral crest. Phalangeal formula for manus 2-2-3-3. Ossified prepollex formed by two elements, a rounded proximal element, and a thinner, elongated and pointy distal element. Tips of terminal manual phalanges weakly expanded into small knobs. Tibiofibula around same length as femur. Phalangeal formula for pes 2-2-3-4-3. Tips of terminal pedal phalanges weakly expanded as in fingers. A single ossified prehallux.

Variation.

Males (SVL 24.4-26.4 mm, n = 6) smaller than females (30.7-34.9 mm, n = 8). Males with a dense covering of minute dark asperities on upper and inner surfaces of finger I and to a lesser extent on the upper medial surface of finger II and inner metacarpal tubercle. Males with smoother skin than females, with few spines on snout, different from females, which have a rough dorsal skin. Parotoid glands on males less conspicuous and more flattened than on females.

Measurements of the type series are presented in Table 7 , and variation in selected body ratios is summarized in Figure 4 . Relative length of fingers sometimes III> IV> II = I. Relative length of toes sometimes IV> III> V> II> I, rarely IV> V> III> II> I. Variation on subarticular tubercles based on five paratypes (ZMB 91788-9 and BMNH 2021.7538-40). Subarticular tubercles at the base of fingers: always double or bilobate on fingers I and II; always single on finger III except for ZMB 91788 on right hand, which is bilobate, and for BMNH 2021.7540 and ZMB 91788 on both hands, which are double; always single on finger IV except for BMNH 2021.7540 on right hand, and for BMNH 2021.7539 on left hand, which are double. Subarticular tubercles at the joint between finger phalanges: always double on finger III; always single on finger IV, except for BMNH 2021.7538 on right hand, which is double, and for ZMB 91788 on right hand, which is absent. Subarticular tubercles at the base of toes: always double on toe I, except for BMNH 2021.7538 on both feet and for BMNH 2021.7540 on left foot, which are single, and for ZMB 91788 and BMNH 2021.7539 on left feet, which are not visible; always single on toe II, except for BMNH 2021.7539 which are double on both feet; always single on toes III-V. Subarticular tubercles at the joint between toe phalanges: always double on toe III; always double on toe IV except for ZMB 91790, distal one on right foot, which is single; always single on finger V, except for BMNH 2021.7540 on both feet and for ZMB 91788 on right foot which are absent, and ZMB 91789, which is double on both feet. Tympanum’s conspicuousness variable, being conspicuous (CHL 0326, FKH-0462), visible (BMNH 2021.7540, FKH-0377, FKH-0380, FKH-0457, ZMB 91788), and not visible in almost half of the collected specimens (BMNH 2021.7538-9, FKH-0378-9, FKH-0381, FKH-0458, ZMB 91789). Metatarsal tubercles oval, outer between half and two thirds the length of inner. Male paratypes usually with no spines, except on snout. Parotoid glands kidney-shaped, but very often in paratypes they look like the holotype’s left one, broken in the middle, consisting of two masses. Plants of hands and feet beset with supernumerary tubercles, less densely on feet than on hands. Spine tips vary in coloration between white, beige and brown.

Coloration varying in shades of grey, beige and brown with some traces of brick orange and dark brown (Fig. 16 ). Color intensity of pale dorsal blotches varied from pale grey (BMNH 2021.7538, BMNH 2021.7540, CHL 0326, FKH-0380, ZMB 91788) to very dark grey (FKH-0377-81, FKH-0457-8, FKH-0462, ZMB 91789). Ventral markings, anterior surface of forearm, posterior surface of tarsus, and palm of manus and pes with similar variation of color intensity. Except for BMNH 2021.7539, which has an immaculate venter, all individuals have dark spots placed along midline of pectoral region, and a dark line curving down in front of insertion of arm, that vary in size and form (usually more elongated antero-dorsally on males, and less elongate on females) (Fig. 16C ). Dorsal hourglass-shaped blotch only absent in three out of 14 paratypes (CHL 0326, FKH-0378-9) (Fig. 16A ). Soles of hands and feet from pale to very dark grey.

Humeri of male ZMB 91788 with a well-developed medial distal crest and a more discrete lateral distal crest (Fig. 7 ). Regular urostyle, with no pointy protrusion. Parasphenoid trifurcated anteriorly. Squamosals with reduced ventral rami. Distal element of prepollex very elongated, more than on the female holotype.

Natural history and habitat.

The type series was collected in the rainy season, during the night, while breeding in small rocky pools on granite boulders, where two pairs were found in axillary amplexus (Fig. 16D ). No advertisement call was heard. All specimens were caught either on moist bedrock or steep boulder faces, near forest streams or natural seepages, while the surrounding habitat included also extensive montane grasslands (Fig. 8 ). Poyntonophrynus nambensis sp. nov. seem to be opportunistic feeders, inferring from the stomach content of one gravid female (ZMB 91789), which had ten swarming termites, one beetle (around 1.5 mm), ten ants (nine of which very recently ingested) near 3 mm in length and all morphologically identical, the remnants of the head of a jumping spider, and other non-identified arthropod body parts. One of the females from the type series deposited 545 eggs after being captured. Eggs were arranged in a single string, had black and white poles (Fig. 16F ), and a diameter of around 1.5 mm. Amphibian species found in sympatry were Hyperolius parallelus ( Günther, 1858), Hyperolius cinereus Monard, 1937, Phrynobatrachus cf. mababiensis FitzSimons, 1932, Ptychadena oxyrhynchus (Smith, 1849), Tomopterna tuberculosa (Boulenger, 1882), and P. cf. fernandae (lineage A).

Distribution and conservation.

This species is only known from the region of Serra da Namba, 1730-1840 m a.s.l., in the Angolan highlands. It has been recorded in various sites in relatively close proximity along the south and western slopes of the main mountain of Namba. So far, it has not been found in the escarpment zone or in other surveyed mountains in the highlands, suggesting that it may be endemic to Namba. The species appears to be locally common and its rupicolous habitat is probably not threatened, but until more research is conducted, we suggest it to be listed as Data Deficient (DD) as per IUCN Red List categories (IUCN 2022).

Etymology.

The specific epithet nambensis (Pt.) is a reference to the Namba mountains. This is the largest and more preserved relic of Afromontane forest and montane grasslands in Angola. However, it lacks official protection. We suggest "Namba pygmy toad" and "sapo pigmeu da Namba" as English and Portuguese common names respectively.

Figures

Figure 4. Morphometric comparisons of Angolan Poyntonophrynus. Boxplots (top whisker-maximum value; lower whisker-minimum value; dark horizontal line-median; box- 1 st quartile - 1.5 interquartile range (IQR), and 3 rd quartile + 1.5 IQR) comparing morphometric features. A SVL, and ratios B SVL / TL, C SVL / FLL, D SVL / HL between Poyntonophrynus species, left to right: P. cf. fernandae (lineage A, green), P. fernandae sp. nov. (lineage B, blue), P. nambensis sp. nov. (lineage C, red), and P. pachnodes (yellow), the closest related species. For each species, the darker shade (on the left) represents females, and the lighter shade (on the right) represents males. Note sexual size dimorphism in all species, except in P. pachnodes (but compare text). SVL = snout-vent length.

Figure 5. Females of the new Angolan Poyntonophrynus lineages detected in this study in (A) dorsal, and (B) ventral view. Left to right: P. fernandae sp. nov. (lineage B, ZMB 91791), P. cf. fernandae (lineage A, ZMB 91785), P. nambensis sp. nov. (lineage C, ZMB 91787). Note differences in body size, robustness, relative limbs size, dorsal coloration (hourglass shape only in P. nambensis sp. nov.), and ventral coloration.

Figure 6. Cranium osteology of Angolan female Poyntonophrynus. A - H Left to right: skulls of P. dombensis (ZMB 91792), P. fernandae sp. nov. (lineage B) (ZMB 91791), P. cf. fernandae (lineage A) (BMNH 2021.7536), and P. nambensis sp. nov. (lineage C) (ZMB 91787), in dorsal view (top row) and lateral view (second row). Green color marks the squamosal, blue indicates the parotic plate, orange indicates the columella, the latter being absent in P. fernandae sp. nov. and P. cf. fernandae. Np identifies the neopalatine. I - L Left to right: squamosals of P. dombensis, P. fernandae sp. nov., P. cf. fernandae, and P. nambensis sp. nov., in 1 - posterior, 2 - anterior, 3 - lateral, and 4 - medial views.

Figure 7. CT-scan reconstructions of arms of male Poyntonophrynus. Left to right: P. pachnodes (UF 184183), P. cf. fernandae (lineage A) (ZMB 91790), P. fernandae sp. nov. (lineage B) (ZMB 91786), and P. nambensis sp. nov. (lineage C) (ZMB 91788), highlighting the humeri. 1 - lateral crest, 2 - ventral crest, 3 - medial crest. Medial and lateral crests on distal part of the humeri, typical of male bufonids, only absent in the reported P. pachnodes male (compare text). Scale bar represents 5 mm.

Figure 8. Poyntonophrynus habitats. A, B Habitat of P. fernandae sp. nov. at Congulo forest, Cuanza-Sul Province. C, D Habitat of P. cf. fernandae and P. nambensis sp. nov. at Namba highlands, Cuanza-Sul Province. E, F Habitat of P. pachnodes at Serra da Neve, Namibe Province. Photos by K. Luchansky (A) and W. R. Branch (D).

Figure 15. Holotype of Poyntonophrynus nambensis sp. nov. (ZMB 91787, female) in preservative. A Dorsal view. B Ventral view. C Palm of right hand. D Palm of right foot. Photos by F. Tillack. Short scale bars represent 1 mm (A, B), black scale bars represent 5 mm (C, D).

Figure 16. Pictures of live Poyntonophrynus nambensis sp. nov. A Female paratype (FKH- 0458) with greyish coloration. B, C Female holotype (ZMB 91787) with dorsal and ventral coloration, respectively. D Pair in axillary amplexus [female (CHL 0326), and male (BMNH 2021.7540) paratypes]. E Female paratype (BMNH 2021.7539) with brighter shades of brown and orange. F Eggs (CHL 0472). Photos by W. R. Branch (B-F).

Figure 17. CT-scan of Poyntonophrynus nambensis sp. nov. holotype (ZMB 91787, female). A Skeleton in dorsal view. B Lateral, dorsal and ventral views of skull (left to right). C Pectoral girdle in ventral view. D Ventral views of right hand and right foot (left to right). Blue indicates the parotic plate, orange indicates the columella. Scale bars represent 5 mm.