Breviceps passmorei, Minter & Netherlands & Du Preez, 2017

Minter, Leslie R., Netherlands, Edward C. & Du Preez, Louis H., 2017, Uncovering a hidden diversity: two new species of Breviceps (Anura: Brevicipitidae) from northern KwaZulu-Natal, South Africa, Zootaxa 4300 (2), pp. 195-216 : 208-212

Breviceps passmorei sp. nov. Minter, Netherlands & Du Preez

http://zoobank.org/urn:lsid:zoobank.org:act:F836CD13-8351-476F-8C90-EE1DFD691A2F Tables 6–7, Figs. 5–6 .

Holotype. Adult male ( SAIAB 204596 ) collected by LM & EN on 26 January 2017 at the type locality ( Lulwane 1, KwaZulu-Natal, South Africa) (S -27.04319°, E 32.28836°, elevation 64 m), a narrow strip of natural vegetation alongside the tarred road (P522) in a fairly heavily populated, rural area. The vegetation type is Tembe Sandy Bushveld: open leguminous woodland with a species-rich shrub layer and grassy undergrowth.

Paratypes (18 males, 2 females). Five adult males (TM 70333, TM 70335–6, TM 70341, TM 70343), collected 13 December 1988 by LM at Bambanana (see Table 1 for locality details); one adult female (SAIAB 204597), collected 26 January 2017 by EN at Bambanana; one adult female (PEM A12003), collected 26 January 2017 by LM at Lulwane 2; two adult males (PEM A12004; SAIAB 204617), collected 18 November 2016 by LdP & EN at Lulwane 3; two adult males (SAIAB 204598; SAIAB 204599), collected 13 December 2015 by LM at Mpophomeni 1; three adult males (SAIAB 204618; PEM A12005; PEM A12006 ), collected 11 December 2015 by LM at Mpophomeni 2; one adult male (PEM A12007 ), collected 17 February 2017 by EN at Ndumo; four adult males (TM 70362–3, TM 70365, TM 70367), collected 23 October 1988 by LM at Shemula Gata 1; one adult male (TM 70361), collected 22 October 1988 by LM at Shemula Gata 2.

Differential diagnosis. This species is placed in the genus Breviceps on the following grounds: snout extremely abbreviated; mouth narrow and downturned; short limbs which, at rest, are held close to the body, not projecting beyond the body outline; digits tapering to apex; inner and outer toes very short or rudimentary; inner and outer metatarsal tubercles well developed, confluent or separated by a narrow groove; vent terminal, not deflected downwards. Furthermore, the placement of these species is supported by monophyly of the mitochondrial 16S marker with other Breviceps taxa ( Fig. 2 ).

Breviceps passmorei sp. nov. is geographically isolated by substantial distances (320–3600 km) from all other known species except B. adspersus , B. carruthersi , B. mossambicus and B. sopranus ( Fig. 1 ., Minter et al. 2004ac). B. bagginsi and B. verrucosus , which have been recorded as close as 320 km from Ndumo, have different habitat preferences: open, moist grassland, and forest or forest fringes, respectively.

Morphologically, B. passmorei can be distinguished from B. macrops , B. namaquensis and B. branchi by its relatively small eyes; the prominent facial mask separates it from B. acutirostris , B. fuscus , B. gibbosus and B. macrops ; the very short outer toe (as long as it is wide) separates this species from all other known species except B. acutirostris , B. adspersus , B. bagginsi , B. carruthersi sp. nov., B. mossambicus , B. poweri , B. rosei and B. sopranus . The dorsal colouration and markings of B. passmorei closely resemble that of B. adspersus , B. bagginsi , B. carruthersi and B. poweri and, to a lesser, extent those of B. mossambicus , which may lack paravertebral patches while retaining dorsolateral patches, and B. sopranus , in which both markings are present but indistinct.

The advertisement call of B. passmorei is strongly pulsed, distinguishing it from B. macrops , B. namaquensis , B. poweri and B. sopranus , which have tonal calls, and B. carruthersi , in which the call is pulsatile. Under optimum conditions, B. passmorei may condense the calls in the call bout into groups of two to three calls, as do B. adspersus and B. mossambicus , but its call has a longer mean duration: 0.305 s compared with 0.193 s in B. adspersus , 0.198 s in B. bagginsi and 0.05 s in B. mossambicus ( Minter 1997) , and a shorter mean duration than that of B. verrucosis (0.612 s, Minter 2003). The advertisement calls of B. bagginsi are not arranged in groups, but consist of a single, rapidly repeated series of pulsed calls (numbering 7 – 19, Minter 2003).

This new species differs from other species within the Breviceps mossambicus complex with regard to the 16S marker, by a net uncorrected p-distance value of 7.1–13.7% (see Table 3). In the case of B. bagginsi reliable identified tissue was not available but this species differs from B. passmorei in advertisement call structure (see above).

Description of holotype ( Tables 6–7, Figs. 5 A–C, E). Morphometrics are given in Table 7. A male, SVL 36.4 mm. Snout extremely abbreviated; pupils horizontally elliptic; tympanum not distinguishable. Vent terminal. Skin of dorsum very glandular, with closely spaced openings of dermal glands that produce the adhesive secretion during amplexus; its surface consists of irregular small folds and tubercles with scattered larger tubercles, giving it a granular appearance. Skin of ventrum glandular, relatively smooth.

Limbs short. Fourth (outer) finger reaches distal subarticular tubercle of third finger; subarticular tubercles of third finger undivided. Webbing absent. No divided subarticular tubercles on hands or feet were observed. Welldeveloped inner metatarsal tubercle separated from outer metatarsal tubercle by a shallow cleft. Outer toe falls short of basal subarticular tubercle of fourth toe.

Measurement Holotype Paratypes

Females Males

n Mean Range SD n Mean Range SD Mass (g) 8.7 2 13.4; 17.6 13 6.6 4.1–10.5 0.2 EAD 8.0 2 7.0; 7.3 11 6.0 5.3–7.7 0.7 EPD 12 2 12.2; 12.8 11 10.9 10.0–11.7 0.7 ES 1.9 2 1.8; 2.0 11 1.8 1.4–2.4 0.3 FL 13.3; 12.9 4 14.7 14.3–15.2 0.5 20 11.6 9.9–12.9 0.7 HW 16.1 2 13.9; 13.2 11 12.0 11.0–12.5 0.5 IMTL 3.3; 3.4 4 4.1 3.6–4.7 0.5 18 2.9 2.0–3.4 0.4 IND 2.1 2 2.9; 2.7 11 2.0 1.8–2.3 0.2 NL 2.7 2 2.6; 2.7 16 1.8 1.6–2.1 0.14 NOD 1.7; 1.7 4 2.2 1.9–2.5 0.3 21 1.9 1.4–2.3 0.3 PFL 3.8; 3.7 4 5.0 4.6–5.6 0.4 22 4.3 3.7–4.8 0.3 SVL 36.4 2 43.2; 46.9 19 32.1 25.5–35.9 4.0 T1L 0.7; 0.7 4 0.9 0.8–1.0 0.1 22 0.7 0.4–0.9 0.1 T1W 0.8; 0.7 4 1.0 0.9–1.0 0.1 19 0.7 0.5–1.1 0.2 T4L 6.4; 6.4 4 7.6 7.2–8.1 0.4 22 5.7 4.6–6.5 0.5 T5L 0.5; 0.5 4 0.7 0.6–0.7 0.1 22 0.6 0.4–0.8 0.1 T5W 0.3; 0.4 4 0.7 0.6–0.8 0.1 19 0.5 0.4–0.8 0.1 Colour in life, dorsum of body light brown to orange-brown; scattered dark blotches join to form a reticulated pattern; tubercles light to dark brown, becoming almost black around the light paravertebral and dorsolateral patches; laterally, some tubercles are unpigmented, forming conspicuous white speckles; six light brown paravertebral, and four dorsolateral patches present; interocular bar present, from which a light vertebral line runs posteriorly to urostyle, joining a distinct heel-to-heel line; there is an indistinct, creamy-yellow spot on urostyle at its junction. A broad, black stripe runs obliquely downwards, from margin of lower eyelid towards base of arm, not reaching it; anterior to this, a broad white stripe runs down to angle of mouth and onto upper and lower lips, separating the dark stripe from gular patch. Gular region not heavily pigmented, with confluent, dark spots anteriorly and laterally.

Sides of body between limbs, light brown with large dark blotches bordering the light dorsolateral patches; unpigmented tubercles form scattered white speckles. Pectoral region and ventrum immaculate, white. In the preserved specimen, orange-brown and brown has faded to cream and shades of grey ( Figs. 5 B, C).

Holotype advertisement call ( Fig. 6 ). A bout of seven calls, comprising three groups of two calls and a single call, were recorded at Lulwane 1 on 26 January 2017 at 01h30, following light rain. Air temperature was not recorded. Three of these calls were analysed. Several other males were calling sporadically in the vicinity, but the chorus was waning. The calls are strongly pulsed and are not frequency modulated; 2–3 harmonics are present; the amplitude increases gradually throughout the call, falling rapidly at the end. Call rate for the entire bout is 62 min -1; call period within a group 0.571 (0.559–0.584) s; call period between two call groups or between a call group and a single call 1.36 (1.046–1.645) s; call duration 0.352 (0.328–0,373) s; number of pulses 47 (44–50); pulse rate 133.5 (131.7–134.7) s -1; dominant frequency 1833 (1820–1850) Hz.

Paratype variation ( Fig. 5 D; Tables 6-7). Morphometrics are given in Table 7. All specimens resemble the holotype in having an extremely abbreviated snout, horizontally elliptic pupil, absence of a visible tympanum, terminal vent and glandular skin. Skin of dorsum granular in 10 individuals, densely granular in five, granular laterally in five; tubercles light to dark brown, becoming almost black around the light paravertebral and dorsolateral patches; dark tubercles on dorsum randomly scattered in 11, confluent in seven, forming a dark border to the lighter paravertebral patches, and absent in two; laterally, some tubercles are unpigmented, forming conspicuous white speckles. Skin of ventrum glandular, relatively smooth. Outer finger reaches distal subarticular tubercle of third finger in 17 individuals, nearly reaching it in two and falling short in one; subarticular tubercles of third finger undivided in all individuals. Well-developed inner metatarsal tubercle separated from outer metatarsal tubercle by deep cleft in 12 specimens and by a shallow cleft in eight. Outer toe falls just short of basal subarticular tubercle of fourth toe in 19 specimens, extending beyond it in one.

Colour in life: dorsum of body light orange-brown to dark brown with scattered dark blotches joining to form a reticulated pattern in seven specimens; three to six paravertebral, and two to four dorsolateral patches present, indistinct in two; interocular bar present in 17 specimens, indistinct in three; light vertebral line distinct in 14 specimens, indistinct in three, present posteriorly in one and absent in two; heel-to-heel line distinct in five, indistinct in eight and absent in seven individuals. A broad, black stripe runs obliquely downwards from margin of lower eyelid, reaching the base of arm in 10 individuals, nearly reaching it in 10; anterior to this, a broad white stripe runs down to angle of mouth and onto upper and lower lips, separating the dark stripe from gular patch in 17 specimens. Gular region: in the two females, freckled and streaked on a white background; in the 18 males, heavy mottling is present in four, mottling and streaking in two, while dark pigmentation partially, to completely, obscures the mottling anteriorly and laterally in 12. Pectoral region and ventrum immaculate, white, with a few scattered spots in two males.

Colour in preservative: dorsum of body medium brown to dark grey, scattered dark blotches join to form a reticulated pattern. Paravertebral patches beige to dark grey. Interocular bar indistinct and beige to dark brown. Dorsolateral patches distinct and pale. Vertebral line prominent in most specimens, only visible posteriorly in a few and absent in two. Heel-to-heel line indistinct to prominent. Indistinct cream patch over urostyle where vertebral line and heel-to-heel line meet. Facial stripe prominent: dark grey to black. Gular patch of male uniformly dark in six, becoming mottled posteriorly in 12; mottled in females. Ventrum immaculate, creamy-white.

Advertisement call data for the paratype males is presented in Table 6. No significant differences between the calls of the holotype male and the paratypes were found.

Etymology. This species is named for Neville Passmore in recognition of his contributions to South African herpetology in the field of bioacoustics, and for instilling a lifelong interest in frogs among his students, many of whom have also made significant contributions in this and other fields.

Distribution and habitat. Currently known only from the area West of Tembe Elephant Reserve, in the vicinity of the Phongolo River ( Fig. 1 , Table 1). (Vegetation types as defined in Mucina & Rutherford, 2006. Breviceps passmorei sp. nov. occurs in SVI 18 (Tembe Sandy Bushveld), SVI 19 (Western Maputaland Sandy Bushveld) and SVI 20 (Western Maputaland Clay Bushveld). All sites were situated in natural but disturbed roadside vegetation on sandy loam to clay loam soils.

Field observations. Calls were recorded after rain in summer, between 17h40 and 00h15. Calling continued for several days following heavy rain. Four males were calling from shallow depressions, concealed under vegetation, while the majority called from exposed sites on the surface.

Available earlier names. Breviceps adspersus adspersus Pienaar, 1963 , B. adspersus pentheri Poynton, 1964 , B. mossambicus var. occidentalis Werner, 1903 , B. parvus caffer Hewitt, 1932 , B. parvus Hewitt, 1925 , B. pentheri caffer Parker, 1934 , B. pentheri pentheri Parker, 1934 , B. pentheri Werner, 1899 , B. pretoriensis FitzSimons, 1930 and B. mossambicus adspersus Broadley, 1971 , all considered to be junior synonyms of B. adspersus (see Poynton 1964); B. mitchelli Hoffman, 1944 , Engystoma granosum Cuvier, 1829 and Systoma granosum Parker, 1868 considered to be junior synonyms of B. mossambicus .

Figures

FIGURE 1. Map of northern KwaZulu-Natal province showing the vegetation types according to Mucina & Rutherford (2006) and the distribution records for Breviceps carruthersi sp. nov. and B. passmorei sp. nov. The type localities are indicated by white arrows.

FIGURE 2. Phylogenetic analysis of eight Breviceps species based on mitochondrial 16 S rDNA sequences. Bayesian inference analysis showing the phylogenetic relationships for Breviceps carruthersi sp. nov. and B. passmorei sp. nov. (represented in bold), four Breviceps species from the Breviceps mossambicus comple x, and two Breviceps species, namely Breviceps gibbosus and Breviceps macrops used as the outgroup. Node support with posterior probabilities> 0.95 shown. The scale bar represents 0.03 nucleotide substitutions presite.

FIGURE 5. Breviceps passmorei sp. nov. from northern KwaZulu-Natal: A, holotype male (SAIAB 204596); B, preserved holotype, dorsal view; C, preserved holotype, ventral view; D, paratype female (SAIAB 204597); E, left foot of holotype.

FIGURE 6. Advertisement call structure of Breviceps passmorei sp. nov. holotype (SAIAB 204596): A — Oscillogram of call bout; B — Spectrogram of call bout; C — Oscillogram of single call; D — Spectrogram of single call. Spectrogram parameters, using a Hanning window, were set at Window size 300 (Fig. 6 B) and 45 (Fig. 6 D); DFT size 512.