Breviceps carruthersi, 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 : 202-207

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

http://zoobank.org/urn:lsid:zoobank.org:act:BC8E4F04-CC6F-4E44-8C39-AD2E7A340A25 Tables 4–5, Figs. 3–4

Holotype. Adult male ( SAIAB 204591 ) collected by LM & LdP on 24 January 2017 at the type locality ( Hluhluwe 1), an open field covered by short, grassy and herbaceous vegetation on red, sandy, clay loam soil, adjacent to the playing fields of Hluhluwe Sports Club, Town of Hluhluwe, KwaZulu-Natal, South Africa (S -28.02278°, E 32.27306°, elevation 88 m).

Paratypes (12 males, 2 females). Three adult males (PEM A11993 –11995), collected 14 December 2015 by LM at Hluhluwe 1; (see Table 1 for locality details); Six adult males (PEM A11996 –11998; SAIAB 204592– 204594) and one adult female (SAIAB 204595), collected 24 January 2017 by LM & LdP at Hluhluwe 1; two adult males (PEM A11999 ; PEM A12000 ), collected 24 January 2017 by Francois Becker at Hluhluwe 2; one adult male (PEM A12001) and one adult female (PEM A12002), collected 24 January 2017 by L. Verburgt, U. Verburgt and A. Coetzer at Ngwenya.

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 carruthersi is geographically isolated by substantial distances (180–3600 km) from all other known species except B. adspersus , B. passmorei , B. mossambicus and B. sopranus ( Fig 1 ., Minter et al. 2004 a-c). Breviceps bagginsi Minter, 2003 and B. verrucosus, Rapp, 1842 , which have been recorded as close as 180 km from Hluhluwe, have different habitat preferences: open, moist grassland, and forest or forest fringes, respectively.

Morphologically, B. carruthersi can be distinguished from B. macrops Boulenger, 1907 and B. namaquensis Power, 1926 and B. branchi Channing, 2012 , by its by its relatively small eyes; the prominent facial mask separates it from B. acutirostris Poynton, 1963 , B. fuscus Hewitt, 1925 , 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. mossambicus , B. passmorei sp. nov., B. poweri , B. sopranus and B. rosei Power, 1926 . The dorsal colouration and markings of B. carruthersi closely resemble that of B. adspersus , B. poweri and B. bagginsi 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. carruthersi is pulsatile, distinguishing it from all other Breviceps species (except B. branchi ), which have either pulsed or tonal calls. The advertisement call of B. branchi is unknown: the holotype specimen was collected north of Port Nolloth , 1800km from Hluhluwe , and resembles B. namaquensis and B. macrops in morphology, having large eyes and fleshy webbing). The calls of B. carruthersi are grouped within the call bout, with up to 28 calls/group. In B. poweri , which has grouped, tonal calls ( Minter 1997), the mean call duration is 0.14 s (0.07 s in B. carruthersi ) and occupies a lower frequency range of 1557–1903 Hz (2182–2481 Hz in B. carruthersi ). Breviceps adspersus , B. bagginsi , B. mossambicus ( Mozambique Island) and B. passmorei differ from B. carruthersi in having pulsed calls with a mean duration of 0.193, 0.198, 0.05 and 0.305 s, respectively ( Minter 1997, 2003, this publication), while B. sopranus has a very long tonal whistle with a mean duration of 1.5 s and a mean dominant frequency of 3332 Hz ( 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 6.8–11.3% (see Table 3). In the case of B. bagginsi reliable identified tissue was not available but this species differs from B. carruthersi in advertisement call structure (see above).

Description of holotype ( Table 5; Figs. 3 A–C, E). Morphometrics are given in Table 5. A male, SVL 34 mm. Snout extremely abbreviated; pupils horizontally elliptic; tympanum not distinguishable. Vent terminal. Skin of dorsum glandular: its surface consists of irregular folds and numerous small and large tubercles, giving it a densely granular appearance; the openings of the dermal glands are closely spaced and evenly distributed. Ventrum smooth. Limbs short. Fourth (outer) finger reaches the distal subarticular tubercle of the 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 deep cleft. Outer toe very short, barely reaching basal subarticular tubercle of fourth toe.

Colour in life: dorsum of body light orange-brown to dark brown, with very dark tubercles forming an incomplete border to the anterior pair of light brown paravertebral patches. Interocular bar present but indistinct; light paravertebral patches distinct; three light dorsolateral spots present, not sharply demarcated. Light vertebral line absent; indistinct heel-to-heel line and small, poorly demarcated cream patch over urostyle present. 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 and separates dark stripe from gular patch. Gular patch uniformly dark anteriorly, becoming mottled posteriorly. Sides of body between limbs light brown with scattered white speckles. Pectoral region and ventrum immaculate, white. In the preserved specimen orange-brown has faded to cream and shades of grey ( Figs. 3 B, C).

Measurement Holotype Paratypes

Females Males

n Mean Range SD n Mean Range SD Mass (g) 5.3 2 15.2; 32.9 9 15.2 3.4–7.6 1.2 EAD 5.6 2 7.5; 8.0 12 5.9 4.7–6.6 0.5 EPD 10.0 2 12.8;14.2 12 10.4 9.0–11.3 0.6 ES 1.4 2 2.8; 2.5 12 1.8 1.4–2.2 0.3 FL 12.5; 11.7 4 17.8 16.7–18.5 0.8 24 11.7 9.2–13.5 0.9 HW 11.2 2 13.0; 14.6 12 11.4 9.6–12.9 0.9 IMTL 3.3; 2.8 4 4.2 3.8–5.1 0.6 23 2.9 2.0–3.5 0.4 IND 1.8 2 2.5; 3.1 12 2.0 1.6–2.5 0.3 NL 2.1; 1.9 4 2.7 2.2–3.2 0.5 24 1.8 1.3–2.1 0.2 NOD 1.8; 1.4 4 2.5 2.2–2.8 0.3 24 2.0 1.7–2.5 0.3 PFL 3.7; 3.8 4 4.8 3.5–5.7 1.0 24 3.7 3.0–4.2 0.4 SVL 34 2 59; 47 9 33.9 28–39 3.3 T1L 0.6; 0.6 4 1.0 1.0–1.1 0.1 24 0.6 0.4–0.8 0.1 T1W 0.7; 0.5 4 1.35 1.0–2.4 0.7 24 0.7 0.5–0.9 0.1 T4L 6.2; 6.3 4 9.2 8.4–10.1 0.7 22 6.0 4.9–7.5 0.6 T5L 0.7; 0.7 4 1.4 1.2–1.6 0.2 23 0.7 0.4–0.8 0.1 T5W 0.7; 0.7 4 0.9 0.7–1.0 0.1 24 0.6 0.4–0.8 0.1 Holotype advertisement call ( Fig. 4 ). Several call bouts consisting of 16 call groups were recorded at the Sports Club in Hluhluwe, on 24th January 2017 at 23h38; air temperature 24 °C. It was raining heavily and a strong chorus had developed. The calls are pulsatile, with amplitude modulation barely distinguishable in most calls, while a few are more strongly modulated; amplitude increases gradually from the start, falling rapidly at the end of the call. Frequency modulation absent. Two to three harmonics are present. All calls in the call bout are condensed into groups consisting of 8–21 calls (mean 12, sd 4). Means and ranges for three calls/call groups are: call period within call group 0.211 s (0.204–0.227); call rate 294 min -1 (290–301); call duration 0.078 s (0.074–0.086); dominant frequency 2378 Hz (2350–2392).

Paratype variation ( Fig. 3 D; Tables 4–5). Morphometrics are given in Table 5. All specimens resemble the holotype in the absence of a visible tympanum; skin densely granular dorsally and laterally, smooth ventrally; one specimen granular laterally, not dorsally. Outer finger reaches distal subarticular tubercle of third finger in 13 specimens, falling just short in one; subarticular tubercles on third finger not divided. Cleft separating inner and outer metatarsal tubercles deep in seven specimens, shallow in seven. Outer toe very short, wider than long, falling short of basal subarticular tubercle of fourth toe in 10 specimens; reaching it in four.

Colour in life: dorsum orange-brown in eight specimens, dark brown in five and pale cream in one unpigmented individual; dark tubercles on dorsum scattered in four, forming a dark border to the lighter paravertebral patches in 10; white lateral speckles present in 13, absent in one. Interocular bar present in seven specimens, indistinct in six, not visible in the unpigmented specimen; light paravertebral patches present in eight, indistinct in six; three light, dorsolateral spots present in 11, indistinct in three. Light mid-vertebral line absent in 12 specimens, present posteriorly in two. A distinct, light-yellowish patch present over the urostyle in four specimens, indistinct in eight, absent in two; light heel-to-heel line indistinct in three, absent in eleven. A broad, black stripe runs obliquely downwards from margin of lower eyelid towards base of arm, reaching it in seven specimens, falling short in seven; anterior to this, a broad white stripe runs down to angle of mouth and onto upper and lower lips in all individuals, separating the dark stripe from the gular patch. Gular patch with scattered, darkgrey mottles on a white background in the two female specimens. In males the gular region is unpigmented in one, uniformly grey or darkened along the lower jaw, becoming lighter medially, in six; in five specimens the gular patch is mottled posteriorly, on a grey to yellowish-brown background. Pectoral region white, with scattered spots in three males. Ventrum immaculate white in 13 specimens; a few scattered spots in one.

Colour in preservative: dorsum of body medium to dark grey. Paravertebral patches beige to dark brown or dark grey in some. Interocular bar indistinct and beige to dark brown. Dorsolateral patches distinct and pale. Heelto-heel line indistinct to absent. Cream patch over urostyle distinct, present in all but two specimens. Facial stripe prominent, dark grey to black. Gular patch uniformly dark anteriorly, becoming mottled posteriorly in most males, mottled in females. Ventrum immaculate, creamy-white.

Advertisement call data for the paratype males is presented in Table 3. No significant differences between the calls of the holotype male and the paratypes were found.

Etymology. This species is named for Vincent Carruthers who, through his numerous books and articles on the natural history of southern Africa in general, and frogs in particular, has done much to stimulate interest in these much-maligned creatures.

Distribution and habitat. Currently known only from the area around Hluhluwe and Phinda Game Reserve ( Fig. 1 ; Table 1). (Vegetation types as defined by Mucina & Rutherford, 2006). Hluhluwe is situated in vegetation type SVI 23 (Zululand Lowveld), which grades into SVI 20 (Western Maputaland Clay Bushveld) on the eastern perimeter of the town. At Phinda Private Game Reserve B. carruthersi occurs mainly in the south, on SVI 20 and SVI 23, as well as SVI 6 (Southern Lebombo Bushveld), less commonly in the sandy soils of CB 1 (Maputaland Coastal Belt) to the north (Daryl Dell 2017, pers. comm.). The first 18 km of the R22 between Hluhluwe and Sodwana consists of SVI 21 (Makatini Clay Thicket), continuing northwards as CB 1.

Field observations. Calls were recorded between 18h45 and 01h15, during and after moderate to heavy rain. Two males were calling from shallow depressions at the base of grasstufts, while the remainder called from exposed positions on the surface. When the vocal sac is inflated, the white stripe separating the gular patch from the dark eyestripe is conspicuous and may function as a visual signal.

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 , 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 3. Breviceps carruthersi sp. nov. from Hluhluwe, KwaZulu-Natal: A, holotype male (SAIAB 204591); B, preserved holotype, dorsal view; C, preserved holotype, ventral view; D, paratype female (SAIAB 204595); E, left foot of holotype.

FIGURE 4. Advertisement call structure of Breviceps carruthersi sp. nov. paratype (PEM A 11997): A – Oscillogram of call bout; B – Spectrogram of call bout; C – Oscillogram of three calls; D – Spectrogram of three calls. Spectrogram parameters, using a Hanning window, were set at Window size 300 (Fig. 4 B) and 45 (Fig. 4 D); DFT size 512.