Fejervarya rufescens ( Jerdon, 1853 )

Garg, Sonali & Biju, S. D., 2017, Description of four new species of Burrowing Frogs in the Fejervarya rufescens complex (Dicroglossidae) with notes on morphological affinities of Fejervarya species in the Western Ghats, Zootaxa 4277 (4), pp. 451-490 : 467-472

Fejervarya rufescens ( Jerdon, 1853)

Rufescent Burrowing Frog ( Daniels 2005) ( Tables 1–7; Figs. 1–8 )

Original name and description. Pyxicephalus rufescens Jerdon, 1853 . Catalogue of reptiles inhabiting the Peninsula of India, Journal of the Asiatic Society of Bengal, 22: 522–534. Type. MNHNP 1984.2348, an adult male, designated as Neotype by Dubois (1984). Type locality. “Malabar Coast”, South India according to the original description, restricted to Gundia, Kemphole forest, west of Sakleshpur, Karnataka state, by neotype designation. Current status of specific name. Valid name, as Fejervarya rufescens ( Jerdon, 1853) .

Specimens studied. MNHNP 1984.2348 , an adult male, Neotype; SDBDU 2015.3070–3074 , five adult males, from Manipal , Udupi district, Karnataka state, India, collected by SDB and SG on 13 July 2015.

Other referred material. SDBDU 2013.2505 , Guddekere , Agumbe reserve forest, Shimoga district, Karnataka state, India, collected by SDB on 17 July 2013 ; SDBDU 2009.4712 , Kollur , Mookambika WLS, Udupi district, Karnataka state, India, collected by SDB on 10 October 2009 ; SDBDU 2008.407 , Peruvannamuzhi , Wayanad district, Kerala state, India, collected by SDB on 0 3 June 2008 ; and SDBDU 2015.2882 , Pozhuthana , Wayanad district, Kerala state, India, collected by SDB and SG on 0 7 June 2015. These samples were only used for genetic identification.

Genetic relationship. Phylogenetically, Fejervarya rufescens is nested in the Fejervarya rufescens group ( Figs. 1–2 ) of the Western Ghats. The average uncorrected pairwise genetic divergences with other members of the group ( F. cepfi sp. nov., F. kadar sp. nov., F. manoharani sp. nov. and F. neilcoxi sp. nov.) are provided in Table 2 and ‘Genetic relationship’ section of each species.

Morphological comparison. Based on the overall morphology and comparable body size, Fejervarya rufescens could be confused with the four new species, F. cepfi sp. nov., F. kadar sp. nov., F. manoharani sp. nov. and F. neilcoxi sp. nov. However, F. rufescens is unique from all these species by its dorsal skin shagreened to granular without prominent warts. For detailed comparison with F. cepfi , F. kadar , F. manoharani and F. neilcoxi , see ‘morphological comparison’ of those species.

Remarks. Dubois (1984) designated a neotype for this species without providing a morphological description. Hence, a detailed description of the neotype (MNHNP 1984.2348) is provided in the present study.

Description of neotype (measurements in mm). Adult male (SVL 35.8), rather stout; head nearly as wide as long (HW 12.9, HL 12.7); snout subovoid in dorsal view and rounded in lateral view, its length (SL 5.0) nearly equal to horizontal diameter of eye (EL 4.9); loreal region acute with rounded canthus rostralis; interorbital space flat, narrower (IUE 1.5) than upper eyelid width (UEW 3.5) and internarial distance (IN 3.2); nostril slightly closer to tip of snout (NS 2.2) than eye (EN 2.4); tympanum (TYD 2.2) 44.9% of eye diameter (EL 4.9); tympanum-eye distance (TYE 1.1) half of the tympanum diameter (TYD 2.2); supratympanic fold well developed, extends from posterior corner of eye to near the shoulder; vomerine ridge present, bearing small teeth, at an angle of 45° to the body axis, as close to choanae as to each other; tongue moderately large, emarginated, bearing no median lingual process; rictal gland present at labial commissure of the mouth. Arms short, forearm length (FAL 7.7) shorter than hand length (HAL 8.6); relative length of fingers IV<II<I<III (FL I 3.9, FL II 2.9, FL III 4.4, FL IV 2.8); finger tips rounded, slightly enlarged without discs, fingers without fringes, webbing between fingers absent; subarticular tubercles prominent, circular; one distinct palmar tubercle, oval, bifid; supernumerary tubercles absent. Hind limbs short, thigh length (TL 15.8) equal to shank length (SHL 15.8) and subequal to foot length (FOL 15.9), distance from the base of tarsus to the tip of toe IV (TFOL 23.0); toes long, relative length of toes I<II<V<III<IV; toe tips rounded, slightly enlarged without discs, toes without fringes, webbing between toes small: I2 – – 2II 2– –3–III2– 3IV 3– 2V; subarticular tubercles prominent, all present, circular; inner metatarsal tubercle prominent, shovel-shaped (IMT 2.1); outer metatarsal tubercle small (OMT 0.7), rounded; supernumerary tubercles absent.

Skin of snout, upper eyelids and lateral sides of head shagreened to sparsely granular, anterior part of dorsum sparsely granular, posterior part of dorsum, and upper and lower parts of flank prominently granular; an interrupted inverse V-shaped ridge on center of dorsum; dorsal surfaces of forelimb, thigh and shank shagreened with scattered granular projections. Ventral surface of throat, chest, belly and limbs shagreened, anterior part of thigh sparsely granular; fejervaryan line present on both sides of the belly ( Fig. 7 ).

Species Sex Locality Museum Number SVL HW HL SL EL TYD TYE EN NS IUE UEW IN FAL HAL TL SHL FOL TFOL

Fejervarya cepfi sp. nov.

M Amboli ZSI/WGRC/V/A/937 (HT) 29.9 11.2 11.1 4.6 3.4 1.8 1.5 1.6 1.6 2.4 2.5 2.5 6.2 7.2 14.8 15.7 16.5 23.5

M Amboli ZSI/WGRC/V/A/938 (PT) 33.1 12.2 12.4 4.8 3.5 1.8 1.6 2.0 1.9 2.5 2.6 2.5 6.2 7.5 15.4 16.4 17.1 24.9 Average 31.5 11.7 11.8 4.7 3.5 1.8 1.6 1.8 1.8 2.5 2.6 2.5 6.2 7.4 15.1 16.1 16.8 24.2 Standard deviation 2.3 0.7 0.9 0.1 0.1 0.0 0.1 0.3 0.2 0.1 0.1 0.0 0.0 0.2 0.4 0.5 0.4 1.0

F Amboli ZSI/WGRC/V/A/939 (PT) 34.5 13.1 12.7 5.2 4.0 1.9 1.5 2.2 2.0 2.9 3.0 2.8 6.2 8.0 15.6 16.8 17.4 26.2

Fejervarya kadar sp. nov.

M Thavalakuzhipara ZSI/WGRC/V/A/940 (HT) 33.5 12.7 12.1 4.5 4.2 1.7 1.5 2.1 2.0 1.8 3.3 2.8 6.2 7.1 15.4 15.5 16.1 21.7

M Thavalakuzhipara ZSI/WGRC/V/A/941 (PT) 31.2 11.9 11.7 4.5 4.0 1.5 1.4 1.9 1.9 1.8 3.0 2.6 5.8 6.8 14.8 14.9 15.8 21.4

M Thavalakuzhipara ZSI/WGRC/V/A/942 (PT) 31.0 11.9 11.9 4.4 4.0 1.5 1.2 1.9 1.8 1.7 3.2 2.7 5.7 6.6 14.5 14.6 15.7 21.4 Average 31.9 12.2 11.9 4.5 4.1 1.6 1.4 2.0 1.9 1.8 3.2 2.7 5.9 6.8 14.9 15.0 15.9 21.5 Standard deviation 1.4 0.5 0.2 0.1 0.1 0.1 0.2 0.1 0.1 0.1 0.2 0.1 0.3 0.3 0.5 0.5 0.2 0.2

F Thavalakuzhipara ZSI/WGRC/V/A/943 (PT) 32.2 12.7 12.2 4.9 4.3 1.6 1.7 2.3 2.1 1.9 2.8 2.5 6.1 6.9 15.1 15.0 15.9 22.1

F Thavalakuzhipara ZSI/WGRC/V/A/944 (PT) 34.2 13.5 13.0 5.0 4.4 1.7 1.5 2.5 2.2 1.9 2.7 2.6 7.4 8.1 17.4 17.4 19.8 26.6 Average 33.2 13.1 12.6 5.0 4.4 1.7 1.6 2.4 2.2 1.9 2.8 2.6 6.8 7.5 16.3 16.2 17.9 24.4 Standard deviation 1.4 0.6 0.6 0.1 0.1 0.1 0.1 0.1 0.1 0.0 0.1 0.1 0.9 0.8 1.6 1.7 2.8 3.2 ...continued on the next page

Table 7. continued

Species Sex Locality Museum Number SVL HW HL SL EL TYD TYE EN NS IUE UEW IN FAL HAL TL SHL FOL TFOL

Fejervarya neilcoxi sp. nov.

M Parambikulam ZSI/WGRC/V/A/951 (HT) 33.3 12.1 11.7 4.3 4.2 1.6 1.4 2.1 2.0 2.1 2.9 3.0 6.2 7.4 14.5 15.8 16.9 22.7 M Parambikulam ZSI/WGRC/V/A/952 (PT) 32.0 11.9 11.4 4.2 4.1 1.6 1.6 1.9 1.8 1.8 2.5 2.5 6.1 7.1 14.0 15.3 16.4 22.1 M Parambikulam ZSI/WGRC/V/A/953 (PT) 32.5 12.0 11.5 4.3 4.2 1.6 1.5 1.9 1.9 2.1 2.8 2.8 6.2 7.2 14.2 15.4 16.3 22.1 Average 32.6 12.0 11.5 4.3 4.2 1.6 1.5 2.0 1.9 2.0 2.7 2.8 6.2 7.2 14.2 15.5 16.5 22.3 Standard deviation 0.7 0.1 0.2 0.1 0.1 0.0 0.1 0.1 0.1 0.2 0.2 0.3 0.1 0.2 0.3 0.3 0.3 0.3 F Parambikulam ZSI/WGRC/V/A/954 (PT) 35.6 13.6 12.1 4.3 4.2 1.9 1.8 2.1 1.9 2.1 3.0 2.7 6.6 7.6 15.6 16.7 17.9 24.2 F Parambikulam ZSI/WGRC/V/A/955 (PT) 34.5 12.9 11.9 4.4 4.3 2.1 1.8 2.2 2.0 2.0 3.0 2.8 7.3 7.9 17.8 17.7 18.7 25.5 Average 35.1 13.3 12.0 4.4 4.3 2.0 1.8 2.2 2.0 2.1 3.0 2.8 7.0 7.8 16.7 17.2 18.3 24.9 Standard deviation 0.8 0.5 0.1 0.1 0.1 0.1 0.0 0.1 0.1 0.1 0.0 0.1 0.5 0.2 1.6 0.7 0.6 0.9

Fejervarya rufescens

M Gundia MNHNP 1984.2348 (NT) 35.8 12.9 12.7 5.0 4.9 2.2 1.1 2.4 2.2 1.5 3.5 3.2 7.7 8.6 15.8 15.8 15.9 M Manipal SDBDU 2015.3070 (RS) 32.1 12.0 11.9 4.5 4.3 1.7 1.2 2.1 1.9 1.4 3.2 2.5 6.2 7.1 15.1 15.0 15.4 M Manipal SDBDU 2015.3071 (RS) 30.5 11.2 11.1 4.5 4.2 1.7 1.3 1.9 1.8 1.6 3.2 2.4 5.7 6.9 14.9 14.8 15.2 M Manipal SDBDU 2015.3072 (RS) 31.2 11.1 11.0 4.2 4.0 1.6 1.2 1.9 2.0 1.7 2.9 2.4 5.6 6.4 14.8 14.5 14.9 20.9 M Manipal SDBDU 2015.3073 (RS) 31.5 11.4 11.3 4.4 3.9 1.8 1.3 2.0 1.8 1.7 2.9 2.5 5.5 6.7 14.7 14.6 14.8 21.2 M Manipal SDBDU 2015.3074 (RS) 32.5 11.7 11.6 4.6 4.2 1.7 1.3 2.3 2.1 1.8 3.2 2.5 5.8 7.0 15.5 15.3 15.7 22.0

Colour of neotype. In preservation. Dorsum light brown with dark brown blotches, upper and lower lip with alternate brown and cream coloured cross bands; forelimbs and hind limbs light brown with darker brown transverse bands, posterior part of thigh light brown with faint dark brown reticulations. Ventral surface of throat light greyish-white, with two lateral black calling patches on either side; belly off-white; margins of the limbs with brownish-grey mottling ( Figs. 7 B–G). In life (SDBDU 2015.3070). Snout, upper eyelids, and dorsum light orange or brick red, prominent red to reddish-brown blotches on mid dorsum; upper and lower lip with faint alternate grey and white cross bands; tympanum light yellow; flanks light yellowish-grey with dark grey mottling; forelimbs brick red with a yellowish tinge, hindlimbs brick red with faint and interrupted grey transverse bands, groin yellowish-grey, anterior part of thigh light yellowish-grey with grey reticulations, webbing light grey. Ventral surface of throat light flesh red with two lateral black calling patches on either side; belly white; forearm and foreleg light flesh red ( Fig. 7 A).

Variations. Morphometric data from six adult males, including the neotype, is given in Table 7. Colour in life. Dorsal colour varies from light orange to dark reddish brown with scattered dark reddish-brown to greenish-brown blotches. Colour in preservation. SDBDU 2015.3070 and SDBDU 2015.3073: dorsum light brown with dark brown blotches; SDBDU 2015.3071 and SDBDU 2015.3074: dorsum uniformly light grey with scattered darker grey markings; SDBDU 2015.3072: dorsum with more prominent blackish brown blotches, and anterior part of head, including upper eyelids, dark brown.

Secondary sexual character. Male: calling patches on either side of the throat.

Vocalization. A male (SDBDU 2015.3070, from Manipal) of Fejervarya rufescens produced a single type of call with pulsatile temporal structure ( Figs. 8 A–C). Calls were not delivered in groups and had uniform intervals. A typical advertisement call ( Fig. 8 B) had a duration of 233.7 ms with 52 pulses delivered at a rate of 227.1 pulses per second. Call had a rise time of 221.9 ms and a short fall time of 11.2 ms. The spectrum was characterized by two broad peaks with a dominant frequency of 2.9 KHz ( Fig. 8 D). The animal was recorded on 13 July 2015, around 20:00 hours. Air temperature at the time of recording: dry bulb 27◦C, wet bulb 26.5◦C. For comparison with the call of Fejervarya manoharani sp. nov. see ‘vocalization’ of that species.

Distribution and natural history. According to the present study, the distribution of Fejervarya rufescens is restricted to Karnataka and adjoining regions in Kerala, north of Palghat gap in the Western Ghats ( Fig. 3 ). We genetically confirmed the presence of this species at Manipal and Mookambika WLS (Udupi district), and Guddekere, Agumbe reserve forest (Shimoga district) in Karnataka; and Peruvannamuzhi and Pozhuthana (Wayanad district) in Kerala. This species is usually associated with open rocky areas (often laterite), and during the early monsoon period (June–July) large aggregations can be observed around temporary water bodies, at night. Previously, F. rufescens was reported to occur widely throughout the Western Ghats, but records outside Karnataka and northern Kerala require verification.

Figures

FIGURE 1. Maximum Likelihood phylogram based on the 16 S mitochondrial DNA dataset of 545 basepairs. Bayesian Posterior Probabilities (BPP) and RaxML bootstrap values of> 50 % are indicated above and below the branches, respectively. The uncorrected pairwise distances between species in the Fejervarya rufescens group are shown near the clade labels. Voucher number and locality details of the samples are referenced in Table 1.

FIGURE 2. Phylogenetic analyses. A. Maximum Likelihood phylogram based on mitochondrial (16 S, COI and Cytb) and nuclear (Rag 1) DNA of 2314 basepairs, showing phylogenetic relationships among members of the Fejervarya rufescens group. Bayesian Posterior Probabilities (BPP) and RaxML bootstrap values of> 50 % are indicated above and below the branches, respectively. Fejervarya granosa (2) was used as the outgroup taxon. Voucher number and locality details of the samples are referenced in Table 1; B. Median Joining haplotype network inferred from 554 basepair fragment of the nuclear Rag 1 gene. Circle sizes are proportional to the number of haplotypes, branch lengths are proportional to the number of mutational steps, and black bars represent mutational steps. Number of individuals used for each species: Fejervarya cepfi (3), Fejervarya kadar (1), Fejervarya manoharani (3), Fejervarya neilcoxi (2), and Fejervarya rufescens (5).

FIGURE 3. Geographical distribution of five species in Fejervarya rufescens group of the Western Ghats, Peninsular India. The Western Ghats biodiversity hotspot region is shown in orange colour. Locality details are referenced in Table 3.

FIGURE 4. Four morphologically recognized Fejervarya groups in the Western Ghats. A – B. Fejervarya nilagirica group: A. Fejervarya nilagirica in life (male, SDBDU 2014.2772); B. Fejervarya keralensis in life (male, SDBDU 2015.3139); C. Fejervarya rufescens group, Fejervarya rufescens in life (male, SDBDU 2015.3070); D. Fejervarya sahyadris group, Fejervarya sahyadris in life (male, SDBDU 2015.3046); E – F. Fejervarya syhadrensis group: E. Fejervarya syhadrensis in life (male, SDBDU 2015.2934); F. Fejervarya granosa in life (male, SDBDU 2014.2541). Numbers on the panels represents: 1. dorsal view, 2. ventral view of foot showing the inner metatarsal tubercle, 3. schematic illustration of foot webbing, 4. thighs showing the marking and colour pattern, 5. lateral view showing the groin markings.

FIGURE 5. Morphological comparison between members of the genus Sphaerotheca and Fejervarya rufescens group of the Western Ghats. A – H. Genus Sphaerotheca: A – E. Sphaerotheca cf. breviceps, in life (SDBDU 2014.2822): A. dorsolateral view, B. ventral view, C. ventral skin texture, D. lateral view showing the groin markings, E. thighs showing the marking and colour pattern; F – H. Inner metatarsal tubercle: F. Sphaerotheca breviceps (syntype ZMB 3351), G. S. dobsonii (Holotype BMNH 1947.2.28.45), H. S. rolandae (Holotype BMNH 1973.3024). I – R. Fejervarya rufescens group: I – K. F. rufescens in life (SDBDU 2015.3070): I. dorsolateral view, J. ventral view, K. ventral skin texture; L – M. F. kadar sp. nov. (Holotype ZSI / WGRC / V / A / 940): L. lateral view showing the groin markings, M. thighs showing the marking and colour pattern; N – R. Inner metatarsal tubercle: N. F. cepfi sp. nov. (Holotype ZSI / WGRC / V / A / 937), O. F. kadar sp. nov. (Holotype ZSI / WGRC / V / A / 940), P. F. manoharani sp. nov. (Holotype ZSI / WGRC / V / A / 945), Q. F. neilcoxi sp. nov. (Holotype ZSI / WGRC / V / A / 951), R. F. rufescens (SDBDU 2015.3070).

FIGURE 6. PCA plot for the first two principal component axes showing morphometric differentiation among adult males of five species in the Fejervarya rufescens groups of the Western Ghats. Factor loadings for each component are provided in Table 4.

FIGURE 7. Fejervarya rufescens, in life and preservation. A. Referred specimen (SDBDU 2015.3070), in life; B – G. Neotype (MNHNP 1984.2348, an adult male): B. dorsal view, in preservation; C. ventral view, in preservation; D. lateral view of head, in preservation; E. ventral view of hand, in preservation; F. ventral view of foot, in preservation; G. schematic illustration of foot webbing.

FIGURE 8. Male advertisement calls of Fejervarya rufescens and Fejervarya manoharani sp. nov. A – D. Fejervarya rufescens: A. ten second call segment; B. one second call segment; C. 0.1 second segment showing a single non-pulsatile call; D. spectrogram of the call shown in Figure 8 B. E – H. Fejervarya manoharani sp. nov.: E. ten second call segment; F. one second call segment; G. 0.1 second segment showing a single non-pulsatile call; H. spectrogram of the call shown in Figure 8 F.