Fejervarya manoharani, Garg & Biju, 2017

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 : 478-481

Fejervarya manoharani sp. nov.

http://zoobank.org/urn:lsid:zoobank.org:act:D9AF4ACC-6820-44EA-8A06-79DA7E39DAB7 Manoharan’s Burrowing Frog

( Tables 1–7; Figs. 1–6 , 8 , 11 )

Etymology. This species is named for Mr TM Manoharan, who severed as the Head of Kerala Forest Department for over a decade, for providing encouragement as well as personal financial support to SDB during the initial phases of his scientific career. The species epithet manoharani is treated as a noun in the genitive case.

Holotype. ZSI/ WGRC /V/A/945, an adult male, from Chathankod-Bonnacaud (0840’24.0’’N 7709’12.25’’E, 460 m asl), Thiruvananthapuram district, Kerala state, India, collected by SDB and SG on 0 4 August 2013.

Paratypes. ZSI/ WGRC /V/A/946–947, two adult males, and ZSI/ WGRC /V/A/948–949, two adult females, collected along with the holotype; ZSI/ WGRC /V/A/950, an adult male, from the same locality as holotype, collected by SDB and SG on 24 June 2015.

Other referred material. SDBDU 2013.2669 , collected along with the holotype; SDBDU 2011.275 , from Kattalapara , Shendurney WLS (08°55’04.6’’N 77°05’43.2’’E, 130 m asl), Kollam district, Kerala state, India, collected by SDB and team on 0 3 September 2011. These samples were only used for genetic identification.

Genetic relationship. Phylogenetically, Fejervarya manoharani sp. nov. 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 are: 4.4% (range 4.1–4.9%, N = 28) for 16S, 10.4% (range 10.1–10.6%, N = 15) for COI, and 11.0% (range 10.8–11.5%, N = 15) for Cytb with F. rufescens ; 5.6% (5.6–5.8%, N = 16) for 16S, 11.7% (range 11.7–11.8%, N = 9) for COI, and 14.4% (range 14.1–14.6%, N = 9) for Cytb with F. cepfi sp. nov.; and 4.5% (N = 4) for 16S, 9.3% (N = 3) for COI, and 12.5% (range 12.3–12.5%, N = 3) for Cytb with F. kadar sp. nov. (Table 2). For comparison with F. neilcoxi sp. nov. see ‘Genetic relationship’ section of that species.

Diagnosis. Fejervarya manoharani sp. nov. can be distinguished from known congeners by the following combination of morphological characters: (1) medium male adult size (SVL 28.1–30.0 mm, N = 4); (2) stout body; (3) snout rounded in dorsal view and vertical in lateral view; (4) presence of rictal gland at labial commissure of the mouth; (5) head wider than long (male HW/HL ratio 105.5–107.7%, N = 4); (6) horizontal diameter of eye nearly equal to snout length (male EL/SL ratio 93.0–97.6%, N = 4); (7) tympanum diameter less than half of eye length, (male TYD/EL ratio 35.0–36.6%, N = 4); (8) tympanum to eye distance nearly equal to tympanum diameter (male TYE/TYD ratio 92.9–100%, N = 4); (9) inter upper eyelid width narrower than upper eyelid width (male IUE/ UEW ratio 56.7–66.7%, N = 4) and internarial distance (male IUE/IN ratio 68.0–79.2%, N = 4); (10) prominent shovel-shaped inner metatarsal tubercle prominent and small outer metatarsal tubercle; (11) webbing between toes small.

Morphological comparison. Based on the overall morphology and comparable body size, Fejervarya manoharani sp. nov. could be confused with the known species F. rufescens and three new species F. cepfi sp. nov., F. kadar sp. nov. and F. neilcoxi sp. nov.

However, Fejervarya manoharani differs from F. rufescens by its prominently glandular dorsal skin with interrupted linear warts (vs. shagreened to granular without prominent warts); snout rounded in dorsal view (vs. subovoid) and vertical in lateral view (vs. rounded); relatively smaller snout-vent size, male SVL 28.1–30.0 mm, N = 4 (vs. larger, male SVL 30.5–35.8 mm, N = 6); head wider than long, male HW 11.2–11.7 mm, HL 10.4–11.0 mm, HW/HL ratio 105.5–107.7%, N = 4 (vs. nearly equal, male HW 11.1–12.9 mm, HL 11.0– 12.7 mm, HW/HL ratio 100.8–101.6%, N = 6); tympanum to eye distance nearly equal to tympanum diameter, male TYE 1.3–1.4 mm, TYD 1.4–1.5 mm, TYE/TYD ratio 92.9–100%, N = 4 (vs. shorter, TYE 1.1–1.3 mm, TYD 1.6–2.2 mm, TYE/ TYD ratio 50.0–76.5% N = 6); thigh length shorter than foot length, male TL 12.9–13.5 mm, FOL 14.4–14.9 mm, TL/FOL ratio 86.6–91.0%, N = 4 (vs. nearly equal, male TL 14.7–15.8 mm, FOL 14.8–15.9 mm, TL/FOL ratio 98.0–99.4%, N = 6); shank length shorter than foot length, male SHL 13.2–13.8 mm, FOL 14.4–14.9 mm, SHL/ FOL ratio 89.9–92.6%, N = 4 (vs. nearly equal, male SHL 14.5–15.8 mm, FOL 14.8–15.9 mm, SHL/FOL ratio 97.3–99.4%, N = 6); and relatively less webbing between toes, male I2– 2II 2– –3– III2–3 1/ 3IV 3 1/3– 2V, specifically the fourth toe webbing below the second subarticular tubercle on either side (vs. more webbing, male I2 – – 2II 2– –3–III2– 3IV 3– 2V, specifically the fourth toe webbing extending up to the second subarticular tubercle on either side).

Fejervarya manoharani differs from F. cepfi by its dorsal skin with relatively more prominent glandular warts (vs. less); snout vertical in lateral view (vs. obtuse) and rounded in dorsal view (vs. subovoid); head wider than long, male HL 10.4–11.0 mm, HW 11.2–11.7 mm, HW/HL ratio 105.5–107.7%, N = 4 (vs. head length nearly equal to head width, male HL 11.1–12.4 mm, HW 11.2–12.2 mm, HW/HL ratio 98.4–100.9%, N = 2); horizontal diameter of eye relatively larger or nearly equal to snout length, male EL 3.9–4.1 mm, SL 4.0– 4.4 mm, EL/SL ratio 93.0–97.6%, N = 4 (vs. smaller, male EL 3.4–3.5 mm, SL 4.6–4.8 mm, EL/SL ratio 72.9–73.9%, N = 2); tympanum diameter less than half of horizontal diameter of eye, male TYD 1.4–1.5 mm, EL 3.9–4.1 mm, TYD/EL ratio 35.0–36.6%, N = 4 (vs. nearly half, male TYD 1.8 mm, EL 3.4–3.5 mm, TYD/EL ratio 51.4–52.9%, N = 2); tympanum to eye distance equal or nearly equal to tympanum diameter, male TYE 1.3–1.4 mm, TYD 1.4–1.5 mm, TYE/TYD ratio 92.9–100%, N = 4 (vs. relatively shorter, male TYE 1.5–1.6 mm, TYD 1.8 mm, TYE/TYD ratio 83.3–88.9%, N = 2); inter upper eyelid width narrower than upper eyelid width, male IUE 1.7–2.0 mm, UEW 3.0 mm, IUE/UEW ratio 56.7–66.7%, N = 4 (vs. nearly equal, male IUE 2.4–2.5 mm, UEW 2.5–2.6 mm, IUE/UEW ratio 96.0–96.2%, N = 2); inter upper eyelid width narrower than internarial distance, male IUE 1.7–2.0 mm, IN 2.4–2.6 mm, IUE/IN ratio 68.0–79.2%, N = 4 (vs. nearly equal, male IUE 2.4–2.5 mm, IN 2.5 mm, IUE/IN ratio 96–100%, N = 2); relatively less webbing between toes, male I2– 2II 2– –3– III2–3 1/ 3IV 3 1/3– 2V (vs. more, male I1 +–2– II1 +–3–III2– 3IV 3–1 1/ 2V).

Fejervarya manoharani differs from F. kadar by its dorsal skin with more prominent glandular warts (vs. scattered glandular warts); snout vertical in lateral view (vs. obtuse); relatively smaller snout-vent size, male SVL 28.1–30.0 mm, N = 4 (vs. larger, male SVL 31.0– 33.5 mm, N = 3); eye length relatively longer than head length, male EL 3.9–4.1 mm, HL 10.4–11.0 mm, EL/HL ratio 36.7 – 37.5%, N = 4 (vs. shorter, male EL 4.0– 4.2 mm, HL 11.7–12.1 mm, EL/HL ratio 33.6–34.7%, N = 3); forearm length relatively shorter than hand length, male FAL 5.1–5.4 mm, HAL 6.4–6.9 mm, FAL/HAL ratio 76.8–79.7%, N = 4 (vs. longer, male FAL 5.7–6.2 mm, HAL 6.6–7.1 mm, FAL/HAL ratio 85.3–87.3%, N = 3); and relatively more webbing between toes, male I2– 2II 2– –3– III2–3 1/ 3IV 3 1/3– 2V, specifically the fourth toe webbing extending close to the second subarticular tubercle on either side (vs. less, male I2 – –2– II2 – –3– III2–3 2/ 3IV 3 2/3– 2V, specifically the fourth toe webbing extending slightly above the third subarticular tubercle on either side).

For differences with Fejervarya neilcoxi see ‘morphological comparison’ of that species.

Description of holotype (measurements in mm). Adult male (SVL 30.0), rather stout; head wider than long (HW 11.7, HL 11.0); snout rounded in dorsal view and vertical in lateral view, its length (SL 4.4) longer than horizontal diameter of eye (EL 4.1); loreal region acute with rounded canthus rostralis; interorbital space flat (IUE 2.0), narrower than upper eyelid width (UEW 3.0) and internarial distance (IN 2.6); nostril nearly as close to tip of snout (NS 1.9) and to eye (EN 2.0); tympanum (TYD 1.5) 36.6% of eye diameter (EL 4.1); tympanum-eye distance (TYE 1.4) subequal to the tympanum diameter (TYD 1.5); 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 5.4) shorter than hand length (HAL 6.8); relative length of fingers IV<II<I<III (FL I 3.2, FL II 2.5, FL III 3.8, FL IV 2.0); 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 (TL 13.5) shorter than shank (SHL 13.8) and foot (FOL 14.9), distance from the base of tarsus to the tip of toe IV (TFOL 21.2); 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– III2–3 1/ 3IV 3 1/3– 2V; inner toe length (ITL 2.3); subarticular tubercles prominent, all present, circular; inner metatarsal tubercle prominent, shovel-shaped (IMT 1.8); outer metatarsal tubercle small (OMT 0.4), rounded; supernumerary tubercles absent.

Skin of snout shagreened with prominent granular projections and interrupted linear warts, upper eyelids prominently tuberculate, anterior and posterior parts of back, and upper and lower parts of flank shagreened with prominent granular projections and scattered glandular warts; 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 smooth to shagreened, anterior part of thigh sparsely granular; fejervaryan line present on both sides of the belly ( Fig. 11 ).

Colour of holotype. In life. Dorsum, upper eyelids and lateral side of snout yellowish-brown with prominent greyish-brown blotches and a few brick red spots, upper and lower lip with faint alternate greyish-brown and white cross bands; tympanum dark greyish-brown; anterior parts of flank light greyish-brown with scattered white mottling; forelimbs and hind limbs light yellowish-brown with greyish-brown transverse bands and scattered brick red spots; groin yellowish-brown; webbing light greyish-brown; anterior part of thigh light yellowish-brown with greyish-brown reticulations. Ventral surface of throat light flesh red with two lateral black calling patches; belly white; forearm and foreleg light flesh red with dark brown mottling on the margins ( Fig. 11 A). In preservation. Dorsum dark greyish-brown with blackish-brown markings, forelimbs and hind limbs light brown with dark brown transverse bands, posterior parts of thigh light brown with faint dark brown reticulations. Ventral surface of throat light grey with two lateral black calling patches on either side; belly off-white and margins of the limbs grey with dark grey mottling ( Fig. 11 ).

Variations. Morphometric data from four adult males and two adult females, including the holotype, is given in Table 7. Colour in preservation. ZSI/WGRC/V/A/947 and ZSI/WGRC/V/A/949: dorsum light-greyish brown with dark brown markings; ZSI/WGRC/V/A/950: dorsum light-greyish brown with more prominent dark blackishbrown markings.

Secondary sexual characters. Male: calling patches on either side of the throat. Female (ZSI/WGRC/V/A/ 948): pigmented eggs present (diameter 1.9 ± 0.3 mm, N = 15).

Vocalization. A male (ZSI/WGRC/V/A/950, from Chathankod-Bonnacaud) of Fejervarya manoharani sp. nov. produced a single type of call with a pulsatile temporal structure ( Figs. 8 E–G). Calls were not delivered in groups and had uniform intervals. A typical advertisement call ( Fig. 8 F) had a duration of 260.1 ms with 76 pulses delivered at rate of 301.5 pulses per second. Call had a rise time of 127.2 ms and a short fall time of 11.7 ms. The spectrum was characterized by two broad peaks with the overall dominant frequency of 2.6 KHz ( Fig. 8 H). The animal was recorded on 24 June 2015, between 19:00–21:00 hours. Air temperature at the time of recording: dry bulb 25◦C, wet bulb 24◦C.

In comparison to Fejervarya rufescens , the call of F. manoharani had a higher number of pulses, 76 pulses (vs. 52 pulses in F. rufescens ) and was delivered at a faster rate, 301.5 pulses per second (vs. 227.1 pulses per second in F. rufescens ). The overall dominant frequency of F. rufescens call (2.9 KHz) was higher compared to F. manoharani (2.6 KHz). The call rise time was also higher in F. rufescens , 221.9 ms (vs. 127.2 ms in F. manoharani ), making the calls of both these species considerably distinct from each other ( Figs. 8 B, 8F).

Distribution and natural history. Fejervarya manoharani sp. nov. is currently known only from its type locality Chathankod–Bonnacad, and Kattalapara (Shendurney WLS) in Agasthyamala hills, south of both the Palghat gap and Shencottah gap in the Western Ghats state of Kerala ( Fig. 3 ). During the monsoon period (June– July), aggregations of a large number of calling males were observed around temporary water collections on open rocky areas surrounded with secondary forest. Though breeding activity was not observed at that time, we collected tadpoles of this species (genetically confirmed) from water puddles on the vegetated edges of large rocky areas, suggesting that this species probably breeds early, either immediately after the summer showers or during the initial monsoon period (May–June). Like other species in the Fejervarya rufescens group, animals are usually sensitive and with any slight movement around them they immediately stop calling, jump away and try to hide inside nearby muddy areas.

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 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.

FIGURE 11. Holotype of Fejervarya manoharani sp. nov. (ZSI / WGRC / V / A / 945): A. dorsolateral view, in life; 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.