Contributions to Zoology, 83 (4) – 2014S.D. Biju; Sonali Garg; Stephen Mahony; Nayana Wijayathilaka; Gayani Senevirathne; Madhava Meegaskumbura: DNA barcoding, phylogeny and systematics of Golden-backed frogs (Hylarana, Ranidae) of the Western Ghats-Sri Lanka biodiversity hotspot, with the description of seven new species
Appendix

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Hylarana malabarica (Tschudi, 1838)

Malabar Fungoid Frog (Chari, 1962)


(Figs 22d-i, 23g-h, 24, 25a-f; Tables 1-2)

Original name and description. Rana malabarica Tschudi, 1838. Classification der Batrachier mit Berücksichtigung der fossilen Thiere dieser Abtheilung der Reptilien, Neuchâtel, Petitpierre, 40. Lectotype. By present designation, MNHN 4440, an adult female, SVL 69.1 mm. Type locality. ‘Malabar’, India. Current status of specific name. Valid name, as Hylarana malabarica (Tschudi, 1838).

Referred specimens. Hylarana malabarica: BNHS 1059, an adult male and BNHS 1056, an adult female, Edanad, Kasaragod dist., collected by P.B. Shekar, in March 1962; SDBDU 2002.584, an adult female, Mannuthy, Thrissur dist, collected by SDB, 21 June 2002; BNHS 5879, an adult female, Meladoor, Thrissur dist., collected by SDB, 7 July 2003. Hylarana malabarica haplogroup 1: BNHS 5880 and BNHS 5883, two adult males, Amboli, Sindhudurg dist. Maharashtra state, collected by SDB and SG, 30 July 2012; BNHS 5881-5882 and SDBDU 2013.2373, three adult males, Amboli, Sindhudurg dist., Maharashtra state, collected by SDB and SG, 5 July 2013; BNHS 5884 and SDBDU 2011.31, two adult males, Kachigebailu, Shimoga dist., Karnataka state, collected by SDB, 10 June 2011; SDBDU 2011.1100a, a sub-adult, Bhimashankar, Pune dist., Maharashtra, collected by SDB, 9 October 2011; SDBDU 2011.596, a sub-adult, Amarkantak, Anuppur dist., Madhya Pradesh, collected by SDB and Systematics Lab team, 23 August 2011.

Other material studied. Hylarana malabarica: BNHS 1031, Cannanore (= Kannur), Kannur dist.; BNHS 1053, Pullampora, Calicut, Kozhikode dist., collected by K.G. Adiyodi, in November 1960; BNHS 2124, Tellicherry (= Thalassery), Kannur dist., collected by Harchekar, 3 March 1973; BNHS 2146, Nilambur, Malappuram dist., collected by Whitakar, in 1971; BNHS 2191-2202, Begur, Mananthavady (= Mānantoddy), Wayanad dist., collected by P.B.S./Mahadik, 29 April 1975; BNHS 1051, Manalur, Palni Hills, Dindigul dist., collected by Br. Navarro. Hylarana malabarica haplogroup 1: BNHS 1043, Kanheri caves, Mumbai dist., collected by H. Abdulali; BNHS 1060, Koyna Nagar, Satara dist., collected by P.W. Soman; BNHS 4083, Amboli, Sindhudurg dist., collected by Varad Giri and V. Hedge; BNHS 1036, Ratnagiri, Ratnagiri dist., collected by Kirtikar; BNHS 1052, Khandala, Pune dist., collected by Br. Navarro; BNHS 2402, Matheran, Raigad dist., collected by I.D. Khehimkar; BNHS 4025, Phansad Wildlife Sanctuary, Raigad dist., collected by Varad Giri; BNHS 4008, Tansa WLS, Thane dist., collected by V. Giri and V. Patil.; BNHS 1997, Goa, collected by H. Abdulali.

Comments. This species was described by Tschudi (1838) from ‘Malabar’, India and subsequently reported from throughout the Western Ghats, central India (Dutta, 1997; Chanda, 2002; Daniels, 2005) and Meghalaya in Northeast India (Chanda, 2002). Padhye et al. (2012) discussed genetic variability in six populations of Hylarana malabarica from Maharashtra in the Western Ghats and regarded them as a complex of species due to considerable morphological and genetic differences.

We studied populations from northern parts of the Western Ghats (states of Maharashtra and Karnataka), together with new collections from Meladoor, Kerala (within the limits of one of the type localities, ‘Malabar’, in the southern Western Ghats). The populations sampled from northern parts of the Western Ghats (Amboli and Kachigebailu), referred to as Hylarana malabarica haplogroup 1, were genetically different from the Hylarana malabarica typical (from Meladoor). We observed significant (3.8% for 16S) or even considerable (3.2% for COI and 6.3% for Cytb) genetic variation between the two populations (Table S3), however, adequate morphological differences were not found to allow recognition of a new species in this complex, perhaps due to insufficient sampling. Therefore, the present study does not designate H. malabarica haplogroup 1 as a new species. More extensive surveys in the entire range of H. malabarica are essential to understand the real diversity in this taxon.

The original description of Rana malabarica was based on six specimens (Guibé, 1950). SDB examined the specimens present in MNHN collection, MNHN 771 and MNHN 4440 from ‘Malabar’, and MNHN 4439 from ‘Bengale’. Considering that the syntype series consists of specimens apparently collected from the opposite limits of this ‘species’ geographic range, and recognizing that two distinct genetic haplogroups are now known, we hereby designate MNHN 4440 (an adult female, SVL 69.1 mm) from ‘Malabar’ as lectotype (Fig. 25a) in order to stabilize the nomenclatural status of this taxon.

Pairwise genetic divergence has been discussed in the ‘Genetic divergence’ section, and morphological differences in the ‘Variation’ section of this species.

FIG2

Fig. 25a-f. Hylarana malabarica: a. dorsolateral view of lectotype of Rana malabarica (= Hylarana malabarica) (MNHN 4440); b-d. referred specimen of H. malabarica (BNHS 1059): b. dorsal view, c. ventral view, d. lateral view of head; e-f. referred specimen of H. malabarica haplogroup 1 (BNHS 5880): e. dorsal view, f. lateral view of head.

Comparison. As a unique species Hylarana malabarica could not be confused with other members of the Hylarana malabarica group, by the combination of its strikingly bright dorsal colouration both in life (Fig. 23) and in preservation (Figs 21, 25). See Hylarana gracilis for more specific comparison with that species.

Genetic divergence. Intraspecific genetic variation within populations of Hylarana malabarica could not be calculated since the present study recorded a single specimen of this species from Meladoor (part of the type locality ‘Malabar’). However, populations of this species from northern parts of the Western Ghats, i.e. Hylarana malabarica haplogroup 1, were found to differ considerably and showed intraspecific genetic variation of 0.2 ± 0.2% (range 0-0.4%, N = 3) for 16S, 0.2 ± 0.1% (range 0.2-0.3%, N = 3) for COI and 1.0 ± 0.7% (range 0.2-1.5%, N = 3) for Cytb; differed from the typical population by genetic divergence of 3.8 ± 0.1% (range 3.7-3.9%, N = 3) for 16S, 3.2 ± 0.1% (range 3.1-3.3%, N = 3) for COI and 6.3 ± 0.7% (range 5.9-7.0%, N = 3) for Cytb (Table S3). Based on phylogenetic position, H. malabarica is closely related to Hylarana gracilis from Sri Lanka (Fig. 4). See Hylarana gracilis for comparison with that species.

Description of lectotype (Fig. 25a). Medium-sized, slender to robust mature female (SVL 69.1). Head small (HW 22.2, HL 26.8, IFE 11.8, IBE 17.3), longer than wide, flat above; snout subovoid in dorsal and ventral view, rounded in lateral view, slightly protruding, its length (SL 9.8) longer than horizontal diameter of eye (EL 4.6); loreal region acute and concave with rounded canthus rostralis; interorbital space flat, subequal (IUE 5.7) to upper eyelid (UEW 5.8); distance between back of eye (IBE 17.3) 1.5 times the distance between front of eye (IFE 11.8); nostril oval, closer to tip of snout (NS 3.4) than eye (EN 5.3); eye diameter (EL 4.6) 83 % of tympanum (TYD 5.5); tympanum-eye distance (TYE 2.0); pineal ocellus present, between anterior border of eye; vomerine ridge present, bearing small teeth, with an angle of 40° to body axis, as close to choanae as to each other, tongue moderately large, emarginated. Forelimbs moderately short and thin; forelimb (FAL 13.9) shorter than hand length (HAL 17.7); finger length formula I<II<IV<III, tip of all fingers rounded, without lateroventral groove, slightly wide compared to finger width (FDI 1.1, FWII 0.9; FDII 0.8, FWII 0.6; FDIII 1.0, FWIII 0.7; FDIV 1.0, FWIV 0.6); subarticular tubercles prominent, oval, single, all present; prepollex distinct, oval; two oval prominent palmar tubercles well developed. Hindlimbs relatively long and thin; thigh length (TL 28.7) shorter than shank (SHL 32.7), and foot (FOL 32.5); relative digit lengths I<II<III<V<IV; tips of all toes rounded without lateroventral grooves, slightly wide compared to toe width (TDI 0.8, TWI 0.6; TDII 0.9, TWII 0.6; TDIII 1.0, TWIII 0.8; TDIV 0.9, TWIV 0.8; TDV 0.8, TWV 0.7); webbing present, rather medium: I1+-2+II12/3 -22/3 III12/3 -3IV3-2-V; dermal ridge along toe V present, subarticular tubercles rather prominent, oval, all present; inner metatarsal tubercles distinct and rather short; outer metatarsal tubercles rounded, rather prominent.

Skin of snout, between eyes, sides of head and anterior part of dorsum shagreened; posterior part of back, upper and lower parts of flanks shagreened and sparsely granular; dorsolateral folds that extend from the posterior corner of the eye to the entire body length on both sides, moderately developed (Figs 5, 25a); dorsal surface of forelimbs smooth; thigh, tibia and tarsus shagreened and sparsely glandular; distinct rictal gland posterior to corner of mouth; ventral surface of throat smooth, anterior parts of belly shagreened, posterior part of belly and thigh granular.

Colour in preservation (Fig. 25a). Dorsum greyish-brown with light brown spots, lower flanks light brownish-black with creamy-white speckles; tympanum light brown; upper flanks light brown; upper lip with white stripe continuing through rictal gland to above arm insertion; dorsal part of forelimbs light brown with scattered greyish-brown markings; thigh dark brown coloured with scattered light greyish-brown patches; throat and margin of throat greyish-white; chest and belly greyish-white; ventral parts of thigh, tibia and foot light brownish-white. Colour in life (BNHS 5879) (Fig. 23g). Dorsum uniform reddish-brown with two black spots; tympanum light brown; flanks dark blackish-brown, groin dark brownish-black with light yellow patches; upper lip with yellow stripe continuing through yellow rictal gland to above arm insertion; iris posterior half reddish-brown and anterior half golden brown; limbs dorsally light brown with black spots; ventral side of throat and belly light grey; limbs light grey; feet and webbing dark grey.

Description of BNHS 5880 (Figs 22g-i, 25e-f). Medium-sized, slender adult male (SVL 55.1). Head moderately large, (HW 19.3, HL 20.5, IFE 9.1, IBE 13.6), longer than wide, flat above; snout subovoid in dorsal and ventral view, rounded in lateral view, protruding, its length (SL 8.7) longer than horizontal diameter of eye (EL 5.5); loreal region acute and concave with rounded canthus rostralis; interorbital space flat, wider (IUE 4.6) than upper eyelid (UEW 4.4) and narrower than internarial distance (IN 4.9); distance between back of eye (IBE 13.6) 1.5 times the distance between front of eye (IFE 9.1); nostril closer to tip of snout (NS 3.0) than eye (EN 4.3); tympanum (TYD 5.6) nearly equal to eye diameter (EL 5.5); tympanum-eye distance (TYE 1.0); pineal ocellus present, between anterior border of eye; vomerine ridge present, bearing small teeth, with an angle of 45° to body axis, as close to choanae as to each other; tongue moderately large, emarginated. Forelimbs short and thin; forelimb (FAL 12.4) shorter than hand length (HAL 15.3); fingers long, finger length formula II<I <IV<III, tips of all fingers rounded, without lateroventral groove; dermal fringe absent; subarticular tubercles rather prominent, oval, single, all present; two oval distinct palmar tubercles well developed; a distinct supernumerary tubercle on base of each finger (Fig. 22g). Hindlimbs relatively long; thigh length (TL 25.9) shorter than shank (SHL 25.8), and shorter to foot (FOL 26.3); relative digit lengths I<II<III<V<IV; tips of all toes rounded without lateroventral grooves; webbing present, rather medium: I11/2 -2+II12/3 -24/5 III2-3IV3-2V; dermal ridge along toe V absent, subarticular tubercles rather prominent, oval, all present; inner metatarsal tubercles distinct and rather short; outer metatarsal tubercles rounded, rather prominent; supernumerary tubercles absent; tarsal tubercles absent.

Skin of snout, between eyes, sides of head shagreened, anterior part of dorsum finely shagreened to sparsely granular, posterior part of back finely glandular; upper parts of flank finely granular; dorsolateral folds that extend from the posterior corner of the eye to the entire body length on both sides, moderately developed (Figs 5, 25e-f); dorsal parts of thigh, shank and foot weakly glandular; distinct rictal gland posterior to corner of mouth; humeral glands prominent; ventral part of throat slightly granular, lower part of belly and posterior parts of thigh granular.

Colour in preservation (Figs 25e-f). Dorsum brownish-orange; lower flanks dark grey with light yellow spots; tympanic area dark brownish-black; upper lip with white stripe continuing through rictal gland to above arm insertion; dorsal part of forelimbs creamy-white with grey cross-bands; dorsal parts of thigh, tibia and foot black with white patches; throat and margin of throat, chest and belly creamy-white; ventral part of throat, chest and belly greyish-white; hands and ventral parts of tibia and foot light grey with black spots; webbing dark grey with minute specks. Colour in life (BNHS 5880) Fig. 23h). Dorsum dark brownish-orange; lower flanks dark brownish-black with yellow spots; tympanic area dark brownish-black; upper lip with yellowish-white stripe continuing through yellow coloured rictal gland to above arm insertion; dorsal part of forelimbs light yellowish-brown with brown cross-bands; dorsal parts of thigh, tibia and foot dark brownish-black with yellow reticulation; throat and margin of throat yellowish-white with black flecks; chest and belly whitish-yellow; ventral parts of thigh, tibia and foot grey with light grey spots; webbing dark grey with minute specks; iris reddish-brown.

Variation. See Table 2 for morphometric data from eight adult males (one H. malabarica + seven H. malabarica haplogroup 1) and four adult females (H. malabarica). SDBDU 2011.31: Dorsum dark brownish-orange with scattered dark brown spots; upper and lower flanks granular, ventral surface with prominent dark grey patches mosaicked with creamy-white colour, ventral parts of thigh, tibia and foot light brownish-black with creamy-yellow reticulations; BNHS 5883, dorsum light brownish-orange with irregular black spots; BNHS 5882 and BNHS 5884, dorsal parts of back brownish-orange dorsum with scattered spots; H. malabarica haplogroup 1 differs from the typical by its third toe webbing up to the first subarticular tubercle on the outside (vs. extending well beyond the first subarticular tubercle) and fifth toe webbing up to the first subarticular tubercle on the inside (vs. extending beyond the first subarticular tubercle).

FIG2

Table 2. Morphometric measurements (in mm) of the specimens used in this study. Status of specimens is given after the Museum number: HT-Holotype, PT-Paratype, LT-Lectotype, PL-Paralectotype, RS-Referred specimens, TT-Topotype. All other abbreviations are defined in the material and methods. Species are arranged by ‘Groups’.

Secondary sexual characters. Males: Single oval shaped nuptial pad on finger I present, cream-coloured; two vocal sacs faintly visible externally on the posterior lateral side of the throat; humeral glands weakly developed, positioned laterally on the preaxial side of the upper forelimb. Females (SDBDU 2002.584): ova white, pigmented on pole (diameter 0.7-1.0 mm, N = 20).

Distribution. We collected this species from Meladoor and Mannuthy in Thrissur dist., Kerala state. This study identified other distribution records by morphological examination of museum specimens from Kerala: Edanad, Kasaragod dist; Cannanore (= Kannur), Kannur dist.; Tellicherry (= Thalassery), Kannur dist.; Pullurampara, Kozhikode dist.; Nilambur, Malappuram dist.; Mananthavady (= Mānantoddy), Wayanad dist.; Tamil Nadu: Manalur, Palni Hills, Dindigul dist.; Karanataka: Manipal, Udupi dist. Hylarana malabarica haplogroup 1 has so far been found to occur in northern Karnataka (Kachigebailu), Maharashtra (Amboli, Bhimashankar and Tungareshwar WLS) and Madhya Pradesh (Amarkantak). Other distribution records based on morphological examination of museum specimens include: Kanheri Caves (Mumbai dist.), Khandala (Pune dist.), Matheran and Phansad WLS (Raigad dist.), Ratnagiri (Ratnagiri dist.), Koyna Nagar (Satara dist.), Tansa WLS (Thane dist.) and Goa (Fig. 24, Table 1). Species identification for SDBDU 2011.596 from Madhya Pradesh was confirmed by molecular data, and the distribution table includes this record (Fig. 4).

Habitat and natural history. The present study reports Hylarana malabarica from disturbed habitats, mainly in human inhabited areas. Specimens were collected between 18:00-21:00 h from a permanent water body near a paddy field or roadside man-made pond. Populations of H. malabarica haplogroup 1 were also mostly studied from disturbed habitats, including wayside streams (BNHS 5880-5883), and secondary forest (BNHS 5884 and SDBDU 2011.31). Individuals of this species were found both in temporary (BNHS 5880-5883) and permanent water bodies (BNHS 5884 and SDBDU 2011.31), often associated with floating vegetation, but none were found in fast flowing streams. We found individuals aggregating near water bodies immediately after monsoon showers. Males called continuously after sunset until approximately 23:00 h. During the dry season this species could not be found in areas where they were abundant during the monsoons season.