Uperodon triangularis

Garg, Sonali, Senevirathne, Gayani, Wijayathilaka, Nayana, Phuge, Samadhan, Deuti, Kaushik, Manamendra-Arachchi, Kelum, Meegaskumbura, Madhava & Biju, Sd, 2018, An integrative taxonomic review of the South Asian microhylid genus Uperodon, Zootaxa 4384 (1), pp. 1-88 : 37-39

Uperodon triangularis ( Günther, 1876 “1875”)

Triangle-spotted Globular Frog

( Figs. 1 , 2A, 2C , 3J , 5I , 8I –L , 10I –L , 11F–K ; Tables 1–4)

Original name and description. Callula triangularis Günther, 1876 “1875”. Third report on collections of Indian reptiles obtained by the British Museum. Proceedings of the Zoological Society of London, 1875: 567–577. Syntypes. NHM 74.4.29.891–900 and NHM 74.4.29.1010, according to Parker (1934). Type locality. “Malabar”, India. Current status of specific name. Valid name, as Uperodon triangularis ( Günther, 1876 “1875”). Synonym. Ramanella triangularis rufeventris Rao, 1937 ( Dutta 1997) , Neotype by present designation, ZSI/WGRC/V/A/959, an adult male, from Mudigere, Karnataka state, India, collected by SD Biju and team on 28 September 2012.

Comments. The original description ( Günther, 1876 “1875”) mentions 11 syntypes from Malabar, all from Col. Beddome’s collection. We examined all the syntypes (nine males and two females) available at NHM, and found NHM 74.4.29.897 (ex. BMNH 1947.2.11.15) to be in agreement with the original description. This specimen was also found to be in well-preserved condition ( Fig. 3J ). Since the original description for this nominal taxon was brief and based on several specimens from an imprecise locality “Malabar” ( Biju 2001), and because this species has often been misidentified by researchers (e.g., Rao 1937; Inger et al. 1984), we herein provide a detailed description of an adult male specimen from the type series, NHM 74.4.29.897 (ex. BMNH 1947.2.11.15), that may serve as a reference of this species for future taxonomic works.

Notes on synonymy and neotypification of Ramanella triangularis rufeventris Rao, 1937 . A new variety of this species was described from “Mudigere, Kadur, Saklespur, Hassan” in Karnataka as Ramanella triangularis rufeventris n. var Rao, 1937. This taxon was considered to be a synonym of Ramanella triangularis (= Uperodon triangularis ) by implication ( Dutta 1997), however, without any justification or comparison. In order to verify this action, we compared the two taxa based on the original description. While describing Ramanella triangularis rufeventris, Rao stated two major differences between the new variety “of the plains” and the typical forms of Uperodon triangularis from “Malnad areas” (= Malenadu region of Karnataka): (1) “the snout is pointed, tips obliquely truncated, prominent”, and (2) “Tibio-tarsal articulation stands well behind the shoulder”, and also included illustrations (Pl. XXIX. Figs. 18 and 18a). Apart from these characters, he used colour and marking differences to distinguish the new variety. During our surveys in regions spanning the type locality of this name bearing taxon (“Mudigere”), we collected Uperodon specimens that were comparable with Rao’s description of “ Ramanella triangularis rufeventris ” particularly in having a more reddish dorsal colour. Due to unavailability of type specimens, considered lost ( Dubois 1984), we relied on the original description to compare our new collections. We found majority of the characters to be same as in Uperodon triangularis , with only minor differences in colour and markings that were not reliable for distinguishing the two taxa from each other. Further, since the snout shape mentioned in the original description of Ramanella triangularis rufeventris is contradicting, we relied on the illustration that clearly shows the snout as “truncate” and not “pointed”, which is also similar to Uperodon triangularis . The mitochondrial 16S rRNA gene sequences of our new collections comparable with Rao’s new variety, and those of Uperodon triangularis from the Malabar region of northern Kerala, were also found to be shallowly divergent (1.5%). Hence, based on findings in this study we confirm Ramanella triangularis rufeventris Rao, 1937 to be a junior subjective synonym of Callula triangularis Günther, 1876 “1875” [= Uperodon triangularis ( Günther, 1876 “1875”)].

Additionally, since the type material for Ramanella triangularis rufeventris Rao, 1937 is lost ( Dubois 1984), we herein also designate ZSI/WGRC/V/A/959 (an adult male from Mudigere) as the neotype of Ramanella triangularis rufeventris Rao, 1937 , in order to define this taxon objectively and to establish taxonomic stability. The description provided along with figures ( Figs. S1F–J ) in the supplementary file S1 also shows that the neotype is largely consistent with what is known of the former name-bearing type.

Comparison. For comparison of Uperodon triangularis with U. globulosus , U. systoma , U. taprobanicus , U. anamalaiensis , U. montanus , U. mormorata , U. nagaoi , U. obscurus and U. palmatus see ‘comparison’ section of those species. Uperodon triangularis cannot be confused with the two other species, U. rohani sp. nov. and U. variegatus , because of its ventral skin being brown to dark blackish-brown with prominent light grey spots and blotches (vs. uniformly white with complete absence of spots and blotches).

Genetic divergence. For 16S mitochondrial gene sequences, the sampled populations of Uperodon triangularis showed an average intraspecific distance of 0.9% (range 0–1.6%, N = 9). Populations from Karnataka and Kerala were observed to be divergent by up to 1.6%. Genetically, U. triangularis is closely related to U. mormorata , from which it was found to differ by an average uncorrected genetic distance of 2.9% (range 2.4–3.6%, N = 99). For interspecific genetic distances with all other members of the genus, see Table 3.

Description of syntype, NHM 74.4.29.897 (measurements in mm) ( Figs. 3J , 10I –L ). Small-sized (SVL 31.6), slender adult female; head small (HW 9.6, HL 7.7, IFE 3.6, IBE 8.4), almost one-fourth (24.4%) of body length, wider than long (HW/HL ratio 1.2); snout rounded to nearly truncate in dorsal and ventral view, nearly acute in lateral view, its length (SL 3.7) longer than horizontal diameter of eye (EL 2.5); loreal region obtuse with rounded canthus rostralis; interorbital space wider (IUE 3.4) than upper eyelid width (UEW 1.9); nostril much closer to tip of snout (NS 0.9) than to eye (EN 2.1); supratympanic fold distinct, extending from posterior corner of upper eyelid to insertion of forelimb at axilla; eye diameter (EL 2.5); vomerine odontophores present on the palate, without teeth; presence of two weakly-developed neopalatinal ridges on posterior side of each choana, fused with the vomerine odontophores; tongue emarginated. Forelimb (FAL 7.1) shorter than hand length (HAL 8.7); finger length formula I<II<IV<III, tips of all fingers with truncate discs, discs moderately wide compared to finger width (FD I 0.8, FW I 0.6; FD II 1.0, FW II 0.7; FD III 0.9, FW III 0.6; FD IV 0.8, FW IV 0.5); subarticular tubercles prominent, oval, all present; two well-developed palmar tubercles (inner, oval, 0.7 mm; outer, shallowly lobed, 1.5 mm). Hind limbs relatively long and thin, thigh length (TL 11.4) longer than shank (SHL 10.9), and shorter than foot (FOL 12.1); tips of all toes with small truncate to rounded discs, discs rather wide compared to toe width; webbing absent between toes; dermal fringes absent on all toes; subarticular tubercles prominent, oval; two smooth metatarsal tubercles, oval, outer one longer (1.6 mm) than the inner (0.9 mm).

Skin of snout, between eyes, sides of head, anterior parts of dorsum, posterior parts of back, and upper and lower parts of flank, shagreened ( Fig. 3J ); dorsal surfaces of forelimb, thigh, tibia and tarsus, shagreened to sparsely granular; ventral surface uniformly shagreened.

Colouration. In preservation (NHM 74.4.29.897): Dorsum orangish-brown with solid darker brown median band on the back starting just above the level of shoulders and extending up to vent, where it becomes wider; brown stripe between eyes; flanks with orangish-brown patches; lateral sides of head brown, anterior and posterior parts orangish-brown; ventral surfaces (including limbs) brown with scattered light brown spots ( Fig. 3J ). Colour in life (SDBDU 2015.2857): Dorsum orange with solid dark brown median band on the back starting just above the level of shoulders and extending close to vent, where it becomes wider; dark brown stripe between eyes and another streak over snout; lateral sides of head and flanks dark brown; dorsal surfaces of limbs (including fingers and toes) dark brown, elbow and knee orange; ventral surfaces (including limbs) dark greyish-brown with scattered light grey spots ( Figs. 11F–K ).

Variations. Morphometric measurements for 19 males and four females are given in Table 4 . Dorsal colouration and markings are highly variable among the examined specimens. SDBDU 2011.503: dorsal skin shagreened to sparsely granular, orange-coloured dorsolateral band discontinuous towards vent; SDBDU 2011.502: dorsal skin shagreened to sparsely granular, orange-coloured dorsolateral band patchy and discontinuous; SDBDU 2012.2038: dorsum largely olive grey in colour with dark brown median patch. SDBDU 2008.409: dorsum light brown with narrow band between upper eyelids.

Secondary sexual characters. Male (SDBDU 2011.504): vocal sac externally visible on the lower jaw; female (SDBDU 2007.6400): ova white, pigmented on pole (diameter 1.3–1.6 mm, N = 10).

Tadpole morphology. In dorsal view, tadpoles of Uperodon triangularis (Gosner stage 35, N = 2) have an elliptical body with narrower anterior region, and wider and longer posterior region; snout appears rounded in dorsal view and depressed in lateral view; eyes small, bulbous, positioned laterally; nasolacrimal duct absent; narial depressions clearly visible in lateral view, located much closer to snout than eyes, pigmentation not visible around nasal depressions; spiracle opens near vent, flap absent; vent tubular, positioned mid-ventrally with aperture opening medially in line with the plane of ventral fin; tail ends bluntly, composed of bilateral myotomic muscle masses divided by V-shaped septa, with unequal membranes on either side of tail musculature; dorsal fins originate after tail-body junction, margin of lower fin not parallel to margin of tail muscle; mouth terminal and appears as slit opening, keratinized structures absent, papillae absent ( Figs. 16K–M ).

Measurements (mm) (N = 1): Lateral measurements include; maximum height of body (bh) = 3.14, maximum width of body (bw) = 6.67, maximum diameter of eye (ed) = 0.56, internarial distance (nn) = 1.63, naro-pupular distance (np) = 2.78, rostro-narial distance (rn) = 0.02, interpupular distance (pp) = 5.43, distance from tip of snout to opening of spiracle (ss) = 6.24, distance from tip of snout to insertion of upper tail fin (su) = 9.82, snout-vent length (svl) = 8.56, total length (tl) = 21.18, distance from vent to tip of tail (vt) = 12.51, maximum height of tail (ht) = 3.85, tail muscle height (tmh) = 1.87, and tail muscle width (tmw) = 1.89.

Vocalization. Male of Uperodon triangularis (SDBDU 2015.2857) from Suganthagiri produced a single type of call with pulsatile temporal structure. The calls had uniform intervals and were not delivered in groups. A typical male call had a duration of 228.9 ms, rise time of 132.3 ms, and fall time of 97.4 ms. The call comprised of 29 pulses that were delivered at a rate of 133.1 pulses/s. The spectrum was characterized by single broad peak with mean dominant frequency of 2.4 kHz ( Figs. 8I –L ).

Geographical distribution and habitat. Uperodon triangularis is known to occur in the South Indian states of Kerala, Karnataka and Tamil Nadu ( Fig. 2C ; Tables 1, S1). In the present study, we confirmed the presence of this species in following regions north of Palghat gap in the Western Ghats : Tamil Nadu (Ooty), northern Kerala (Kalpetta, Mananthavady , Pozhuthana and Suganthagiri ) and southern Karnataka ( Bygoor , Madikeri , Mudigere , and Wattakoli ). It is a mid to high elevation species (about 675 m up to 2200 m asl). Individuals were found under fallen logs and stones during the non-breeding season, and observed around temporary puddles and permanent water bodies during the breeding season. At Bygoor, this species was found about four feet above ground on tree bark inside coffee plantations. For misidentified records from south of Palghat gap see ‘Notes’ under U. anamalaiensis .

Figures

FIGURE 1. Maximum Likelihood phylogram based on 511 bp of mitochondrial 16S rRNA gene sequences from 73 individuals representing all known members of the genus Uperodon. Three samples representing taxon under synonymy are shown inquotationmarks.Outgroup not shown for graphical purposes.BayesianPosterior Probabilities and bootstrap values of>50 are shown above and below the branches, respectively. Values towards the species labels represent mean uncorrected genetic distances between the species with range values in parentheses.

FIGURE 2. A. Geographic distribution of the genus Uperodon in Bangladesh, Bhutan, India, Nepal, Pakistan and Sri Lanka; B. Distributionof Uperodon globulosus, U. systomaand U.taprobanicus; C. Distribution of four endemic Uperodon species of the Western Ghats (excluding the widely distributed Indian member U. variegatus, shown in Fig.12A); D. Distribution of four endemic Uperdodon species of Sri Lanka. Details of localities reported in the present study are provided in Table 1. Records from literature are listed in supplementary Table S1 and indicated here based onapproximate coordinates.

FIGURE 3. Preserved type specimens of Uperodon species in dorsal and ventral view. A. Uperodon systoma, Syntype, ZMB 3551 (female); B. Uperodon globulosus, Syntype, NHM 62.12.29.4 (ex. BMNH 1947.2.10.97) (female); C. Kaloula pulchra taprobanica, Holotype, NHM 1905.3.25.138 (ex. BMNH 1947.2.10.62) (female); D. Ramanella anamalaiensis, Neotype, ZSI/ WGRC/V/A/956 (male); E. Hylaedactylus montanus, Holotype, NHM 72.4.17.212 (ex. BMNH 1947.2.11.19) (female); F. Ramanella mormorata, Neotype, ZSI/WGRC/V/A/958, (female); G. Ramanella nagaoi, Holotype, WHT 2826 (male); H. Callula obscura, Holotype, NHM 58.11.28.42 (ex. BMNH 1947.2.11.20) (female); I. Ramanella palmata, Holotype, NHM 90.11.8.62 (ex.BMNH 1947.2.11.21); J. Callula triangularis, Lectotype, NHM 74.4.29.897 (ex.BMNH 1947.2.11.15) (male); K.Hylaedactylus carnaticus, Lectotype, ZSI 2761(female); L. Uperodonrohani sp. nov., Holotype, DZ1449 (male).(Images: SD Biju and Sonali Garg).

FIGURE 5. Ventral surface of the palate in Uperodon species showing vomerine odontophores separated or fused with dermal projectionsand/or neopalatinalridgeson posterior sides ofthe choanae (indicated witharrows).A. Uperodon systoma, SDBDU 2005.2787 (female) and SDBDU 2005.2806 (male); B. Uperodon globulosus, SDBDU 2014.2673 (female) and SDBDU 2005.4762 (female); C. Uperodon taprobanicus, SDBDU 2007.6364 (female) and SDBDU 2005.4732A (male); D. Uperodon anamalaiensis, SDBDU 2013.2302 (female) and SDBDU 2002.3050 (male); E. Uperodon montanus, SDBDU 2002.24B (female) and SDBDU 2003.40115 (male); F. Uperodon mormorata, SDBDU 2011.507 (male) and SDBDU 2012.43 (male); G. Uperodon obscurus, DZ 1366 (male); H. Uperodon palmatus, DZ 1331 (male); I. Uperodon triangularis, SDBDU 2007.6400 (female) and ZSI/WGRC/V/A/959 (male); J. Uperodon variegatus, SDBDU 2005.4726 (female) and SDBDU 2005.4727 (male); K.Uperodon rohani sp. nov., DZ 1521 (male).(Images:SD Biju).

FIGURE 8. Male advertisement calls of Uperodon anamalaiensis, U. mormorata and U. triangularis. A–D. Uperodon anamalaiensis: 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 Figure8B; E–H. Uperodon mormorata: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 8G; I–L. Uperodon triangularis: I. ten second call segment; J. one second call segment; K. 0.1 second segment showing a single nonpulsatile call; L. spectrogram of the call shown in Figure 8J.

FIGURE 10. Head, hand, foot and foot webbing in Uperodon obscurus, U. palmatus, U. triangularis and U.variegatus. A–D. Holotype ofUperodon obscurus(NHM58.11.28.42 ex.BMNH 1947.2.11.20, female):A. Lateralview of head; B. ventral view of hand; C. ventral view of foot; D. schematic illustration of foot webbing; E–H. Holotype of Uperodon palmatus (NHM 90.11.8.62 ex. BMNH 1947.2.11.21, female): E. Lateral view of head; F. ventral view of hand; G. ventral view of foot; H. schematic illustration of foot webbing; I–L. Lectotype of Uperodon triangularis (NHM 74.4.29.897 ex. BMNH 1947.2.11.15, male): I. Lateral view of head; J. ventral view of hand; K. ventral view of foot; L. schematic illustration of foot webbing; M. Lectotype of Uperodon variegatus (ZSI 2761, female), lateral view of head; N–P. Referred specimen of Uperodon variegatus (ZSI 4726, female): N. ventral view of hand; O. ventral view of foot; P. schematic illustration of foot webbing. (Illustrations: SD Biju).

FIGURE 11. Uperodon palmatus, U. triangularis and U. variegatus in life. A–E. Uperodon palmatus: A. Dorsolateral view (DZ 1372, male); B. dorsolateral view (DZ 1372, male); C. ventral view (DZ 1371, male); D. dorsal view (DZ 1331, male); E. dorsolateral view (DZ 1331, male); F–K. Uperodon triangularis: F. Dorsolateral view (ZSI/WGRC/V/A/959, male); G. dorsal view (SDBDU 2015.2857, male); H. ventral view (SDBDU 2015.2857, male); I. dorsolateral view (SDBDU 2011.502, male); J. dorsolateral view (SDBDU 2012.2200, subadult male); K. dorsofrontal view (SDBDU 2012.2038, male); L–P. Uperodon variegatus: L. Dorsolateral view (not preserved); M. ventral view (SDBDU 2007.4994, male); N. dorsolateral view (not preserved); O. dorsolateral view of an albino (or possibly leucistic) form (not preserved); P. dorsolateral view (not preserved). (Images: SD Biju,Sonali Garg, N & P - Shyamal L, O - Romulus Whitaker).

FIGURE 16. Tadpoles of Uperodon globulosus, U. anamalaiensis, U. nagaoi, U. obscurus and U. triangularis. A–C. Uperodon globulosus in life, Gosner stage 32:A. Lateral view; B. dorsal view; C. ventral view; D–F. Uperodon anamalaiensis in preservation, Gosner stage 34; D. Lateral view; E. dorsal view; F. ventral view; G–H. Uperodon nagaoi in preservation, Gosner stage 37: G. Lateral view; H. lateral view of head; I–J. Uperodon obscurus in life: I. Lateral view, Gosner stage 30; J. Lateral view of head, Gosner stage 38; K–M. Uperodon triangularis in life,Gosner stage 35: K. Lateral view; L. ventral view; M. dorsal view.(Images:SD Biju, I–J& G–H.Madhava Meegaskumbura).