Uperodon anamalaiensis ( Rao, 1937 )

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 : 23-27

Uperodon anamalaiensis ( Rao, 1937)

Anamalai Globular Frog

( Figs. 1 , 2A, 2C , 3D , 5D , 6D–F , 7A–E , 8A–D ; Tables 1–4)

Original name and description. Ramanella anamalaiensis Rao, 1937 . On some new forms of Batrachia from S. India. Proceedings of the Indian Academy of Sciences. Section B, 6: 387–427. Neotype. By present designation, ZSI/WGRC/V/A/956, an adult male, SVL 30.9 mm, from Parambikulam, Kerala state, India, collected by SD Biju and team on 15 June 2011. Type locality. “Base of Anamalai Hills, Coimbatore District”, Tamil Nadu, India. Current status of specific name. Valid name, as Uperodon anamalaiensis ( Rao, 1937) . Synonym. Ramanella minor Rao, 1937 syn. nov. [= Uperodon minor ( Rao, 1937) ], Neotype by present designation, ZSI/WGRC/V/A/ 957, an adult male, from Sakleshpur, Karnataka state, India, collected by SD Biju and team on 29 September 2012.

Neotypification of Ramanella anamalaiensis Rao, 1937 . This species was described from the “Base of Anamalai Hills, Coimbatore District” based on a single specimen (“total length 28.00 mm”), which was deposited in the Central College, Bangalore (CCB). The original name bearing type for this taxon is considered lost ( Dubois 1984; Biju 2001) and the species was known only from its original description, hence also presumed to be “lost”, until it was rediscovered recently from the wet evergreen forests of Parambikulam Tiger Reserve (Vijayakumar et al. 2011). In the original description, Rao (1937) stated several morphological characters based on which he recognized this taxon to be new, but did not provide any comparison with the other closely known members. Our collections from Parambikulam, which is part of the Anamalai Hills (type locality), are comparable with the original description of Uperodon anamalaiensis ( Rao 1937) in their general size, morphology, and dorsal and ventral markings. The primary inconsistency between our recent collections and the original description is in the degree of webbing on foot. Rao (1937) mentions “toes perfectly free” but the accompanying illustration ( Rao 1937, plate XXIX, fig. 20) suggests presence of at least small foot webbing. However, since we found variation in foot webbing among the various examined populations of this species, we do not consider this as a reliable character for diagnosing the species. Further, since the taxonomic status of Ramanella anamalaiensis Rao, 1937 has remained doubtful ( Dutta 1997) primarily due to unavailability of its name bearing type, in accordance with Article 75 of The Code, designation of a neotype is considered necessary for this taxon, in order to clarify its taxonomic status and to define it objectively. Hence, based on diagnostic characters found useful for differentiating Ramanella anamalaiensis Rao, 1937 (= Uperodon anamalaiensis ) from its congeners (as stated in the ‘comparison’ section below), we herein formally designate ZSI/WGRC/V/A/956, an adult male (SVL 30.9 mm) from Parambikulam, as the neotype of Ramanella anamalaiensis Rao, 1937 . The neotype description provided subsequently also shows that the neotype is largely consistent with what is known of the former name-bearing type.

Synonymization and neotypification of Ramanella minor Rao, 1937 . Rao (1937) described another taxon, Ramanella minor , from Sakleshpur in Karnataka state along with Ramanella (= Uperodon ) anamalaiensis . During our surveys in the Sakleshpur region (type locality) we collected an Uperodon specimen that was comparable with Rao’s description of Ramanella minor . Since the type specimen of this taxon that was originally deposited in the Central College Bangalore (CCB), is also considered lost ( Dubois 1984; Biju 2001), a critical study of the original description of Ramanella minor Rao suggests that the majority of the mentioned characters are nearly the same as for Ramanella anamalaiensis Rao and not helpful in distinguishing them from each other. The major diagnostic characters stated for Ramanella minor by Rao (1937), such as ‘snout broadly truncated, distance between nostrils equals width of the upper eyelid, interorbital space nearly twice the width of the upper eyelid, no occipital fold,’ and the overall colouration, also match with our collections of Uperodon anamalaiensis . The major differences between these two taxa as per Rao’s descriptions seem to be ‘postnarial ridges strongly developed’ (vs. ‘ridges incompletely developed’ in U. anamalaiensis ), ‘diameter of the eye less than the length of the snout’ (vs. ‘diameter of the eye greater than the length of the snout’ in U. anamalaiensis ), ‘canthus rostralis obtuse’ (vs. ‘rostralis rounded’ in U. anamalaiensis ) and few other minor characters, which are all found to be variable among the various Uperodon anamalaiensis populations examined by us ( Table 4 ) and therefore may not be sufficient to distinguish U. minor and U. anamalaiensis from each other. We also compared the 16S rRNA gene sequences of our collection from Sakleshpur and the Uperodon anamalaiensis population from Parambikulam, and found them to show a low genetic difference of 0.8%. Hence, in accordance with Articles 24.2.1 (Statement of the Principle of the First Reviser) and 24.2.2 (Determination of precedence of names or acts by the First Reviser) of The Code, and Recommendation 24A of The Code, we act as the First Revisers and consider Ramanella minor Rao, 1937 as a junior subjective synonym of Ramanella anamalaiensis Rao, 1937 (= Uperodon anamalaiensis ). Furthermore, since the taxonomic status of Ramanella minor Rao, 1937 syn. nov. has been considered doubtful ( Dutta 1997) primarily due to unavailability of name bearing types, in accordance with Article 75 of The Code, we herein designate ZSI/WGRC/V/A/957 (an adult male, SVL 31.7 mm, from the original type locality ‘Sakleshpur’) as the neotype of Ramanella minor Rao, 1937 , in order to define this taxon objectively and to establish taxonomic stability. The neotype description of Ramanella minor Rao, 1937 syn. nov. provided along with figures ( Figs. S1A–E ) in the supplementary file S1, also shows that the neotype is largely consistent with what is known of the former name-bearing type.

Comparison. Uperodon anamalaiensis differs from U. globulosus , U. systoma and U. taprobanicus by its smaller snout-vent size, male SVL 25–37 mm, N = 14, female SVL 35–39 mm, N = 4 (vs. larger, U. globulosus : male SVL 51–56 mm, N = 2, female SVL 66–72 mm, N = 3; U. systoma : male SVL 51–56 mm, N = 2, female SVL 47–64 mm, N = 4; U. taprobanicus : male SVL 42–52 mm, N = 3, female SVL 53–55 mm, N = 2). It also differs from the former two by its finger tips with truncate discs (vs. finger tips rounded without discs), ventral surface with large spots or blotches (vs. without any markings), and presence of two indistinct neopalatinal ridges on posterior side of each choana, fused with the vomerine odontophores (vs. two prominent dermal projections on the neopalatinal ridges on posterior side of each choana, separated from the vomerine odontophores); differs from U. taprobanicus by presence of two indistinct neopalatinal ridges on posterior side of each choana, fused with the vomerine odontophores (vs. well-developed neopalatinal ridges). Further, U. anamalaiensis differs from U. nagaoi , U. rohani sp. nov. and U. variegatus by its ventral surface in having large spots or blotches (vs. absent) and presence of webbing between toes, I1 +– 2–II 1– 2–III 1+– 2–IV 2– 1V (vs. absent). This species could be confused with U. montanus , U. mormorata , U. obscurus , U. palmatus and U. triangularis due to presence of large spots or blotches on ventral skin. However, U. anamalaiensis differs from all these species by presence of continuous broad median band extending from behind the eye up to near the vent (vs. absent or discontinuous patches). Specifically, U. anamalaiensis differs from three Indian congeners by the following characters: from U. montanus by its relatively larger snout-vent size, male SVL 25–37 mm, N = 14, female SVL 35–39 mm, N = 4 (vs. relatively smaller, male SVL 21–28 mm, N = 12, female SVL 28–34 mm, N = 8); shank shorter than thigh, male: SHL/TL ratio 0.8–0.9, N = 14, female: SHL/TL ratio 0.9, N = 4 (vs. shank equal to thigh, male: SHL/TL ratio 1.0, N = 12, female: SHL/TL ratio 1.0, N = 8); and thigh almost equal to foot length, male: TL/FOL ratio 1.0–1.1, N = 14, female: TL/FOL ratio 1.0, N = 4 (vs. thigh shorter than foot, male: TL/FOL ratio 0.8–0.9, N = 14, female: TL/FOL ratio 0.8–1.0, N = 8) ( Table 4 ). It differs from U. mormorata by its relatively smaller snout-vent size, male SVL 25–37 mm, N = 14, female SVL 35–39 mm, N = 4 (vs. relatively larger, male SVL 31–40 mm, N = 9, female SVL 32–43 mm, N = 3) and ventral skin surface with scattered spots or blotches (vs. densely marbled); and from U. triangularis by presence of webbing between toes ( Figs. 7C–E ) (vs. absent) and presence of dermal fringes on fingers and toes (vs. absent). Further, U. anamalaiensis differs from the Sri Lankan congeners by the following characters: from U. palmatus by its snout longer than eye diameter, male: EL/SL ratio 0.5–0.7, N = 14, female: EL/ SL ratio 0.6–0.8, N = 4 (vs. equal, male: EL/SL ratio 1.0, N = 4, female: EL/SL ratio 1.0, N =2); and from U. obscurus by its shank shorter than thigh, male: SHL/TL ratio 0.8–0.9, N = 14, female: SHL/TL ratio 0.9, N = 4 (vs. nearly equal, male: SHL/TL ratio 0.9–1.0, N = 17, female: SHL/TL ratio 0.9–1.1, N = 5) ( Table 4 ).

Genetic divergence. For 16S mitochondrial gene sequences, the sampled populations of Uperodon anamalaiensis showed an average intraspecific distance of 0.4% (range 0–0.8%, N = 6). Genetically, U. anamalaiensis is closely related to U. montanus , from which it was found to differ by an average uncorrected genetic distance of 3.2% (range 2.6–4.0%, N = 60). For interspecific genetic distances with all other members of the genus, see Table 3.

Description of neotype (measurements in mm) ( Figs. 3D , 7A–D ). Small-sized (SVL 30.9), slender adult male; head small (HW 8.5, HL 6.3, IFE 3.9, IBE 7.0), about one-fifth (20.3%) of body length, wider than long (HW/HL ratio 1.3); snout truncate in dorsal and ventral view, vertical in lateral view, protruding, its length (SL 3.0) longer than horizontal diameter of eye (EL 2.2); loreal region acute with rounded canthus rostralis; interorbital space about twice as wide (IUE 3.6) as upper eyelid width (UEW 1.7); nostril oval without lateral flap of skin, closer to tip of snout (NS 0.7) than to eye (EN 1.7); tympanum not visible externally, distinct supratympanic fold extending from posterior corner of upper eyelid near to insertion of forelimb at axilla; eye diameter (EL 2.2); vomerine odontophores present on the palate, prominent, with or without teeth; presence of two indistinct neopalatinal ridges on posterior side of each choana, fused with the vomerine odontophores; tongue moderately large, emarginate. Forelimbs moderately long and thin; forearm (FAL 6.9) shorter than hand length (HAL 8.5); finger length formula I<II<IV<III; tips of all fingers with truncate discs, without grooves, moderately wide compared to finger width (FD I 1.5, FW I 0.3; FD II 1.5, FW II 0.4; FD III 1.8, FW III 0.5; FD IV 1.5, FW IV 0.4); subarticular tubercles prominent, oval, all present; two well-developed palmar tubercles, inner oval, outer bilobed. Hind limbs relatively long and thin, thigh length (TL 13.9) longer than shank (SHL 12.4) and foot (FOL 13.5); relative digit lengths I<II<V<III<IV; tips of all toes with small truncate to rounded discs, rather wide compared to toe width (TD I 0.7, TW I 0.4; TD II 0.9, TW II 0.5; TD III 1.0, TW III 0.5; TD IV 1.1, TW IV 0.5; TD V 0.8, TW V 0.4); foot webbing present, moderate: I1 +– 2–II 1– 2–III 1+– 2–IV 2– 1V; well-developed dermal fringes present on all toes; subarticular tubercles prominent, oval, all present; two smooth metatarsal tubercles, oval, outer tubercle slightly larger than the inner.

Skin of snout, between eyes, and sides of head, shagreened to granular; anterior and posterior parts of back, and upper and lower parts of flank, granular ( Fig. 3D ); dorsal surfaces of forelimb, thigh, tibia and tarsus, shagreened to sparsely granular; throat, chest, abdomen, and ventral surfaces of limbs, shagreened ( Fig. 3D ).

Colouration. In preservation: Dorsum dark greyish-brown with faint dark grey band extending from posterior end of upper eyelid on either side, along the side of dorsum, and approaching the vent; a faint dark grey stripe between eyes; throat, chest and belly, brown with scattered light grey blotches; ventral surfaces of forelimb, thigh, tibia and foot, dark grey with light grey blotches ( Fig. 3D ). Colour in life: Dorsum brown with irregular yellowishbrown spots and prominent yellowish-brown band extending from posterior end of upper eyelid near to vent; yellowish-brown stripe between eyes; lower part of flank brown with yellow speckles; dorsal surfaces of forelimbs, thigh, shank and foot, brown with yellowish-brown cross bands; throat, chest and belly, greyish-brown with scattered light grey blotches; ventral surfaces of forelimb, thigh, tibia and foot, dark grey with light yellow blotches.

Variations. Morphometric measurements for 18 specimens, including the neotype, are given in Table 4 . There is not much variation observed in the overall morphology, except for skin colour and markings, sex-based webbing differences ( Figs. 7D–E ), and presence of vomerine teeth in SDBDU 2013.2302 ( Fig. 5D ). Dorsal colour and skin granulation varies slightly between individuals even from the same populations. SDBDU 2011.233A, SDBDU 2011.234, SDBDU 2011.548, SDBDU 2012.2000 and SDBDU 2012.1998: dorsum dark grey with a light grey dorsal band extending over the back and a light grey stripe between the eyes, dorsal skin shagreened to sparsely granular, ventral surface (including limbs) uniformly coffee brown with yellowish-grey spots and blotches; SDBDU 2013.2302: anterior parts of thigh sparsely granular with scattered spinular projections; SDBDU 2013.928: dorsum light greyish-brown with a straw coloured band extending over the back, foot webbing I2– 2II 2– – 3–III 2– 3IV 3– – 2–V ( Fig. 7E ); SDBDU 2012.1995: anterior parts of thigh prominently granular with scattered spinular projections.

Secondary sexual characters. Male: vocal sac externally visible on the lower jaw; female (SDBDU 2017.3507): ova white, pigmented on pole (diameter 0.6–0.9 mm, N = 10).

Tadpole morphology. In dorsal view, tadpoles of Uperodon anamalaiensis (Gosner stage 34, N = 2) have an elliptical body with narrower and shorter 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 visible clearly in lateral view, located much closer to snout than to eyes, pigmentation not visible around nasal depressions; spiracle opens near the vent, flap present; vent tubular, positioned midventrally with aperture opening medially in line with the plane of ventral fin; tail ends with round tip, 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 a slit opening, keratinized structures absent, papillae absent.

Measurements (mm) (N = 1): Lateral measurements include, maximum height of body (bh) = 3.41, maximum width of body (bw) = 6.87, maximum diameter of eye (ed) = 0.58, internarial distance (nn) = 1.65, naro-pupular distance (np) = 2.86, rostro-narial distance (rn) = 0.02, interpupular distance (pp) = 5.42, distance from tip of snout to opening of spiracle (ss) = 6.44, distance from tip of snout to insertion of upper tail fin (su) = 9.72, snout-vent length (svl) = 8.86, total length (tl) = 21.78, distance from vent to tip of tail (vt) = 13.51, maximum height of tail (ht) = 3.83, tail muscle height (tmh) = 1.97, tail muscle width (tmw) = 1.97.

Vocalization. A male of Uperodon anamalaiensis (SDBDU 2012.1994) from Methooty produced a single type of call with pulsatile temporal structure. Calls were not delivered in groups. A typical male call had a duration of 208.9 ms, a short rise time of 4 ms, and fall time of 202.3 ms. The call comprised of 35 pulses that were delivered at a rate of 175.8 pulses/s. Spectrum was characterized by an overall dominant frequency of 1.2 kHz ( Figs. 8A–D ).

Geographical distribution and habitat. Uperodon anamalaiensis was only known from its original description until its recent rediscovery from Parambikulam in the southern Western Ghats of India. The present study provides further morphological and genetically confirmed reports of this species from Kerala (Chathankod and Methooty) and Karnataka (Sakleshpur) ( Fig. 2C ; Table 1), at elevations between 100–650 m asl. It is also likely to be present in the Anamalai region of Tamil Nadu. Individuals were collected from tree holes, ground puddles and shallow water channels inside disturbed secondary forests (Chathankod and Methooty) as well as primary forest areas, either protected (Parambikulam) or unprotected (Ponmudi and Sakleshpur).

Notes on previous reports. This species was previously misidentified as Uperodon triangularis from Ponmudi hills ( Inger et al. 1984) and Thiruvananthapuram district (Andrew et al. 2005) of Kerala state. The report of U. anamalaiensis from Munnar in Kerala ( Harpalani et al. 2015) most likely refers to U. montanus (see Supplementary Table S1 for list of localities and references thereto).

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 6. Uperodon taprobanicus, U. anamalaiensis and U. montanus in life. A–C. Uperodon taprobanicus (SDBDU 2014.2567, male): A. dorsolateral view; B. dorsal view; C. ventral view; D–F. Uperodon anamalaiensis: D. dorsolateral view (SDBDU 2013.2302, female); E. dorsal view (SDBDU 2017.3507, female); F. ventral view (SDBDU 2017.3507, female); G– L. Uperodon montanus: G. dorsolateral view (SDBDU 2011.849, male); H. dorsolateral view (SDBDU 2011.1197, male); I. ventral view (SDBDU 2002.1925, male); J. dorsolateralview (SDBDU 2002.1925, male); K.dorsal view (SDBDU 2015.3001, male); L. dorsal view (SDBDU 2011.905, male). (Images: SD Biju and Sonali Garg).

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.

FIGURE7. Head, hand, foot and foot webbing in Uperodon anamalaiensis, U. montanus, U. mormorata and U. nagaoi. A–E. Uperodon anamalaiensis: A–D. Neotype of Uperodon anamalaiensis (ZSI/WGRC/V/A/956, male):A. lateral view of head; B. ventral view of hand; C. ventral view of foot; D. schematic illustration of foot webbing; E. schematic illustration of foot webbing in referred specimen of U. anamalaiensis (SDBDU 2013.928, female); F–L. Uperodon montanus: F–H. Topotype of Uperodon montanus (SDBDU 2011.849, male): F. lateral view of head; G. ventral view of hand; H. ventral view of foot; I. schematic illustration of foot webbing; J–L. schematic illustration of foot webbing in referred specimens of Uperodon montanus: J. SDBDU 2015.3001, male; K. SDBDU 2003.40115, female; L. SDBDU 2005.30, female; M–S. Uperodon mormorata: M–P. Neotype of Uperodon mormorata (ZSI/WGRC/V/A/958, female): M. lateral view of head; N. ventral view of hand; O. ventral view of foot; P. schematic illustration of foot webbing; Q–S. schematic illustration of foot webbing in referred specimens of Uperodon mormorata: Q. SDBDU 2002.567, female; R. SDBDU2012.43, male; S. SDBDU 2015.3082, male.T–W. Holotype of Uperodon nagaoi (WHT 2826, male):T. lateral view ofhead;U. ventral view of hand;V. ventral view of foot; W. schematic illustration of foot webbing. (Illustrations:SD Biju).