Rana banjarana, Leong & Lim, 2003

Leong, T. M. & Lim, B. L., 2003, A New Species Of Rana (Amphibia: Anura: Ranidae) From The Highlands Of The Malay Peninsula, With Diagnostic Larval Descriptions, Raffles Bulletin of Zoology 51 (1), pp. 115-122 : 117-121

Rana banjarana , new species

( Figs. 2-4 , Table 1)

Sungai Brinchang, coll. N. Smedley, 29 May.1931; ZRC.1.9668, 9669, 9671, 9673 (all adult males), from same microhabitat/ type locality as type series, coll. T. M. Leong, K. K. P. Lim & B. L. Lim, 10 May.2002 . Maxwell’s Hill: DWNP.A.1203-1204 (subadult, adult male), from forests in vicinity of upper guest houses below the peak area (ca. 1,000 m asl), coll. Jim McGuire, (17 Oct.1997: 1203, 21 Nov.1997: 1204); ZRC.1.6048-6049 (adult males), from creeks beside road near upper guest houses (ca. 1,000 m asl), coll. T. M. Leong, 17 Dec.2000 . Fraser’s Hill: ZRC.1.3455a & b (adult males), from small stream at Bishop’s Trail (ca. 1,000 m asl), coll. T. M. Leong, 11 Dec.1996 . Genting Highlands: ZRC.1.10050-10051 (two males), from small stream along primary hill forest, ca. 700 m asl, coll. Jeet Sukumaran & Peter Paul van Dijk (Apr.2002). [South Thailand] Yala Province; Hala Bala Wildlife Sanctuary, Ban Chula Porn 7: NSM 4095-4096 , 4112- 4116 (one female, six males) along small waterfalls and rocky streams between 700-1,200 m asl., coll. Tanya Chan-ard & Yodchaiy Chuaykern, 10-11 Mar.2002 .

Diagnosis. – Dorsolateral skin folds present in varying degrees, a continuous ridge from post-orbital to inguinal area; longitudinal dermal ridges on dorsal surface of tibia, from knee to tibiotarsal joint; raised, rounded granules on dorsum and flanks, each granule tipped with whitish asperities and surrounded by smaller ones [present in both sexes] ( Fig. 3 ); similar asperities on dorsal surfaces of fore- and hindlimbs [present in both sexes]; finger and toe tips dilated, similar in size, not twice as broad as penultimate joint, circum-marginal grooves present ( Fig. 4 ); reduced webbing on Material examined. - Holotype - ZRC.1.8325 (adult male), from bank of gentle, slow-flowing stream (1 m wide, 20 cm deep) in montane forest, feeding into main river of Parit Falls , Tanah Rata , Cameron Highlands, Pahang, Peninsular Malaysia (4º 28’N, 101º 23’E, ca. 1,300 m asl), coll. T. M. Leong, 30 Jul.2001 ( Fig. 2 ).

Paratypes – (four designated, all adult males) ZRC.1.8326, 8327: same collector and date of collection as holotype ; ZRC.1.9670, 9672: coll. T. M. Leong, K. K. P. Lim & B. L. Lim, 10 May.2002 .

Non-types – [West Malaysia] Cameron Highlands: ZRC.1.855-858 (three females, one male), from Tanah Rata, coll. N. Smedley (19 May.1931: 855-857, 28 May.1931: 858); ZRC.1.854 (female), from hindfeet ( Fig. 4b ): web between 1 st and 2 nd toes just reaching respective subarticular tubercles, slightly surpassing proximal subarticular tubercles between 2 nd and 3 rd, reaching distal subarticular tubercle on outer edge of 3 rd toe and middle subarticular tubercle of 4 th toe on both sides, reaching just beyond distal subarticular tubercle of 5 th toe; nuptial pad on first finger ( Fig. 4a ) and subgular vocal sacs present, but humeral gland absent [in males] .

Description. – Habitus moderately stocky, head longer than wide; snout obtuse, slightly projecting, rounded in profile; nostril closer to snout tip than eye; canthus rostralis distinct, lores concave; eye diameter about equal to eye-snout distance; tympanum distinct, diameter 0.57-0.67 of eye diameter, supratympanic fold present, but not extending to axilla; vomerine teeth in short oblique rows, in line with and bordered by choanae.

Finger tips expanded into distinct, small discs less than twice width of penultimate phalanges; all discs bearing circum-marginal grooves; first finger longer than second; subarticular and metacarpal tubercles prominent; discs of toes equal to finger discs, all with circum-marginal grooves; webbing of 1 st and 2 nd toes just reaching respective subarticular tubercles, on 2 nd and 3 rd just beyond proximal subarticular tubercles, reaching distal subarticular tubercle on outer edge of 3 rd toe and middle subarticular tubercle of 4 th toe on both sides, reaching just beyond distal subarticular tubercle of 5 th toe; 4 th toe with three phalanges free; inner and outer metatarsal tubercles distinct, inner metatarsal tubercle elongate, half length of 1 st toe, outer metatarsal tubercle conical, smaller than inner; no free skin flaps on margins of 1 st or 5 th toes; tibia 0.58-0.64 of snout-vent.

Continuous dorsolateral fold present in the form of distinctly raised or low-lying chain of enlarged/fused granules; dorsum (from post-orbital to vent) with polygonal mosaic of raised granules, each granule rounded at its apex and tipped with whitish glandule, each glandule surrounded by other smaller glandules; same granular ornamentation on upper flanks, continuous with dorsolateral fold; whitish glandules also present on dorsolateral fold itself and on dorsal surfaces of all limbs, but not extended onto fingers and toes; tibia with parallel streaks of longitudinal dermal ridges; ventral surfaces smooth. In Smedley’s specimens (ZRC.1.854-858, collected May 1931, presumably fixed in ethanol instead of formalin), the dorsolateral folds and longitudinal tibial ridges have become less pronounced, but still discernible under magnification; dermal glandules and sub-glandules are still clearly visible.

Colour. – In life, basal colour of dorsum and flanks olive brown to orange brown, with black reticulations; snout tip, canthus rostralis, margin of upper eyelid, dorsolateral folds usually devoid of black pigmentation; lores black, iris orange, tympanum deep brown, upper jaw with streaks of basal colour from below eye to jaw angle; forelimbs with same basal colour as body, black barring/reticulation on forearms only, never on upper arms; hindlimbs (from femur to toe tips) barred/reticulated with black; venters light grey to dark brown with randomly distributed white spots (under throat, belly and/or hind limbs); webbing of hindfeet finely pigmented with dark brown. In preservative, basal colours of body fade to beige, the orange of iris disappears, but all black pigmentation remains.

Sexual dimorphism. – There is a noticeable size difference between males and females of this species, with males having an SVL of 32.9-42.2 mm, while females range between 40.9- 55.0 mm. A mature female (ZRC.1.855, SVL 52.4 mm, from Cameron Highlands) was found to have pigmented ova (diameter 1.8-2.0 mm). Males exhibit non-constricted, unpigmented, finely granular nuptial pads spanning the inner surface of the first finger, beginning from the proximal margin of the inner metacarpal tubercle and not exceeding distal margin of the subarticular tubercle ( Fig. 4a ). Males also possess paired subgular vocal sacs, exhibiting wrinkling of the skin on the ventral portions of the jaw angles.

Natural history. – At night, along the stream of the type locality, adult males were observed to be calling individually from the sides while perched low on fallen branches, live vegetation, from sandy bank, or leaf litter. No females were encountered at this site. Other frogs encountered along the same stream as Rana banjarana include Limnonectes laticeps (Boulenger) and Megophrys longipes Boulenger. Along the main river, we observed Rana hosii Boulenger and Bufo asper Gravenhorst. While exploring this stream, a venomous snake ( Trimeresurus popeiorum Smith ) was found to be hunting and it is most likely that Rana banjarana (along with L. laticeps and M. longipes ) would be preyed upon by this viper (Family Crotalidae ). The calls of male Rana banjarana are superficially similar to that of R. signata , comprising a single burst of a series of pulses (T. M. Leong & J. Sukumaran, pers. observ.).

Etymology. – This new species is named after the local Malay term for ‘mountain range’ – ‘ banjaran ’, indicative of its altitudinal distribution, which is restricted to the highlands of the peninsula.

snout tip; eyes dorsolateral, IOD 1.85-2.37 of IND; spiracle sinistral, slightly projecting as a short, free tube, tapered towards the opening, oval opening directed upwards and backwards, spiracle visible from above and below, snoutspiracle 0.43-0.55 of BL; vent dextral, tubular, fused with ventral fin, opening directed towards posterior. Tail gently tapering towards a round tip, fins sub-parallel for anterior half of tail, deepest point at middle of tail, dorsal fin slightly deeper than ventral fin, TAL 1.73-2.40 of BL, MTH 0.24- 0.28 of TAL. Lateral line pores on body and along tail muscle distinct. Small, whitish glandules scattered on dorsum, sides and venter of body; arranged sub-marginally along dorsal and ventral fins.

Larval microhabitat. – Found in well shaded forest stream of type locality; waters clear, slow-flowing, substrate mostly sandy. Larvae observed to be most active at night, feeding on detritus along stream bed.

Larval diagnosis. – A large tadpole (the longest larva [Stage 40] attained a total length of 64.6mm); body and tail lightly scattered with small, whitish glandules (glandules on tail predominantly confined to a single sub-marginal row each in both dorsal and ventral fins); pigmentation pattern of black spots/blotches on body and tail (in advanced stages, black spots of dorsum begin to aggregate, resembling reticulation of the adults); oral disc not emarginate; LTRF 3(2-3)/3(1), width of third labial tooth row of posterior labium _ of second row.

Larval morphology. – ( Figs. 5 , 6 ) Body elliptical, BL 1.43- 1.71 of BW, mildly depressed dorsoventrally, BH 0.67-0.75 of BW; snout rounded, nostril equidistant between eye and Colour/Markings. – In life, dorsum and flanks of body light honey brown, tail muscle beige, tail fins translucent; numerous black specks/spots/ blotches on body and tail; venter unpigmented, translucent, internal organs (e.g., coiled gut) visible, ventral tube unpigmented. In preservative, body becomes a lighter shade of brown, but all black patterns are retained.

Oral Disc. – ( Fig. 7 ) Mouth ventral, sub-terminal, oral disc width 0.26-0.37 of BW, oral disc not emarginate (i.e. no distinct indentations at lateral corners to demarcate anterior and posterior labia), single row of marginal papillae at lateral corners of anterior labium and continuous with entire margin of posterior labium, infra-marginal papillae on posterior labium; upper and lower jaw sheaths serrated, edged with black; upper jaw sheath with slight median convexity.

LTRF. – 3(2-3)/3(1); first labial tooth row of anterior labium continuous, second and third rows broadly interrupted by jaw sheaths, width of each half about 1/5 of first row; first labial tooth row of posterior labium narrowly interrupted at the centre, second row uninterrupted, slightly shorter than first, third row shortest, about 1 / 4 width of first row.

Developmental changes. – In the advanced stages (Stage 40 onwards), the black pigmentation of the dorsum begins to resemble the reticulated pattern of the adults, and crossbars are already visible on the limbs. About two days after eruption of forelimbs, the tail is completely resorbed, and the emergent exhibits an orange iris, as in the living adults. The venter of emergents are grey to brown, with scattered white spots. The dorsolateral dermal folds and tibial ridges are not pronounced as yet, but the individual granules on the dorsum are already demarcated and tipped with a whitish granule each. However, the smaller sub-glandules are not developed at this point. Measurements of BL and TL of the developmental series are reflected in Table 2. A stage 40 larva was dissected to reveal a set of poorly developed lungs, indicative of its high reliance on gill respiration even at this advanced stage (T. M. Leong & R. J. Wassersug pers. observ.). This may point towards high levels of dissolved oxygen in its mountain stream habitat, which would allow for a delayed development of the lungs.

Remarks. – The presence of whitish glandules on the body and tail is not unique to the larvae of R. banjarana alone. Subdermal glandules are also found in larval R. signata as well ( Inger, 1966, 1985), although these glandules occur at a much higher density than in R. banjarana . Besides this shared character, R. banjarana tadpoles differ significantly from those of R. signata in terms of their larger size and spotted pattern. Its oral disc is also significantly different, not only from R. signata , but also from the other known Rana (Hylarana) larvae of Sundaland, in terms of the unique nonemarginate condition. Although this condition was not specifically emphasised in Berry’s (1972) description, it was clearly illustrated as such ( Berry, 1972: 345, Fig. 3 (7)).

Based on adult characters, R. banjarana may be placed within the subgenus Hylarana Tschudi. These characters include: finger and toe tips dilated into distinct discs, with circum-marginal grooves separating upper and lower surfaces; outer metatarsals separated nearly to the base, omosternal style not forked at base; terminal phalanges with feeble transverse expansion. According to Boulenger’s (1920) organisation of this subgenus into ten sections, R. banjarana would come under the Ranae Erythreae section, which exhibit the following characters: finger discs similar to and not larger than toe discs, which are not twice width of penultimate joint; transverse distal expansion of terminal phalanx feeble; dorsolateral fold present. The south-east Asian species belonging to this section include R. erythraea , R. miopus , R. macrodactyla , R. nicobariensis and R. alticola (see Boulenger, 1920). R. banjarana may be readily distinguished from these five species by its unique granular texture of the dorsum and flanks, bearing apical glandules and peripheral sub-glandules.

Another section (Ranae Luctuosae) proposed by Boulenger (1920) shared all the above-mentioned characters with the Ranae Erythreae section, except for the dorsolateral fold, which is absent in this section. This included the south-east Asian species of R. luctuosa , R. baramica , R. glandulosa , R. signata , and R. picturata (see Boulenger, 1920). A recently described species, R. siberu Dring, McCarthy & Whitten 1990 , which also lacks dorsolateral folds, may also be included within this section. For R. signata , however, the presence/absence of dorsolateral folds has suffered from repeated inconsistencies in various references. Inger (1966) and Berry (1975) reported that there was no distinct dorsolateral fold, but the dichotomous key in Berry (1975) implied that R. signata may be either with, or without such folds. In Taylor’s (1962) identification key to the Thai ranids, R. signata stems from the dichotomous branch which states the absence of a dorsolateral glandular fold, but contradicts himself when he mentions a dorsolateral fold as part of the diagnostic character in this species.

Furthermore, in Kampen’s (1923) account of R. signata , he mentions ‘a flat dorsolateral glandular fold, which may be little distinct or absent, or represented by a chain of large warts’. In his identification key, both paths originating from the absence/presence of these glands also lead to R. signata . In addition to previously available references, Kampen examined specimens from the west Sumatran coast of Airbangis, as indicated by an (!) just after the said locality. Another Sumatran locality mentioned was Mt. Simbolon, but without any (!) indicated after this locality. However, upon examination of R. signata specimens from Sumatra, Thailand, Peninsular Malaysia and Borneo (see Appendix), it was determined that such a fold/ridge was not present at all, although it is understandable how the characteristic colour pattern of the contrasting light dorsolateral stripes against a dark background may create the initial impression/ illusion that a raised skin fold exists.

While no highland specimens resembling R. signata from Sumatra were available, there is a possibility that a montane species comparable with R. banjarana may occur there, due to its proximity and earlier connections with the Malay Peninsula (Voris, 2000; Inger & Voris, 2001). Until research efforts in Sumatra are heightened, R. banjarana is currently regarded as endemic to the Malay Peninsula. Within Peninsular Malaysia, the occurrence of R. banjarana in the other mountain ranges (Banjaran Benom, Banjaran Gunong Tahan and Banjaran Timur) remains to be investigated. As further herpetological expeditions are carried out in the peninsula, it will not be surprising to discover range extensions for this species in these highlands.

Figures

Fig. 2. Lateral (a) and dorsal (b) aspects of adult male Rana banjarana, new species (Holotype: ZRC.1.8325, SVL 34.6mm). Note dorsolateral dermal folds, longitudinal ridges on tibia, raised granules on dorsum and flanks, and absence of humeral gland.

Fig. 3. Dermal segment of Rana banjarana dorsum, depicting dorsolateral skin fold and raised granules bearing apical asperities/ glandules, each surrounded by smaller ones (head towards left; illustrated from holotype: ZRC.1.8325). Scale bar = 1mm.

Fig. 4. Ventral aspects of left forelimb (a) and left hindlimb (b) of adult male Rana banjarana (illustrated from holotype: ZRC.1.8325). Note nuptial pad (unpigmented, non-constricted) on inner face of first finger. Scale bar = 5mm.

Fig. 5. Lateral (a) and dorsal (b) aspects of early (Stage 27) larval Rana banjarana.

Fig. 6. Lateral (a) and dorsal (b) aspects of advanced (Stage 43) larval Rana banjarana.

Fig. 7. Oral disc of larval Rana banjarana (Stage 39). Note nonemarginate condition; LTRF 3(2-3)/3(1). Scale bar = 1mm.