Limnonectes utara, Matsui & Belabut & Ahmad, 2014

Matsui, Masafumi, Belabut, Daicus M. & Ahmad, Norhayati, 2014, Two new species of fanged frogs from Peninsular Malaysia (Anura: Dicroglossidae), Zootaxa 3881 (1), pp. 75-93 : 80-86

Limnonectes utara sp. nov.

Synonymy: Rana kuhlii: Boulenger, 1912, p. 229 (part); Taylor, 1962, p. 408 (part); Berry, 1975, p. 71 (part). Rana kuhli: Inger, 1966, p. 196 (part). Limnonectes kuhlii: Grismer et al., 2010, p. 152 .

Holotype. UKMHC 528 (former KUHE 54064 ), an adult male from the upper part of Bukit Larut (= Larut Hill), State of Perak, Malaysia (4 o 51' N, 100 o 48' E, 1160 m a.s.l.: Fig. 10 ), collected on 28 February 2011 by Masafumi Matsui.

Paratypes. KUHE 15447 , 15463 , 15465 , 15514 (four adult females) , KUHE 15442 (one young male) , KUHE 15441 (one young female), and KUHE 15461 (one unsexed young) from lower part of Bukit Larut (680 m a.s.l.), collected on 3 January 1993 by Masafumi Matsui . KUHE 54065 , 54089 (two adult males) , KUHE 54086–54088 (three adult females) , KUHE 54090 (one unsexed young) from the type locality, collected from 27 to 28 February 2011 by Masafumi Matsui and Norihiro Kuraishi .

Referred specimens. UKMHC 700 , 703 , 704 from Sungai Tembat , Hulu Terengganu, State of Terengganu, Malaysia (ca. 5°26' N; 102°58' E, 168–170 m a.s.l.), collected in 2009 by Daicus M. Belabut ; KUHE 49514 (three larvae) from lower part of Bukit Larut (600 m a.s.l.), collected on 3 January 1993 by Masafumi Matsui .

Etymology. The specific epithet utara is a Malay word denoting north, alluding to the northerly-restricted distribution of the new species within the Peninsular Malaysia.

Diagnosis. The new species is assigned to the genus Limnonectes only by molecular phylogenetic evidence, because morphological diagnostic characters of the genus previously proposed (e.g. Emerson and Berrigan 1993; Fei et al. 2005) are mostly osteological ones, which we did not examine. Moreover, osteological synapomorphic characters proposed by previous authors suffer from limited taxon sampling and require reexamination. Morphological assignment of the new species to Limnonectes was based only on the single characteristic usually found in the genus, enlarged “fangs” (tooth-like projections [odontoid processes]) on the lower jaw. A mediumsized species morphologically similar to L. kuhlii , with adult SVL 70–79 mm in males, 59–79 mm in females; males with relatively longer head than females; tibia dorsally densely covered by warts; toe webbing full, with very shallow excision between toes; first finger usually slightly longer than second, and nuptial pad present on first finger of males; morphologically differs from L. selatan , described below, in smoother dorsal skin, less densely arranged circum-cloacal warts, more confluent dorsal dark markings, and lack of large dark blotches on rear of thigh ( Fig. 6 ).

Description of holotype (measurements in mm). SVL 79.1; habitus stocky ( Figs. 3A , 4A,B ); head enlarged, longer (HL 36.0, 45.5%SVL) than broad (HW 33.8, 42.7%SVL); snout obtusely pointed, obtuse in profile, projecting beyond lower jaw; eye length (EL 11.0,13.9%SVL) shorter than snout length (SL 13.0, 16.4%SVL); canthus rounded; lore sloping, concave; nostril dorsolateral on canthus, closer to tip of snout than to eye; internarial distance (IND 5.8, 7.3%SVL) equal to upper eyelid (UEW 5.8, 7.3%SVL) and wider than interorbital distance (IOD 5.4, 6.8%SVL); pineal spot visible; tympanic annulus barely visible through skin; vomerine teeth in oblique groups, between and behind line connecting anterior rims of choanae, groups separated from one another by onefifth length of one group and from choana by about one-fourth length of one group; lower jaw with a pair of toothlike projections (odontoid processes) near symphysis, more than twice depth of mandible at base of projections; tongue oval, deeply notched posteriorly, without papillae; vocal sac and vocal slits absent.

Forelimb heavy, relatively short (FLL 41.9, 53.0% SVL); fingers moderately slender; finger length formula: II <I <IV <III ( Fig. 5A ), first finger slightly longer than second, length of first (11.0, 13.9%SVL, measured from distal edge of inner palmar tubercle) equal to length of eye; fourth finger much longer than second; tips of fingers bluntly rounded, forming small pads without circummarginal grooves; no webs between fingers; inner palmar tubercle moderate (4.1, 5.2% SVL), oval, not elevated; middle palmar tubercle oval, smaller than inner palmar tubercle, not contacting outer or inner palmar tubercles; outer palmar tubercle slightly smaller than middle tubercle; proximal subarticular tubercles round and elevated; distal subarticular tubercles low and indistinct; no supernumerary metacarpal tubercles; narrow, but distinct flaps of skin along both edges of second and third fingers.

Hindlimb heavy, relatively short (HLL 117.0,147.9% SVL) about 2.8 times length of forelimb; tibia short (TL 35.2, 44.5% SVL), heels not overlapping when limbs are held at right angles to body; tibiotarsal articulation of adpressed limb reaching to point posterior to eye; foot (FL 37.1, 46.9% SVL) slightly longer than tibia; toe length formula I <II <V <III <IV; tips of toes expanded into round, elevated pads lacking grooves (disk diameter of fourth toe, 4TDW 2.0, 2.5% SVL); all toes webbed to base of disks ( Fig. 5B ); webbing formula: I 0 – 0 II 0 – 0 III 0 – 0 IV 0 – 0 V; a distinct, movable flap of skin on outer edge of fifth toe and on inner edge of first toe; subarticular tubercles oval and distinct; an elongate inner metatarsal tubercle, length (IMTL 5.7, 7.2%SVL), about half length of first toe (1TOEL 11.2, 14.2% SVL); no outer metatarsal tubercle.

Dorsum anteriorly very weakly rugose, without warts, posteriorly with very low ridges radiating from scattered, low warts ( Fig. 4A ); top of snout without tubercles, but eyelid covered with small warts and wrinkles with medial, longitudinal ridge formed by fused warts; weak transverse fold between posterior margins of eyes; a strong, supratympanic fold from eye to above axilla; posterior side of trunk scattered with tubercles; circum-cloacal warts small being sparsely and narrowly distributed anterior to cloaca, posteriorly more scattered but widely distributed, increasing size to end at dorso-ventral border of thigh ( Fig. 6A ); dorsal surface of thigh smooth on proximal two-thirds and scattered with small, low warts tipped with translucent spinules on distal one-third, continuing to tibia; tibia dorsally covered with numerous large and small round warts each tipped with large whitish cone surrounded by clusters of much smaller, whitish asperities; tarsus less densely covered by similar warts dorsolaterally; tarsus with a thick dermal ridge extending proximally from metatarsal tubercle; throat and chest weakly rugose, abdomen smooth ( Fig. 4B ); a distinct creamy tinge, with minute asperities, forming a nuptial pad covering medial surface of first finger from its base to level of subarticular tubercle, sharply set off from remainder of skin on first finger.

Color. In life, dorsum light brown with confluent dark brown markings ( Figs. 3A , 4A ); head with a narrow light band anterior to dark interorbital bar; blackish brown stripe on canthus rostralis; side of head pale brown with dark markings; oblique blackish brown temporal stripe on and along supratympanic fold beginning behind eye reaching inguinal area, and continuing on flank; lips barred with dark brown; dark brown stripe on anterior side of upper arm; limbs marked dorsally with dark-brown crossbars; dorsal and ventral border of posterior thigh scattered with small brown spots ( Fig. 6A ); throat weakly mottled with pale gray, spotted with dark brown posteriorly; abdomen immaculate cream ( Fig. 4B ); ventral surfaces of hand and foot dark brown ( Figs. 5 A,B ). In preservative, the dorsal coloration has slightly faded, but otherwise no obvious change in color or pattern has occurred.

Variation. Individual variation in size and body proportions is given in Table 3 . Males have relatively longer head than females. Well-developed warts are invariably present, but there are some variations in qualitative traits. The postorbital light-colored bar was absent (50% of adults examined) or only vaguely traced (42%), and a few (8%) had a thin bar. The majority (83%) had a wide temporal stripe, and at least narrow temporal stripe was present (17%). Distinct spots were found widely distributed on dorsum in many (83%) individuals, and were found on at least part of the dorsum in others (17%). Many (75%) had weak spots or dots on the chin, but some had dusty marking (17%) or lacked chin spots (8%). The dark stripe on the upper arm was clear and continuous (38%) or weak or disjunct (46%), but was absent in some individuals (15%). Dorsal warts on the body were present usually (75%) only partially, and some (25 %) had very few warts. The first finger was usually longer than the second (69%), but was subequal (15%), or shorter than the first (15%) in some individuals.

Eggs and tadpoles. The diameter of nine ovulated eggs from a female (KUHE 15447) ranged from 2.59–3.09 (mean±1SD = 2.74±0.17) mm. The animal hemisphere of the egg is dark brown and the vegetal hemisphere is pale yellow in color. Three tadpoles putatively assigned to the new species and at stage ( Gosner, 1960) 35–36 (total length = 39.0–39.9 [39.6±0.5] mm, head-body length = 13.6–14.1 [13.8±0.3] mm) are nearly same as those of L. selatan described below in body shape and coloration (see Fig. 7 ).

Comparisons. Limnonectes utara is most similar to L. selatan sp. nov., but is significantly larger in male SVL, and has relatively smaller internarial space, tibia, hindlimb, and first toe, and larger inner metatarsal tubercle and fourth toe disk. The dorsal dark markings are clearer and more confluent, marking on rear of thigh is less clear, and the circum-cloacal warts are less developed than in L. selatan ( Fig. 6 ). The new species, along with L. selatan , is differentiated from all the other named species except for some Bornean L. kuhlii -like frogs by their tibia, which is heavily covered by large, conical tubercles (vs. tibia at most with weak tubercles dorsally). In addition, it differs from L. namiyei by the lack of vocal openings, and from L. fragilis by smaller subarticular tubercles and possession of nuptial pads in males. From L. kuhlii , it differs in possession of nuptial pads in males and larger body size (mean SVL 74 mm in males and 70 mm in females vs. 62 mm and 59 mm, respectively, in L. kuhlii ). The new species, with a back usually without distinct ridges, and nuptial pad only on the first finger, differs from L. fujianensis , which has a back with many ridges, including a dorsolateral ridge, and nuptial pads on the two inner fingers. From L. bannaensis , it differs by lacking nuptial pad on the second finger. Limnonectes utara sp. nov. invariably has confluent dark dorsal marking unlike L. jarujini and L. isanensis , which usually lack dark dorsal markings. Limnonectes utara sp. nov. differs from L. taylori in having few dorsal warts, which are much more abundant and widely present in L. taylori . From L. megastomias , L. utara sp. nov. differs in having a smaller body size, relatively shorter head, lacking a nuptial pad on the second finger, and not having a heavily pigmented venter. In addition, the second finger is not constantly longer than first in the new species, unlike L. megastomias .

Range. Peninsular Malaysia: Bukit Larut (= Larut Hill), State of Perak, (600–680 m a.s.l., 1160 m a.s.l.), Sungai Tembat, Hulu Terengganu, State of Terengganu, (168–170 m a.s.l.). Records of Rana or Limnonectes kuhlii from Larut Hills at about 4500 ft ( Berry 1975), Ulu Kenas Recreational Forest, Gunung Bubu ( Grismer et al. 2010), and Gunung Lawit (790 m), State of Terengganu ( Dring 1979) are thought to represent this species (see Discussion). Known localities range in altitude from 168–1372 m a.s.l.

Natural history. At the type locality (1160 m a.s.l.), the type series of L. utara sp. nov. was found in and along a small stream in a roadside ditch (width <1 m) in a secondary forest, while at the lower elevation site (680 m a.s.l.), frogs were found at the edge of the shaded main stream (width <3 m) in dipterocarp forest. Females collected in early January and late February had fully developed ova in ovaries. Tadpoles in later stages of development were also found in early January. Therefore, the breeding period may be relatively extended. Other amphibian species at the type locality were Megophrys longipes , Leptolalax heteropus , Ansonia malayana , Limnonectes khasianus , L. blythii , Amolops larutensis , Odorrana hosii , Hylarana banjarana , Philautus petersi , and Ichthyophis larutensis .

Karyotype. The diploid chromosome number is 22, with six large and five small pairs (Matsui, unpub. data).

Figures

FIGURE 3. Dorsolateral views of male holotypes of Limnonectes utara sp. nov. (UKMHC 528) from Larut Hill (A) and L. selatan sp. nov. (UKMHC 529) from Genting Highlands (B).

FIGURE 4. Dorsal (A, C) and ventral (B, D) views of anesthetized male holotypes of Limnonectes utara sp. nov. (UKMHC 528) from Larut Hill (A, B) and L. selatan sp. nov. (UKMHC 529) from Genting Highlands (C, D) Scale bar = 10 mm.

FIGURE 5. Ventral views of hand (A) and foot (B) of male holotype of Limnonectes utara sp. nov. (UKMHC 528) from Larut Hill, and preaxial view of hand (C) and ventral view of foot (D) of male holotype of L. selatan sp. nov. (UKMHC 529) from Genting Highlands. In anesthetized state, scale bar = 10 mm.

FIGURE 6. Posterior views of left thigh of preserved male holotypes of Limnonectes utara sp. nov. (UKMHC 528) from Larut Hill (A) and L. selatan sp. nov. (UKMHC 529) from Genting Highlands (B), showing circum-cloacal warts and dark blotches along dorso-ventral border. Not to scale.

FIGURE 7. Lateral (A, D), dorsal (B, E), and ventral (C, F) views, and oral disk (G, H) of larvae putatively assigned to Limnonectes utara sp. nov. from Larut Hill (A, B, C, G: KUHE 49514, Stage 36, total length = 39.9 mm) and confirmed as Limnonectes selatan sp. nov. from Genting Highlands (D, E, F, H: KUHE 49515, Stage 38, total length = 45.4 mm) after preservation. Scale bar for A–F= 10 mm. G, H=not to scale.

FIGURE 10. Schematic map of the Malay Peninsula, illustrating the five mountain ranges (from west to east: A, Banjaran Bintang; B, Banjaran Titiwangsa; C, Banjaran Benom; D, Banjaran Gunung Tahan; E, Banjaran Timur), the type localities (filled triangles) of Limnonectes utara sp. nov. (Larut Hill) and L. selatan sp. nov. (Genting Highlands), and known localities of either of the two or unidentified species (dark circles: 1, Hulu Terengganu; 2, Ulu Gombak; 3, Gunung Bubu; 4, Gunung Lawit; 5, Endau Rompin). Hatching indicates areas 300 m a.s.l. and above in elevation.