A group of fanged frogs from Southeast and East Asia has long been considered a single widespread species Limnonectes kuhlii, but occurrence in this group of many cryptic species has recently been demonstrated mainly in the continent through molecular phylogenetic analyses. This led to similar analyses of populations from other parts of the known range, and phylogenetic relationships inferred for frogs from the island of Borneo through mitochondrial and nuclear DNA resulted in the presence of nearly 20 distinct lineages. We studied morphological variation in 13 of these lineages from the Malaysian part and confirmed their taxonomically distinct statuses. We applied existing names to three of them, L. conspicillatus, L. kong, and L. mocquardi, and described 10 remaining ones as new species.
Introduction
Limnonectes kuhlii (Tschudi, 1838), originally described (as Rana kuhlii) from Java, was long thought to be distributed very widely, from southern China to Thailand and Malaysia on the continent, and Sunda Islands, including Sumatra, Java, and Borneo (e.g. Boulenger, 1920; Liu and Hu, 1961; Taylor, 1962; Inger, 1966; Berry, 1975). However, intensive taxonomic studies, mainly made on continental populations, have revealed that they are distinct from L. kuhlii at the species level (e.g., Ye and Fei, 1994; McLeod, 2010; Matsui et al., 2013). These studies were made chiefly based on molecular phylogenetic approaches.
Populations of fanged frogs on Borneo Island have been studied molecular phylogenetically (Matsui et al., 2016). The Bornean lineages, L. hikidai Matsui and Nishikawa, 2014b, and L. asperatus (Inger, Boeadi, and Taufik, 1996) formed a clade with their sister species, L. cintalubang Matsui, Nishikawa, and Eto, 2014c, which together was monophyletic with the clades of (1) Javanese L. kuhlii and Sumatran L. sisikdagu McLeod, Horner, Husted, Barley, and Iskandar, 2011, (2) Chinese L. fragilis (Liu and Hu, 1973), and (3) the clade of the continental species (Thai L. taylori Matsui, Panha, Khonsue, and Kuraishi, 2010, L. isanensis McLeod, Kelly, and Barley, 2012, and L. jarujini Matsui, Panha, Khonsue, and Kuraishi, 2010, Chinese L. bannaensis Ye, Fei, Xie, and Jiang, 2007 and L. fujianensis Ye and Fei, 1994, and Japanese L. namiyei (Stejneger, 1901), with unresolved relationships.
As shown in Fig. 1, occurrence of 17 genetically distinct lineages (plus L. hikidai and L. asperatus) in two clades (Clade A and Clade B) was ascertained in a mitochondrial (mt) DNA phylogeny in the Bornean fanged frogs (Matsui et al., 2016). In Clade A, Lineages 1–8 (plus L. hikidai and L. asperatus) were recognized, and it was split into Clade A1 (Lineages 1–5) and Clade A2 (Lineages 6–8). Whereas Clade B contained Lineages 9–17, and it was split into Clade B1 (only Lineage 9) and Clade B2 (Lineages 10–17). Of these, only three (Lineage 6=L. conspicillatus (Günther, 1872), Lineage 9=L. mocquardi, Matsui, Dubois, and Ohler, 2013, and Lineage 8=L. kong Dehling and Dehling, 2017) have names and the remaining lineages still need taxonomic decisions.
Fig. 1.
Mitochondrial genealogy of Limnonectes kuhlii-like frogs and close relatives from Borneo. Numbers in bold italic face indicate assigned lineages. Modified from Matsui et al. (2016). Capital letters indicate clades and subclades.
Each of these unnamed lineages can represent a species, because some of them are syntopic and must be heterospecific with each other, and others are genetically well differentiated in mtDNA. However, assessment of taxonomic status and formal description of these cryptic members have never been made partly because of the lack of morphological knowledge.
The purpose of this study is to analyze morphological variation among genetic lineages from the Malaysian part of Borneo that were elucidated by Matsui et al. (2016), to determine taxonomic status of each lineage, and to provide formal descriptions of undescribed forms. Of the 17 lineages recognized in the mtDNA tree, Malaysian Lin. 2 and Lin. 12 included a small number of samples, and Lin. 3 and 4 were form Kalimantan, Indonesian Borneo, where sampling was insufficient. These four lineages were excluded in the present morphological study. Mitochondrial Lin. 7 and Lin. 8, and Lin. 13 and Lin. 14, respectively, partially mingled in the nuclear (nu) DNA tree, but they were separately treated in examining morphological variation.
Materials and Methods
Morphological analyses
Specimens examined are stored in 70% ethanol at the BORNEENSIS (BOR) collection, the University Malaysia Sabah (UMS); Sabah Parks (SP); the Sarawak Forestry Corporation (SFC-GRB) and the Kyoto University, Graduate School of Human and Environmental Studies (KUHE). We also studied type series of L. conspicillatus at Natural History Museum, London (BMNH), and of L. mocquardii at Museum National d' Histoire Naturelle, Paris (MNHN).
We took body measurements to the nearest 0.1 mm, and when necessary, using a binocular dissecting microscope, mainly, following Matsui (1984, 1994): (1) snout-vent length (SVL); (2) head length (HL), from tip of snout to hind border of angle of jaw (not measured parallel to the median line); (3) snout length (SL); (4) eye length (EL), including eyelid; (5) head width (HW); (6) internarial distance (IND); (7) interorbital distance (IOD); (8) upper eyelid width (UEW); (9) lower arm and hand length (LAHL) from elbow to tip of third finger; (10) forelimb length (FLL); (11) inner metacarpal tubercle length (IMCTL=thenar tubercle); (12) first finger length (1FL), from distal end of inner metacarpal tubercle to tip of first finger; (13) hindlimb length (HLL); (14) thigh length (THIGHL), from vent to tip of knee; (15) tibia length (TL); (16) foot length (FL); (17) inner metatarsal tubercle length (IMTL); (18) first toe length (1TOEL), from distal end of inner metatarsal tubercle to tip of first toe. We also measured: (19) third finger disk width (3FDW); (20) basal width of third finger disk (3FDbW); (21) fourth toe disk width (4TDW); and (22) basal width of fourth toe disk (4TDbW).
In the statistical analyses for the morphological characters 1–18, we separated sexes, because these frogs are known to exhibit pronounced sexual dimorphisms in some of them (Inger, 1966; Matsui, 1979). We compared SVL by Tukey-Kramer test, while we performed Dunn's multiple comparison tests for ratio values and detection of the presence or absence of differences in the frequency distributions. Significance level of 5% was used in all statistical tests. All statistical analyses were performed by R 3.6.1 (R Core Team, 2023). In the following description, average values are shown with 1 standard deviation (±SD).
We conducted multivariate analyses using log10-transformed metric values for examining overall morphological variation among 13 male and 12 female mitochondrial lineages. Samples of Lin. 15 lacked females. We conducted canonical discriminant analysis (CANDISC) using R 3.6.1.
Results
Univariate analyses
Concurring mtDNA separation (Matsui et al., 2016), 13 genetic lineages of Limnonectes kuhlii-like frogs from Malaysian Borneo were separated from each other in morphometric characters. As shown in comparisons of each lineage (Table 1, 2), results of the Tukey-Kramer test indicated that some lineages significantly differed from the other lineages in SVL (P<0.05), and similarly, significant differences were detected in the ratio characters between some lineages (Dunn's multiple comparison tests, P<0.05).
As stated above, Lin. 7 and Lin. 8 (L. kong), and Lin. 13 and 14, respectively, were discriminated by mtDNA, but not by nuDNA (Matsui et al., 2016). Comparisons of these two combinations resulted in each one significant difference: Lin. 7 and Lin. 8 (L. kong) differed in the ratio of disk of fourth toe to disk of third finger, and Lin. 13 and Lin. 14 differed in the ratio to SVL of inner metacarpal tubercle in males.
Table 1.
Measurements in Limnonectes kuhlii-like fanged frogs from Malaysian Borneo. SVL (mean±SD, in mm) and medians of ratios (R) of other characters to SVL, followed by ranges in parentheses. See text for character abbreviations.
Continued.
Table 2.
Measurements in finger and toe disks in Limnonectes kuhlii-like fanged frogs from Malaysian Borneo. Medians of ratios (R) of characters to SVL, and ratios of characters, followed by ranges in parentheses. See text for character abbreviations.
Multivariate analyses
CANDISC analysis resulted in poor separation of lineages in both sexes (Fig. 2). In males, roughly three groups, i.e., Lin. 6 (L. conspicillatus), Lin 8 (L. kong), and Lin. 9 (L. mocquardi), were recognized on the first two axes (CAN1–CAN2). Lin. 6 and Lin. 8 did not overlap, but Lin. 6 and Lin. 9 overlapped slightly. Lin. 6 largely overlapped with Lin. 10, while Lin. 8 overlapped with Lin. 7. Each half of Lin. 9 and Lin. 11 overlapped, and Lin. 1, Lin. 11–14, and Lin. 16–17 overlapped them. On CAN1–CAN3 plane, Lin. 8 and Lin. 9 partly overlapped, and were separated from Lin. 14 and Lin. 16–17 that had larger values on CAN3 axis. The proportions of eigenvalues of the first (CAN1), second (CAN2), and third (CAN3) axes accounted for 0.298, 0.214, and 0.161, respectively. On the first axis, the highest absolute magnitude of the standardized canonical discriminant coefficients was 52.17 of HW, followed by LAHL (49.99), FL (–48.81), SVL (–39.81), and LAHL (–9.84). On the second axis, HW (–26.51), 1FL (23.58), and 1TOEL (–21.66) were high contributors.
Separation in females was worse than in males, but Clade A (Lin. 1, 5, 6, 7, 8) based on mtDNA tended to form a group with larger values than Clade B on the CAN1 axis. The proportions of eigenvalues of the first three axes accounted for 0.345, 0.204, and 0.152, respectively. SVL (–39.11), SL (27.74), 1TOEL (–25.20), and HLL (20.96) on the first axis, and LAHL (–44.15), SL (30.59), and FL (26.09) on the second axis, were high contributors.
Fig. 2.
Canonical components scores of morphological variables for male (A) and female (B) samples of fanged frogs. Lin. 1: Lineage 1; Lin. 5: Lineage 5; Lin. 6: L. conspicillatus; Lin. 7: Lineage 7; Lin. 8: L. kong; Lin. 9: L. mocquardi; Lin. 10: Lineage 10; Lin. 11: Lineage 11; Lin. 13: Lineage 13; Lin. 14: Lineage 14; Lin. 15: Lineage 15; Lin. 16: Lineage 16; Lin. 17: Lineage 17.
Of lineages genetically mingled by nuDNA (Matsui et al., 2016), only males of Lin. 7 and Lin. 8 overlapped and females of Lin. 7 and Lin. 8, as well as both sexes of Lin. 13 and 14 were discriminated in both sexes by the first two axes (CAN1–CAN2).
The lineages that occur sympatrically (Matsui et al., 2016) tended to be separated on the first two axes (CAN1–CAN2). Nine combinations (Lin. 1 vs 13, Lin. 5 vs 9, 16, and 17, Lin. 6 vs 8, Lin. 8 vs 14 and 15, Lin. 13 vs 16, and Lin. 14 vs 15) in males and eight combinations (Lin. 6 vs 10, Lin. 5 vs 9, 16, and 17, Lin. 8 vs 14 and 15, Lin. 13 vs 16, and Lin. 14 vs 15) in females did not overlap. In contrast, lineages largely overlapped in Lin. 1 vs 11, Lin. 6 vs 10, and Lin. 9 vs 17, and partly overlapped in Lin. 9 vs 13 in males. In females, Lin. 9 vs 17 completely overlapped, Lin. 9 vs 13 largely overlapped, Lin. 1 vs 11 and Lin. 6 vs 8 slightly overlapped, and Lin. 1 vs 13 partly overlapped.
These results of the morphological analyses concur with the previous results of phylogenetic analyses, which strongly suggested that each of the 13 lineages examined is a genetically distinct species (Matsui et al., 2016). Because three of these 13 lineages already have valid names, we name below each of the 10 remaining lineages as a distinct species.
Systematics
1. Limnonectes tawauensis Matsui, Nishikawa et Shimada sp. nov.
[English name: Tawau Fanged Frog]
Fig. 3A, B
Rana kuhli (part) Inger, 1966, 196.
Limnonectes sp. Lineage 1 Matsui et al., 2016, 307.
Holotype
KUHE 8450, an adult male from Brumas Plantation, Sabah Softwoods Sdn. Bhd., Tawau, Tawau District, Tawau Division, Sabah (04°38′ N, 117°44′ E, 120 m asl), collected between 20 and 29 September 1985 by M. Matsui.
Paratypes
Sabah. KUHE 8474–8476 data same as the holotype. BOR 09074 collected on 28 July 2004, BOR 09198, 09224, 09225 on 30 July 2004, BOR 09232, 09234 on 1 August 2004, BOR 09251 on 2 August 2004, BOR 22016–22021, 22058, 22059 on 3 August 2004, BOR 22100, 22101 on 4 August 2004, BOR 22166 on 6 August 2004, all from Tawau Hills National Park (04°23′54″ N, 117°53′13″ E, 269 m asl) by M. Matsui, K. Nishikawa, and T. Shimada.
Referred specimens
Sabah. KUHE 8982–9002 data same as the holotype. BOR 22279, 22281 from Tabin Wildlife Reserve, (05°16′ N, 118°39′ E, 150 m asl) collected on 11 August 2004. BOR 22346, 22347 on 18 August 2004, BOR 22495 on 17 March 2005 from Paginatan, between Ranau and Telupid, Sabah (5°46′N, 116°49′E, 120 m asl). BOR 22800 from Sungai (Sg.=River) Kipungit 2, Poring, Kinabalu National Park (KNP), 400 m asl. BOR 22852, SP 01601, SP 21070 (former BOR 22805) from Hot Spring–Sg. Kipungit 2, Poring, KNP, on 7 August 2005. BOR 12848, 12849 from Masak, Crocker Range National Park (CRP), 610 m asl on 19 August 2003. SP 21655–21658 from Kinolosodon, CRP, 133 m asl. BOR 23405, 23407, 23436 from Sg. Kilanpung, CRP, 380 m asl on 17 August 2005. BOR 12803 from Ulu Senagan, CRP, (05°20′40″ N, 116°01′45″ E, 550 m asl) on 17 August 2003. BOR 08837 from Trail 4 of UMS-JICA 2002 expedition to the Crocker Range (Kueh et al., 2004), Ulu Kimanis, Papar, on 4 December 2003. BOR 08099, 08104 from Base Camp of UMS-JICA 2002 expedition to the Crocker Range, Ulu Kimanis, Papar, 144 m asl on 28 August 2002. SP 00327 from Sg. Kadamaian, Kiau, KNP collected on 6 May 1985 by Tan Fui Lian. KUHE 38013 from Imbak, Deramakot Forest Reserve (05°04′ N, 116°57′ E, 150 m asl) collected on 14 May 2004 by A. Mori.
Etymology
The specific epithet tawauensis is derived from the District of Tawau, eastern Sabah, where the new species occurs.
Diagnosis
The new species can be differentiated from its relatives by the combination of tibia, dorsally, densely covered by large warts with pointed tips and intervening minute warts (Fig. 11A); first finger slightly longer than second. A medium-sized species with adult mean SVL 49 mm in males and 51 mm in females; head medium-sized; forelimb short; hindlimb short; tibia short; dorsal skin scattered with warts, from which networks of wrinkles originating and running in all directions; outer edge of third finger with freely movable, narrow ridges of skin; tip of third finger forming small disk, width not much wider than basal phalanx (Fig. 10A); tip of fourth toe swollen into small disk, width wider than basal phalanx; fourth toe disk wider than third finger disk; fourth toe broadly webbed to disk; inner and outer webbing of fourth toe little excised (Fig. 12A); dorsum olive brown with dark brown marking on scattered warts.
Description of holotype (measurements in mm)
SVL 60.0; habitus moderately stocky; head not enlarged and medium-sized, longer (HL 28.8, 48.0%SVL) than broad (HW 26.0, 43.3%SVL); snout slightly pointed, rounded in profile, projecting beyond lower jaw; eye length (EL 9.4, 15.7%SVL) as large as snout length (SL 9.4, 15.7%SVL); canthus distinct; lore slightly sloping, concave; nostril dorsolateral, below canthus, slightly closer to snout than to eye; internarial distance (IND 4.9, 8.2%SVL) narrower than interorbital distance (IOD 5.2, 8.7%SVL), latter wider than upper eyelid (UEW 4.2, 7.0%SVL); pineal spot visible; tympanum indistinct but visible, oval, diameter (TD 3.3, 5.5%SVL) less than half eye length and separated from eye (T-EL 4.4, 7.3%SVL) by more than tympanum diameter; vomerine teeth in oblique groups, between medial rims of choanae, groups closely set from one another, and from choana by half length of one group; lower jaw with a pair of sharply pointed tooth-like projections near symphysis, more than twice the depth of mandible at base of projections; vocal sac and vocal slits absent.
Forelimb short (FLL 34.7, 57.8%SVL; LAHL 25.3, 42.2%SVL); fingers moderately slender; first finger longer than second; length of first, measured from distal edge of inner metacarpal tubercle (1FL 8.4, 14.0%SVL) shorter than length of eye; tips of fingers slightly swollen, forming small disks without circummarginal grooves; disk width of third finger (3FDW 1.0, 1.7%SVL) not much wider than basal phalanx; remnant of webs between fingers; inner metacarpal tubercle moderate (IMCL 2.5, 4.2%SVL) oval, slightly elevated; middle metacarpal tubercle oval, as large as and not contacting inner metacarpal tubercle; outer metacarpal tubercle elongate, as large as inner metacarpal tubercle; proximal subarticular tubercles oval and elevated; distal subarticular tubercles low, but distinct; no supernumerary metacarpal tubercles; outer edge of third finger with freely movable, narrow ridge of skin.
Hindlimb short (HLL 86.2, 143.7%SVL) less than three times length of forelimb; tibia short (TL 26.6, 44.3%SVL), heels not overlapping when limbs are held at right angles to body; tibiotarsal articulation of adpressed limb reaching to posterior corner of eye; foot (FL 27.2, 45.3%SVL) slightly longer than tibia; tips of toes swollen into small disks, disk width of fourth toe (4TDW 1.15, 1.9%SVL) wider than basal phalanx and disk width of third finger (3FDW); inner and outer webbing of fourth toe little excised; fourth toe broadly webbed to disk; a flap of skin along outer edge of fifth toe freely movable; subarticular tubercles oval and distinct; an elongate inner metatarsal, length (IMTL 3.7, 6.2%SVL) less than half length of first toe (1TOEL 7.7, 12.8%SVL); no outer metatarsal tubercle.
Dorsal skin scattered with warts, from which networks of wrinkles originate and run in all directions; wrinkles very weak on head; very weak transverse fold between inner margins of upper eyelids; temporal fold from eye to above insertion of upper arm; large warts, covered by warts tipped with white, dense on posterior dorsum; side of trunk covered with fine tubercles; anus surrounded by groups of minute warts from above and below; dorsal surface of tibia densely covered by small warts among scattered large warts with pointed tips; tarsus with a thick dermal ridge extending proximally from metatarsal tubercle; throat very slightly wrinkled; chest, and abdomen smooth; distinct yellow-brownish tinge, but without asperities, forming a nuptial pad covering medial surface of first finger from its base to level of subarticular tubercle.
Color
In preservative, dorsum olive brown with dark brown marking on interorbital and upper eyelid bar, and scattered warts, from which networks of wrinkles originating; an oblique dark brown supratympanic stripe from behind eye to above arm insertion; canthus rostralis banded with dark brown; side of head from posterior half of lore to inguinal area paler brown; lateral side of trunk without marking, sharply split into dorsal brown and ventral cream; dark brown bars on upper and lower lips indistinct; limbs with dark crossbars dorsally; ventral side of upper arm covered with dark brown; throat cream weakly dusted with pale brown; chest to abdomen and ventral side of limbs cream.
Variation
SVL did not differ between the sexes, and the ratios to SVL were not sexually dimorphic, either (Table 1). Pineal spot sometimes absent; tympanum hidden, but sometimes visible or evident; freely movable, narrow ridge of skin sometimes present on outer edge of second and inner edge of third fingers. Body sometimes reddish brown, and some with wide, cream middorsal stripe; supratympanic dark marking narrow or wide; vertical dark bar on upper lip vague or indistinct, and on lower lip indistinct; throat cream, dusted with brown, mottled with light brown or brown, or heavily mottled with brown.
Comparisons
Limnonectes tawauensis sp. nov. is sympatric with L. paginatanensis sp. nov. at Paginatan and Poring, KNP, and with L. separatus sp. nov. at lower altitudes of CRP, but easily differentiated from the other species by its tibia, which dorsally, is densely covered by warts.
The uncorrected pairwise sequence divergence for fragments (445 bp) of 16S rRNA between L. tawauensis sp. nov. and the co-occurring L. paginatanensis sp. nov. and L. separatus sp. nov. is 7.8–8.3 and 6.8–7.3%, respectively (Matsui et al., 2016).
Morphometrically, L. tawauensis sp. nov. differs from L. conspicillatus by larger eye (median REL 15.4%SVL vs. 14.1%SVL) in males; from L. penerisanensis sp. nov. by smaller inner metatarsal tubercle (median RIMTL 7.2%SVL vs. 8.4%SVL) in males, and by narrower disk of third finger (R3FDW median 1.8%SVL vs. 2.6%SVL) and fourth toe (R4TDW median 2.3%SVL vs. 3.6%SVL), and smaller ratio of disk to base of third finger (3FDW/3FDbW median 1.0 vs. 1.3); from L. paginatanensis sp. nov. by narrower disk of third finger (R3FDW median 1.8%SVL vs. 2.7%SVL) and fourth toe (R4TDW median 2.3%SVL vs. 3.6%SVL); from L. separatus sp. nov. by longer first finger (median R1FL 14.2%SVL vs. 13.1%SVL) in males; from L. lanjakensis sp. nov. by longer eye (median REL 15.4%SVL vs. 14.1%SVL), shorter forelimb (median RFLL 56.8%SVL vs. 60.5%SVL), and smaller inner metatarsal tubercle (median RIMTL 7.2%SVL vs. 8.3%SVL) in males, and by narrower disk of third finger (R3FDW median 1.8%SVL vs. 2.6%SVL) and fourth toe (R4TDW median 2.3%SVL vs. 3.7%SVL); from L. batulawensis sp. nov. by narrower disk of third finger (R3FDW median 1.8%SVL vs. 2.5%SVL), disk of fourth toe (median R4TDW 2.3%SVL vs. 3.8%SVL), and base of fourth toe disk (R4TDbW median 1.6%SVL vs. 2.9%SVL); and from L. paulyambuni sp. nov. by shorter thigh (median RTHIGHL 48.7%SVL vs. 52.4%SVL in males, 49.0%SVL vs. 55.2%SVL in females) and smaller inner metatarsal tubercle (median RIMTL 7.2%SVL vs. 7.9%SVL) in males, and by narrower disk of fourth toe (R4TDW median 2.3%SVL vs. 3.6%SVL).
Range
Endemic to Sabah. Tawau Division, Tawau District, Tawau, 120 m asl, 269 m asl. Lahad Datu Division, Tawau District, Tabin Wildlife Reserve, 150 m asl. Sandakan Division, Tongod District, Imbak, Deramakot Forest Reserve, 150 m asl. West Coast Division, Ranau District, Paginatan, 120 m asl; Poring, KNP, 400 m asl; Kiau, KNP, 900 m asl. West Coast Division, Papar District, Kinolosodon, CRP, 133 m asl; Ulu Kimanis, Papar, 144 m asl. Interior Division, Keningau District, Masak, CRP, 610 m asl; Sg. Kilanpung, CRP, 380 m asl; Ulu Senagan, CRP, 550 m asl.
Natural history
Matsui (2016 as Limnonectes cf. kuhlii) split juvenile and adults by SVL (<38 mm and >42 mm, respectively) and analyzed stomach contents. Juvenile frogs always had stomach content mass of up to 3% of body mass, and had a larger average number of small food items compared to adults. In adult, few individuals lacked stomach contents, and food items were generally larger than in juvenile frogs.
Fig. 3.
Dorsal (A, C) and ventral (B, D) views of male paratype of Limnonectes tawauensis sp. nov. (BOR 09232, A, B) and female holotype of L. barioensis sp. nov. (SFC-GRB-00599 [=former KUHE 53065], C, D). Scale bar=10 mm.
2. Limnonectes barioensis Matsui et Nishikawa sp. nov.
[English name: Bario Fanged Frog]
Fig. 3C, D
Limnonectes sp. Lineage 5 Matsui et al., 2016, 307.
Holotype
SFC-GRB-00599 (former KUHE 53065), an adult female from a stream along the trail to New Dam, Bario, Bario Subdistrict, Miri District, Miri Division, Sarawak (03°45′N, 115°26′E, 1150 m asl), collected on 17 August 2009 by M. Matsui.
Paratypes
Sarawak. SFC-GRB-00600 (former KUHE 42535) from Failed Dam, Bario (03°46′07″N, 115°27′20″E, 1022 m asl) collected on 17 August 2008 by M. Matsui. SFC-GRB-00601 (former KUHE 53091) from Pa Ramapuh, Bario (03°44′N, 115°27′E, 1080 m asl) on 18 August 2009 by M. Matsui.
Referred specimens
Sarawak. KUHE 12374, 12430, 12431 collected between 17–20 January 1991 from Pa Belaban, Bario (03°51′N, 115°31′E, 1150 m asl).
Sabah. BOR 12534, 12535, 12554, 12555 collected on 7 August 2003, BOR 12698 on 10 August 2003 from Mahua, CRP, Tambunan District, Interior Division (05°48′N, 116°24′E, 1200 m asl). SP 21695 from Tambunan, 750 m asl.
Etymology
The specific epithet barioensis is derived from Bario, a town in the Kelabit Highlands in Sarawak, northwestern Borneo, where this species was first found.
Diagnosis
The new species can be differentiated from its relatives by tibia, especially anterodorsally, covered with warts of various size (Fig. 11B); first finger slightly longer than second; tip of third finger forming small disk, width not much wider than basal phalanx (Fig. 10B); fourth toe broadly webbed to disk; inner and outer webbing of fourth toe little excised (Fig. 12B). A medium-sized species with adult mean SVL 54 mm in males and 51 mm in females; head short; forelimb medium-sized; hindlimb medium-sized; tibia short; dorsal skin extremely folded, with networks of wrinkles running in all directions; small warts scattered only posteriorly; outer edge of third finger with freely movable, narrow ridges of skin; tip of fourth toe swollen into moderate-sized disk, width slightly wider than basal phalanx; fourth toe disk much wider than third finger disk; dorsum clay brown with small dark brown marking.
Description of holotype (measurements in mm)
SVL 52.7; habitus moderately stocky; head short and not enlarged, longer (HL 21.6, 41.0%SVL) than broad (HW 20.4, 38.7%SVL); snout slightly pointed, rounded in profile, projecting beyond lower jaw; eye length (EL 7.1, 13.5%SVL) smaller than snout length (SL 7.8, 14.8%SVL); canthus distinct; lore slightly sloping, and concave; nostril dorsolateral, below canthus, slightly closer to snout than to eye; internarial distance (IND 4.4, 8.3%SVL) wider than interorbital distance (IOD 3.5, 6.6%SVL), latter slightly wider than upper eyelid (UEW 3.3, 6.3%SVL); pineal spot visible; tympanum not visible; vomerine teeth set closely together, oblique groups, behind medial rims of choanae, groups separated from one another by one-sixth length of one group, and from choana by one-fourth length of one group, lower jaw with a pair of low projections near symphysis, about twice the depth of mandible at base of projections; vocal sac and vocal slits absent.
Forelimb medium-sized (FLL 29.2, 55.4%SVL; LAHL 22.7, 43.1%SVL); fingers moderately slender; first finger slightly longer than second; length of first, measured from distal edge of inner metacarpal tubercle (1FL 7.2, 13.7%SVL) slightly longer than length of eye; tips of fingers slightly swollen, forming small disks without circummarginal grooves; disk width of third finger (3FDW 0.75, 1.4%SVL) not much wider than basal phalanx; remnant of webs between fingers; inner metacarpal tubercle moderate (IMCL 2.4, 4.6%SVL) oval, slightly elevated; middle metacarpal tubercle oval, as large as and not contacting inner metacarpal tubercle; outer metacarpal tubercle oval, as large as inner metacarpal tubercle; proximal subarticular tubercles oval and elevated; distal subarticular tubercles low, but distinct; no supernumerary metacarpal tubercles; outer edge of third finger with freely movable, narrow ridges of skin; dermal fringes of other fingers not freely movable.
Hindlimb medium-sized (HLL 76.4, 145.0%SVL) less than three times length of forelimb; tibia short (TL 24.4, 46.3%SVL), heels not overlapping when limbs are held at right angles to body; tibiotarsal articulation of adpressed limb not reaching to posterior corner of eye; foot (FL 24.5, 46.5%SVL) subequal to tibia; tips of toes swollen into moderate-sized disks, disk width of fourth toe (4TDW 1.3, 2.4%SVL) slightly wider than basal phalanx, and much wider than 3FDW; inner and outer webbing of fourth toe little excised; fourth toe broadly webbed to disk; a flap of skin along outer edge of fifth toe freely movable; subarticular tubercles oval and distinct; an elongate inner metatarsal, length (IMTL 3.4, 6.5%SVL) nearly half length of first toe (1TOEL 6.9, 13.1%SVL); no outer metatarsal tubercle.
Dorsal skin extremely folded, with networks of wrinkles running in all directions; small warts scattered only posteriorly; wrinkles weak on top of head; indistinct, transverse fold between inner margins of eyelids; several warts on upper eyelid; temporal fold from eye to above insertion of upper arm; side of trunk reticulated with fine wrinkles; vent laterally surrounded by warts; tibia covered with warts of various sizes, especially anterodorsally; tarsus with a thick dermal ridge extending proximally from metatarsal tubercle; throat covered with very weak wrinkles; chest, and abdomen smooth.
Color
In preservative, dorsum clay brown with a few, small dark brown warts, from which networks of wrinkles originating; dark brown markings on interorbital and upper eyelid; interorbital dark bar anteriorly with light bar; canthus rostralis with brown bar; an oblique dark brown temporal stripe medium in width on and along supratympanic fold from behind eye to above arm insertion; lateral side of trunk covered with small brown spots; dark bar unclear on upper lip, and irregular and vague on lower lip; limbs with weak dark crossbars dorsally; ventral side of lower arm covered by dark brown; throat cream weakly dusted with light brown; chest to abdomen cream; ventral side of limbs cream, with dark spots anteriorly and posteriorly; ventral surface of hand and foot gray brown.
Variation
Sexes did not differ in SVL, but the ratios to SVL were larger in males than females in head width (RHW median 42.5%SVL in males and 38.7%SVL in females) and lower arm length (RLAHL 44.9%SVL in males and 43.8%SVL in females).
Snout either slightly dorsally rounded, or slightly pointed; dorsal skin extremely folded, wrinkles running from warts, which may be spiny, or fold sometimes with regularly arranged warts; freely movable skin flap on outer and inner edges of third finger or on outer edge of third finger; dorsally with dark brown spots, sometimes few in number; on lateral body, dorsum brown and venter cream with sharply split or spotted brown at boundary; dark bar on upper lip wide or indistinct, and on lower lip distinct or indistinct; throat dusted, peripherally mottled by light brown spots, or spotted allover.
Comparisons
Limnonectes barioensis sp. nov. is sympatric with L. batulawensis sp. nov. in Bario, Sarawak, L. mocquardi in Mahua and Tambunan, Sabah, and L. paulyambuni sp. nov. in Mahua, Sabah.
The uncorrected pairwise sequence divergences for fragments (445 bp of 16S rRNA) between L. barioensis sp. nov. and the co-occurring L. mocquardi, L. batulawensis sp. nov., and L. paulyambunis sp. nov. are 5.5–8.0%, 7.8–8.5%, and 8.3–10.0%, respectively (Matsui et al., 2016).
Limnonectes barioensis sp. nov. differs from L. conspicillatus by shorter lower arm and hand (RLAHL median 43.8%SVL vs. 44.9%SVL) in females; from L. lambirensis sp. nov. by narrower upper eyelid (RUEW median 7.1%SVL vs. 8.1%SVL), wider internarial (RIND median 8.3%SVL vs. 7.6%SVL) and shorter lower arm and hand (RLAHL median 43.8%SVL vs. 45.1%SVL) in females; from L. penerisanensis sp. nov. by narrower disk of third finger (R3FDW median 1.8%SVL vs. 2.6%SVL) and smaller ratio of disk to base of third finger (3FDW/3FDbW median 1.0 vs. 1.3); from L. lanjakensis sp. nov. by narrower disk of fourth toe (R4TDW median 2.7%SVL vs. 3.7%SVL) and smaller ratios of disk to base of fourth toe (4TDW/4TDbW median 1.2 vs. 1.6); from L. batulawensis sp. nov. by shorter thigh (RTHIGHL median 48.9%SVL vs. 55.1%SVL), tibia (RTL median 47.2%SVL vs. 53.6%SVL), and inner metatarsal tubercle (RIMTL median 6.6%SVL vs. 8.6%SVL) in females, and by narrower base of fourth toe disk (R4TDbW median 2.2%SVL vs. 2.9%SVL); and from L. paulyambuni sp. nov. by shorter thigh (RTHIGHL median 48.9%SVL vs. 55.2%SVL) and shorter lower arm and hand (RLAHL median 43.8%SVL vs. 46.0%SVL) in females.
Range
Sarawak. Miri Division, Miri District, Bario Subdistrict, Bario, 1000 m asl.
Sabah. Interior Division, Tambunan District, Mahua, CRP, 1200 m asl; Tambunan, 750 m asl.
3. Limnonectes conspicillatus (Günther, 1872)
[English name: Matang Fanged Frog]
Fig. 4A, B
Rana conspicillata Günther, 1872, 597.
Rana kuhlii (part) Günther, 1874, 79.
Rana kuhli (part) Inger, 1966, 196.
Limnonectes conspicillatus Matsui et al., 2013, 187.
Limnonectes sp. Lineage 6 Matsui et al., 2016, 307.
Lectotype
BMNH 72.2.18.22=1947.2.29.20 an adult male from “Matang”, Sarawak.
Paralectotypes
BMNH 72.2.19.23–26, 82=1947.2.29.21–27 data same as the holotype.
Referred specimens
Sarawak. KUHE 12025, 12032–12034, 12057 collected on 19 December 1990 at 153 m asl, KUHE 19591 on 24 December 1994 at 225 m asl, KUHE 48715, 48716 on 26 December 2013 from 275 m asl, KUHE 54521, 54523–54526 on 28 December 2012 at 275 m asl, KUHE 17008, 17009 on 24 July 1993 at 300 m asl, KUHE 12444 on 31 January 1991 at 305 m asl, KUHE 10652, 10653 on 21–22 January 1990, KUHE 42641, 42662 on 27–28 November 2008, KUHE 53807 on 27 August 2010, all from Gunung Serapi, Kubah NP, Matang, Kuching District, Kuching Division (around 01°36′25″N, 110°11′27″E). KUHE 48860–48862 on 8 March 2014 from Kubah–Matang, Kuching Division. KUHE 33613 from Gunung Gading NP, Lundu District, Kuching Division (01°41′26″N, 109°50′45″E, 50 m asl) collected on 19 December 1994 by M. Matsui. KUHE 53914 on 2 September 2010, KUHE 54425 on 19 February 2012, KUHE 54466 on 21 February 2012, KUHE 55639, 55640 on 12 March 2013, KUHE 55490 on 13 March 2013, KUHE 48546 on 20 December 2013 all at Batu Panggah, 1040 m asl. KUHE 48518, 48519, 48540 collected on 19 December 2013 at down waterfall stream. KUHE 48647 on 22 December 2013 from the river nr' hostel, 730 m asl by Shimada, all from Gunung Penrissen, Padawan Subdistrict, Kuching District, Kuching Division (01°07′21″N, 110°13′43″E).
Etymology
The specific epithet conspicillatus is Latin meaning spectacled, which may have derived from horizontal dark marking across upper eyelid.
Diagnosis
The species can be differentiated from its relatives by the combination of tibia dorsally coarsely scattered with small, low warts tipped with white (Fig. 11C); first finger longer than second; tip of third finger forming small disk, width not much wider than basal phalanx (Fig. 10C); fourth toe broadly webbed to disk; inner and outer webbing of fourth toe fairly well excised (Fig. 12C). A large-sized species with adult mean SVL 63 mm in males and 60 mm in females; head long; forelimb short; hindlimb short; tibia medium-sized; dorsal skin folded, with networks of wrinkles running in all directions and with few warts; wrinkles very weak and nearly smooth on head; both edges of second and third fingers with broad, moveable dermal flaps; tip of fourth toe swollen into moderate-sized disk, width wider than basal phalanx; fourth toe disk wider than third finger disk; dorsum reddish brown scattered with darker marking; dark brown markings on interorbital and upper eyelid.
Description of a male topotype (KUHE 42662, measurements in mm)
Snout-vent length 70.2; habitus stocky; head long and enlarged, longer (HL 29.7, 42.3%SVL) than broad (HW 28.5, 40.6% SVL); snout slightly pointed, rounded in profile, projecting beyond lower jaw; eye length (EL 9.1, 13.0%SVL) smaller than snout length (SL 10.4, 14.8%SVL); canthus distinct; lore slightly sloping, concave; nostril dorsolateral, below canthus, slightly closer to snout than to eye; internarial distance (IND 6.3, 9.0%SVL) narrower than interorbital distance (IOD 6.6, 9.4%SVL), latter wider than upper eyelid (UEW 5.5, 7.8%SVL); pineal spot visible; tympanum indistinct; lower jaw with a pair of sharply pointed tooth-like projections near symphysis, more than twice the depth of mandible at base of projections; vocal sac and vocal slits absent.
Forelimb short (FLL 40.1, 57.1%SVL; LAHL 30.3, 43.2%SVL); fingers moderately slender; first finger longer than second; length of first, measured from distal edge of inner palmar tubercle (1FL 11.0, 15.7%SVL) longer than length of eye; tips of fingers slightly swollen, forming small disks without circummarginal grooves; disk width of third finger (3FDW 1.25, 1.8%SVL) not much wider than basal phalanx; remnant of webs between fingers; inner metacarpal tubercle moderate (IMCL 3.5, 5.0%SVL) oval, only slightly elevated; middle metacarpal tubercle oval, as large as and not contacting inner metacarpal tubercle; outer metacarpal tubercle oval, smaller than inner metacarpal tubercle; proximal subarticular tubercles oval and elevated; distal subarticular tubercles low, but distinct; no supernumerary metacarpal tubercles; both edges of second and third fingers with broad, moveable dermal flaps.
Hindlimb thick, short (HLL 105.7, 150.6%SVL) less than three times length of forelimb; tibia medium-sized (TL 33.5, 47.7%SVL), heels not overlapping when limbs are held at right angles to body; tibiotarsal articulation of adpressed limb reaching to posterior corner of eye; foot (FL 34.0, 48.4%SVL) nearly as long as tibia; tips of toes swollen into moderate-sized disks, disk width of fourth toe (4TDW 1.65, 2.4%SVL) wider than basal phalanx and much wider than 3FDW; inner and outer webbing of fourth toe slightly and fairly well excised, respectively; fourth toe webbed to disk, but web distal to distal tubercle narrowed; a flap of skin along outer edge of fifth toe freely movable; subarticular tubercles oval and distinct; an elongate inner metatarsal, length (IMTL 6.3, 9.0%SVL) more than half length of first toe (1TOEL 10.0, 14.3%SVL); no outer metatarsal tubercle.
Dorsal skin folded, with networks of wrinkles running in all directions and with few warts; wrinkles very weak and nearly smooth on head; weak transverse fold between inner margins of upper eyelids; temporal fold from eye to above insertion of upper arm; anus with fine warts mainly dorsally; side of trunk reticulated with fine wrinkles; dorsal surface of thigh weakly wrinkled, with few warts distally, that of tibia and tarsus coarsely scattered with small, low warts tipped with white; tarsus with a thick dermal ridge extending proximally from metatarsal tubercle; throat covered with weak wrinkles; chest, and abdomen smooth; distinct brownish tinge, but without asperities, forming a nuptial pad covering medial surface of first finger from its base to level of subarticular tubercle.
Color
In preservative, dorsum reddish brown scattered with darker marking; dark brown markings on interorbital and upper eyelid; a lighter bar anterior to interorbital dark bar; a wide, oblique dark brown supratympanic stripe from behind eye to above arm insertion; canthus rostralis banded with dark brown; lateral side of trunk spotted with light brown; upper lip vaguely barred with dark brown; lower lip with clear dark brown bars; limbs with dark crossbars dorsally; ventral side of upper arm covered with dark brown; throat and chest cream weakly dusted with light brown; abdomen cream; ventral side of limbs weakly dusted with light brown.
Variation
Males differed from females by having a relatively longer and wider head (RHL median 45.8%SVL vs. 42.0%SVL; RHW 41.4%SVL vs. 39.0%SVL), and relatively wider interorbital (RIOD 9.8)%SVL vs. 8.1%SVL).
Snout rounded or pointed in profile; dorsum with weak wrinkles with few warts; weak dorsolateral ridge may be present: tympanum may be visible; tibia scattered with small and minute warts, or warts with wrinkles.
Dorsum may yellow brown with wide, irregular dark marking or few dark markings; some individuals with yellow, mid-dorsal stripe of medium width; dorsum laterally dusted or spotted brown; dark bars on upper and lower lips indistinct or wide; throat dusted or covered by dark brown; chest cream, dusted by brown, or spotted by brown; abdomen and thigh cream, or cream peripherally spotted brown; tibia cream ventrally, with scattered spots, or heavily spotted.
Comparisons
Limnonectes conspicillatus is sympatric in Sarawak with L. kong in Kubah and Gading, and L. penerisanensis sp. nov. in Penrissen.
The uncorrected pairwise distances for fragments (445 bp of 16S rRNA) toward the co-occurring L. kong and L. penerisanensis sp. nov. (see below) are 5.3–6.3% and 7.8–8.0%, respectively (Matsui et al., 2016).
Limnonectes conspicillatus differs from L. tawauensis sp. nov. by shorter eye (REL median 14.1%SVL vs. 15.4%SVL) in males and by shorter head (RHL median 42.0%SVL vs. 42.8%SVL) in females; from L. barioensis sp. nov. by longer lower arm and hand (RLAHL median 44.9%SVL vs. 43.8%SVL) in females; from L. lambirensis sp. nov. by narrower upper eyelid (RUEW median 7.3%SVL vs. 8.1%SVL) in females; from L. penerisanensis sp. nov. by narrower disks of third finger (R3FDW median 2.0%SVL vs. 2.6%SVL) and fourth toe (R4TDW median 2.7%SVL vs. 3.6%SVL), and smaller ratio of disk to base of third finger (3FDW/3FDbW median 1.0 vs. 1.3); from L. paginatanensis sp. nov. by narrower upper eyelid (RUEW median 7.3%SVL vs. 8.4%SVL) in females, and by narrower disk of fourth toe (R4TDW median 2.7%SVL vs. 3.6%SVL) and smaller ratio of disk to base of third finger (3FDW/3FDbW median 1.0 vs. 1.2); from L. lanjakensis sp. nov. by shorter lower arm and hand (RLAHL median 43.7%SVL vs. 46.5%SVL) and forelimb (RFLL median 55.8%SVL vs. 60.5%SVL) in males, and by narrower disk fourth toe (R4TDW median 2.7%SVL vs. 3.7%SVL) and smaller ratios of disk to base of third finger (3FDW/3FDbW median 1.0 vs. 1.2) and fourth toe (4TDW/4TDbW median 1.3 vs. 1.6); from L. abanghamidi sp. nov. by smaller ratio of disk to base of third finger (3FDW/3FDbW median 1.0 vs. 1.2); from L. batulawensis sp. nov. by shorter snout (RSL median 15.7%SVL vs. 16.2%SVL) in males, and by narrower disk and base of fourth toe (R4TDW median 2.7%SVL vs. 3.8%SVL and R4TDbW median 2.0%SVL vs. 2.9%SVL), and from L. paulyambuni sp. nov. by shorter thigh (RTHIGHL median 49.5%SVL vs. 52.4%SVL in males and 49.4%SVL vs. 55.2%SVL in females).
Range
Endemic to Sarawak. Kuching Division, Kuching District, Gunung Serapi, Kubah NP, Matang, 153 m asl, 225 m asl, 275 m asl, 300 m asl, 305 m asl; Kuching Division, Kuching District, Padawan Subdistrict, Gunung Penrissen, Batu Panggah, 1040 m asl; Gunung Penrissen, stream down waterfall near hostel, 730 m asl. Kuching Division, Lundu District, Gunung Gading NP, 50 m asl.
Fig. 4.
Dorsal (A, C) and ventral (B, D) views of male topotype of Limnonectes conspicillatus (KUHE 42662, A, B) and male holotype of L. lambirensis sp. nov. (SFC-GRB-00602 [=former KUHE 53601], C, D). Scale bar=10 mm.
4. Limnonectes lambirensis Matsui et Nishikawa sp. nov.
[English name: Lambir Fanged Frog]
Fig. 4C, D
Limnonectes sp. Lineage 7 Matsui et al., 2016, 307.
Holotype:
SFC-GRB-00602 (former KUHE 53601), an adult male from Lambir Hills N.P. Lambir, Miri District, Miri Division, Sarawak (04°11′54″N, 114°02′34″E, 465 m asl), collected on 17 August 2010 by M. Matsui and K. Nishikawa.
Paratype:
Sarawak. SFC-GRB-00603 (former KUHE 53600), adult female collected on 16 August 2010 from the type locality.
Referred specimens:
Sarawak. KUHE 53602 on 17 August 2010 from the type locality. KUHE 53686, 53687, 53688 from Bukit Kana, Tatau District, Bintulu Division (02°21′04″N, 112°54′13″E, 200 m asl) collected on 23 August 2010 by M. Matsui and K. Nishikawa. KUHE 53740, 53741 from Bukit Kana, 210 m asl collected on 24 August 2010.
Etymology:
The specific epithet lambirensis is derived from Lambir Hills, northwestern Sarawak, where the new species occurs.
Diagnosis
The new species can be differentiated from its relatives by the combination of tibia dorsally coarsely scattered with small, conical warts (Fig. 11D); first finger longer than second; tip of third finger forming moderate-sized disk, width not much wider than basal phalanx (Fig. 10D); tip of fourth toe swollen into small disk, width slightly wider than basal phalanx; fourth toe broadly webbed to disk. A small-sized species with adult mean SVL 59 mm in males and 53 mm in females; head short; forelimb long; hindlimb long; tibia medium-sized; Dorsal skin covered with networks of wrinkles originating from scattered warts and running in all directions, and scattered with warts; edges of second and third fingers with weekly movable, narrow ridges of skin; fourth toe disk slightly wider than third finger disk; inner and outer webbing of fourth toe fairly well excised (Fig. 12D); dorsum brown with darker brown interorbital bar and spots surrounding large warts; abdomen cream peripherally scattered with brown dots.
Description of holotype (measurements in mm)
Snout-vent length (SVL) 65.3; habitus stocky; head enlarged and short, shorter (HL 26.8, 41.0%SVL) than broad (HW 29.3, 44.9% SVL); snout slightly pointed, rounded in profile, projecting beyond lower jaw; eye length (EL 9.2, 14.1%SVL) smaller than snout length (SL 9.6, 14.7%SVL); canthus distinct; lore slightly sloping, concave; nostril dorsolateral, below canthus, slightly closer to snout than to eye; internarial distance (IND 5.1, 7.8%SVL) narrower than interorbital distance (IOD 7.7, 11.8%SVL), latter wider than upper eyelid (UEW 4.9, 7.5%SVL); pineal spot visible; tympanum not visible; lower jaw with a pair of sharply pointed tooth-like projections near symphysis, more than twice the depth of mandible at base of projections; vocal sac and vocal slits absent.
Forelimb long (FLL 38.6, 59.1%SVL; LAHL 28.5, 43.6%SVL); fingers moderately slender; first finger longer than second; length of first, measured from distal edge of inner metacarpal tubercle (1FL 9.4, 14.4%SVL) slightly longer than length of eye; tips of fingers slightly swollen, forming moderate-sized disks without circummarginal grooves; disk width of third finger (3FDW 1.2, 1.8%SVL) not much wider than basal phalanx; remnant of webs between fingers; inner metacarpal tubercle moderate (IMCL 3.9, 6.0%SVL) oval, slightly elevated; middle metacarpal tubercle oval, smaller than and not contacting inner metacarpal tubercle; outer metacarpal tubercle elongate, as large as inner metacarpal tubercle; proximal subarticular tubercles oval and elevated; distal subarticular tubercles distinct; no supernumerary metacarpal tubercles; edges of second and third fingers with weekly movable, narrow ridges of skin.
Hindlimb long (HLL 97.3, 149.0%SVL) less than three times length of forelimb; tibia medium-sized (TL 30.1, 46.1%SVL), heels not overlapping when limbs are held at right angles to body; tibiotarsal articulation of adpressed limb reaching to posterior corner of eye; foot (FL 31.6, 48.4%SVL) slightly longer than tibia; tips of toes swollen into small disks, disk width of fourth toe (4TDW 1.4, 2.1%SVL) slightly wider than basal phalanx and 3FDW; inner and outer webbing of fourth toe fairly well excised; fourth toe broadly webbed to disk; a flap of skin along outer edge of fifth toe freely movable; subarticular tubercles oval and distinct; an elongate inner metatarsal, length (IMTL 4.5, 6.9%SVL) more than half length of first toe (1TOEL 8.2, 12.6%SVL); no outer metatarsal tubercle.
Dorsal skin covered with networks of wrinkles originating from scattered warts and running in all directions, and scattered with warts; wrinkles very weak on eyelid and top of snout; very weak transverse groove between inner margins of upper eyelids; temporal fold from eye to above insertion of upper arm; warts around anus very fine; side of trunk reticulated with fine wrinkles and warts; dorsal surface of tibia coarsely scattered with small, conical warts; tarsus with a thick dermal ridge extending proximally from metatarsal tubercle; throat covered with networks of wrinkles; chest, and abdomen smooth; distinct yellow-brownish tinge, but without asperities, forming a nuptial pad covering medial surface of first finger from its base to level of subarticular tubercle.
Color
In preservative, dorsum orange brown with darker brown interorbital bar and spots surrounding large warts; oblique dark brown temporal stripe of medium width on and along supratympanic fold from behind eye to above arm insertion; side of head without pale marking; canthal dark stripe weak; brown color of lateral side of trunk gradually fading towards cream ventrum; upper and lower lips without bars; limbs with dark crossbars dorsally; throat and anterior chest covered with light brown; posterior chest to abdomen cream peripherally dotted with light brown; ventral side of limbs spotted with brown; ventral surfaces of hand and foot light brown.
Variation
SVL did not differ between the sexes, but the ratios to SVL were sexually dimorphic in some characters: Males have wider head (RHW, median 43.5% in males vs. 39.8% in females), internarial (RIND, 8.0% vs. 7.6%), and interorbital (RIOD, 10.0% vs. 7.8%), and longer forelimb (RFLL, 59.3% vs. 56.4%) and inner metacarpal tubercle (RIMCL, 6.1% vs. 5.5%), while females have wider upper eyelid (RUEW, 7.6% vs. 8.1%) and longer eye (REL, 14.0% vs. 14.5%) (Table 1). Some specimens with oval tympanum of 6.9–8.2%SVL; weekly movable ridges of skin sometimes on edges of third finger; fourth toe webbed to disk, but narrowly distal to distal subarticular tubercle; dorsum with round or elongated warts scattered rather regularly; some with cream middorsal stripe of medium width. A light bar posterior or anterior to interorbital bar; dark bar on lower lip clear or unclear; throat covered by light brown, with few spots, or spotted with large dark brown marking.
Comparisons
Limnonectes lambirensis sp. nov. is not sympatric with other species of the L. kuhlii-like fanged frogs in Borneo.
Limnonectes lambirensis sp. nov. differs from L. tawauensis sp. nov. by longer forelimb (RFLL median 59.3%SVL vs. 56.8%SVL) in males; from L. barioensis sp. nov. by wider upper eyelid (RUEW median 8.1%SVL vs. 7.1%SVL) and longer lower arm and hand (RLAHL median 45.1%SVL vs. 43.8%SVL), but narrower internarial (RIND median 7.6%SVL vs. 8.3%SVL) in females; from L. conspicillatus by wider upper eyelid (RUEW median 8.1%SVL vs. 7.3%SVL) in females; from L. kong by smaller ratio of disk of fourth toe to disk of third finger (4TDW/3FDW median 1.2 vs. 1.3); from L. mocquardi by smaller ratio of disk to base of fourth toe (4TDW/4TDbW median 1.2 vs. 1.5); from L. penerisanensis sp. nov. by narrower disk of third finger (R3FDW median 2.1%SVL vs. 2.6%SVL), disk of fourth toe (R4TDW median 2.5%SVL vs. 3.6%SVL), smaller ratio of disk to base of third finger (3FDW/3FDbW median 1.0 vs. 1.3), and disk to base of fourth toe (4TDW/4TDbW median 1.2 vs. 1.4); from L. paginatanensis sp. nov. by narrower internarial (RIND median 7.6%SVL vs. 8.5%SVL) in females, and by narrower disk of third finger (R3FDW median 2.1%SVL vs. 2.7%SVL), disk of fourth toe (R4TDW median 2.5%SVL vs. 3.6%SVL), smaller ratio of disk to base of third finger (3FDW/3FDbW median 1.0 vs. 1.2) and disk to base of fourth toe (4TDW/4TDbW median 1.2 vs. 1.6); from L. separatus sp. nov. by narrower internarial (RIND median 7.6%SVL vs. 8.4%SVL) in females, and by smaller ratio of disk to base of third finger (3FDW/3FDbW median 1.0 vs. 1.2), of fourth toe (4TDW/4TDbW median 1.2 vs. 1.4), and disk of fourth toe to disk of third finger (4TDW/3FDW median 1.2 vs. 1.4); from L. lanjakensis sp. nov. by narrower disk of fourth toe (R4TDW median 2.5%SVL vs. 3.7%SVL), base of fourth toe disk (R4TDbW median 2.1%SVL vs. 2.3%SVL), smaller ratios of disk to base of third finger (3FDW/3FDbW median 1.0 vs. 1.2), of disk to base of fourth toe (4TDW/4TDbW median 1.2 vs. 1.6), and of disk of fourth toe to disk of third finger (4TDW/3FDW median 1.2 vs. 1.4); from L. abanghamidi sp. nov. by narrower disk of fourth toe (R4TDW median 2.5%SVL vs. 3.2%SVL), smaller ratios of disk to base of third finger (3FDW/3FDbW median 1.0 vs. 1.2), of disk to base of fourth toe (4TDW/4TDbW median 1.2 vs. 1.5), and of disk of fourth toe to disk of third finger (4TDW/3FDW median 1.2 vs. 1.4); from L. batulawensis sp. nov. by narrower internarial (RIND (median 7.6%SVL vs. 9.0%SVL), shorter tibia (RTL median 46.7%SVL vs. 53.6%SVL), thigh (RTHIGHL median 48.1%SVL vs. 55.1%SVL), and inner metatarsal tubercle (RIMTL median 7.0%SVL vs. 8.6%SVL) in females, and by narrower disk of third finger (R3FDW median 2.1%SVL vs. 2.5%SVL) and fourth toe (R4TDW median 2.5%SVL vs. 3.8%SVL), narrower base of fourth toe disk (R4TDbW median 2.1%SVL vs. 2.9%SVL), smaller ratios of disk to base of third finger (3FDW/3FDbW median 1.0 vs. 1.2) and of disk of fourth toe to disk of third finger (4TDW/3FDW median 1.2 vs. 1.5); and from L. paulyambuni sp. nov. by shorter head (RHL median 41.7%SVL vs. 42.2%SVL) and thigh (RTHIGHL median 48.1%SVL vs. 55.2%SVL) in females, and by narrower disk of fourth toe (R4TDW median 2.5%SVL vs. 3.6%SVL), smaller ratios of disk to base of third finger (3FDW/3FDbW median 1.0 vs. 1.1), of fourth toe (4TDW/4TDbW median 1.2 vs. 1.4), and of disk of fourth toe to disk of third finger (4TDW/3FDW median 1.2 vs. 1.4).
Range
Endemic to Sarawak. Miri Division, Miri District, Lambir Hills NP, Lambir 465 m asl. Bintulu Division, Tatau District, Bukit Kana 200 m asl, 210 m asl.
Note
Limnonectes lambirensis sp. nov. and allopatric L. kong have the small uncorrected pairwise sequence divergences for fragments (445 bp of 16S rRNA) of 2.3–4.5%, and in nuclear DNA, they are not clearly differentiated (Matsui et al., 2016).
Fig. 5.
Dorsal (A, C) and ventral (B, D) views of male of Limnonectes kong (KUHE 53824, A, B) and male topotype of L. mocquardi (BOR 22776, C, D). Scale bar=10 mm.
5. Limnonectes kong Dehling et Dehling, 2017
[English name: Poorly Webbed Fanged Frog]
Fig. 5A, B
Rana conspicillata (part) Günther, 1872, 597.
Rana kuhlii (part) Günther, 1874, 79.
Limnonectes sp. Lineage 8 Matsui et al., 2016, 307.
Limnonectes kong Dehling and Dehling, 2017, 300.
Holotype
NMBE (Naturhistorisches Museum der Burgergemeinde Bern, Switzerland) 1059923, an adult male from Kubah NP, Matang Range, Sarawak (1°36′24″N, 110°11′24″E; 290 m asl), collected on 26 September 2009 by J. Maximilian Dehling and D. Matthias Dehling.
Paratypes
Sarawak. NMBE 1059917–1059920, from Kubah NP. NMBE 1059924–1059926 from Bako NP (1°42′40″ N, 110°26′46″ E). NMBE 1059927–1059932, from Gunung Gading NP (1°41′42″ N, 109°50′27″ E). All collected by J. M. Dehling and D. M. Dehling between 22 September and 18 October 2009.
Referred specimens:
Sarawak. KUHE 17085 collected on 7 August 1993, KUHE 17129, 17159, 17160 on 6 August 1993, KUHE 17157 on 8 August 1993, KUHE 17173 on August 1993, KUHE 17185, 17188, 17194, 17195 on 7 August 1993 from Sg. Batu, KUHE 17198, 17199 on 4 August 1993, KUHE 17202–17205 on 5–6 August 1993, KUHE 33614, 33615 on 19 December 1994, all from Gunung Gading NP, Lundu District, Kuching Division (1°41′26″N, 109°50′45″E, 50 m asl). KUHE 17418 collected on 31 August 1993, KUHE 17441, 17442 on 29 August 1993, KUHE 17482 on 25 August 1993 from Sungai Jelak, a branch of Sungai Engkari, Bukit Lanjak, Sri Aman Division (01°20′N, 112°00′E, 350 m asl). KUHE 10651 on 21–22 January 1990, KUHE 19589 on 24 December 1994 from Gunung Serapi 92 m asl, KUHE 19590 on 25 December 1994 from Serapi 275 m asl, KUHE 42642 on 27 November 2008, KUHE 48665 on 23 December 2013, KUHE 48714, 48728 on 26 December 2013 from Rayu Trail, KUHE 48843, 53845 on 7 March 2014, KUHE 54522 on 28 December 2012 from <275 m asl, KUHE 54546 on 29 February 2012 from Matang Wildlife Sanctuary, all Kubah NP, Matang (around 01°36′25″N, 110°11′27″E). KUHE 56025 on 1 September 2015 from Bako NP (01°43′ N, 110°28′ E, 66 m asl). KUHE 53824, 53858, 53859 on 29 August 2010 from Gunung Santubong, Kuching District, Kuching Division (01°44′N, 110°20′E, 60 m asl). KUHE 17584 on 5 September 1993 from Samunsam, 50 m asl. KUHE 47838 on 3 June 2014 from Ranchan, Serian, Serian Division (01°08′30″N, 110°34′57″E, 64 m asl).
Etymology
According to the original description (Dehling and Dehling, 2017), the species epithet, kong, is named after the fictional giant gorilla, which exhibits pronounced male-biased sexual dimorphism, as seen in this species.
Diagnosis
The species can be differentiated from its relatives by the combination of fourth toe broadly webbed to distal subarticular tubercle and not to disk (Fig. 12E); edges of second and third fingers with narrow, non-moveable dermal fringes; tibia dorsally coarsely scattered with warts of various size (Fig. 11E); first finger longer than second. A large-sized species with adult mean SVL 60 mm in males and 53 mm in females; head medium-sized; forelimb short; hindlimb short; tibia short; dorsal skin extremely folded, with networks of wrinkles originating from tubercles of various shape and size, and running in all directions; tip of third finger forming small disk, width not much wider than basal phalanx (Fig. 10E); tip of fourth toe swollen into moderate-sized disk, width slightly wider than basal phalanx; fourth toe disk wider than third finger disk; inner webbing of fourth toe fairly well excised; dorsum brown without darker marking except for interorbital marking.
Description of a male KUHE 53824 from Santubong (measurements in mm)
Snout-vent length (SVL) 68.1; habitus stocky; head enlarged and long, longer (HL 32.2, 47.3%SVL) than broad (HW 30.9, 45.4% SVL); snout slightly pointed, rounded in profile, projecting beyond lower jaw; eye length (EL 9.4, 13.8%SVL) smaller than snout length (SL 11.4, 16.7%SVL); canthus distinct; lore slightly sloping, concave; nostril dorsolateral, below canthus, slightly closer to snout tip than to eye; internarial distance (IND 6.1, 9.0%SVL) narrower than interorbital distance (IOD 7.8, 11.5%SVL), latter much wider than upper eyelid (UEW 4.4, 6.5%SVL); pineal spot present; tympanum not visible; vomerine teeth in oblique groups, between medial rims of choanae, groups closely set from one another, and from choana by half length of one group; lower jaw with a pair of sharply pointed tooth-like projections (odontoid processes) near symphysis, more than twice the depth of mandible at base of projections; vocal sac and vocal slits absent.
Forelimb medium-sized (FLL 38.2, 56.1%SVL; LAHL 31.6, 46.4%SVL); fingers moderately slender; first finger longer than second; length of first, measured from distal edge of inner metacarpal tubercle (1FL 10.5, 15.4%SVL) longer than length of eye; tips of fingers slightly swollen, forming small disks without circummarginal grooves; disk width of third finger (3FDW 1.2, 1.8%SVL) not much wider than basal phalanx; remnant of webs between fingers; inner metacarpal tubercle moderate (IMCL 4.4, 6.5%SVL) oval, slightly elevated; middle metacarpal tubercle oval, smaller than and not contacting inner metacarpal tubercle; outer metacarpal tubercle elongate, as large as inner metacarpal tubercle; proximal subarticular tubercles oval and elevated; distal subarticular tubercles low, but distinct; no supernumerary metacarpal tubercles; edges of second and third fingers with narrow, non-moveable dermal fringes.
Hindlimb thick, short (HLL 102.2, 150.1%SVL) less than three times length of forelimb; tibia short (TL 32.0, 47.0%SVL), heels not overlapping when limbs are held at right angles to body; tibiotarsal articulation of adpressed limb reaching to center of eye; foot (FL 32.5, 47.7%SVL) only slightly longer than tibia; tips of toes swollen into moderate-sized disks, disk width of fourth toe (4TDW 1.4, 2.1%SVL) slightly wider than basal phalanx and wider than 3FDW; inner webbing of fourth toe fairly well excised; fourth toe broadly webbed to distal subarticular tubercle and not to disk; a flap of skin along outer edge of fifth toe freely movable; subarticular tubercles oval and distinct; inner metatarsal elongate, length (IMTL 5.0, 7.3%SVL) more than half length of first toe (1TOEL 7.7, 11.3%SVL); no outer metatarsal tubercle.
Dorsal skin extremely folded, with networks of wrinkles originating from tubercles of various shape and size, and running in all directions; wrinkles weak on head, and posterior half of upper eyelid covered by small warts; very weak transverse groove between inner margins of upper eyelids; temporal fold from eye to above insertion of upper arm; side of trunk reticulated with fine wrinkles; throat covered with very weak wrinkles; chest, and abdomen smooth; anus with fine warts mainly from above; dorsal surface of tibia coarsely scattered with warts of various size; tarsus with a thick dermal ridge extending proximally from metatarsal tubercle; distinct yellow-brownish tinge, but without asperities, forming a nuptial pad covering medial surface of first finger from its base to level of subarticular tubercle.
Color
In preservative, dorsum brown with a narrow cream-colored mid-dorsal stripe, and without darker marking except for interorbital marking; canthus rostralis with dark stripe; a wide, oblique dark brown supratympanic stripe from behind eye to above arm insertion; lateral side of trunk dusted with light brown; upper lip with large dark brown bars; lower lip dark brown and cream bars; throat cream dusted with light brown; chest to abdomen cream; limbs with dark crossbars dorsally; ventral side of limbs dusted with light brown; inner side of upper arm mottled with brown.
Variation
Neither SVL nor the ratios to SVL were sexually dimorphic.
Some with pointed snout; snout may be truncate in profile; outer edge of third finger may be movable; outer webbing of fourth toe may be slightly excised; dorsum may with large conical warts evident posteriorly; tibia may be scattered with warts mainly distally, or with ridge and large warts.
Dorsum may have black spots on warts; dorsum normally without mid-dorsal stripe, or stripe may be narrow; light colored bar usually present anterior to interorbital brown bar; side of trunk may be gradually paler, and suddenly change in color; upper lip bar indistinct or wide; lower lip bar indistinct or distinct; throat may be slightly dusted, heavily dusted, mottled, or heavily mottled brown; thigh may be cream ventrally.
Comparisons
Limnonectes kong is sympatric with L. conspicillatus at Kubah and Gading, and L. lanjakensis sp. nov. and L. abanghamidi sp. nov. at Lanjak Entimau but has fourth toe broadly webbed only to distal subarticular tubercle and not to disk, unlike fully webbed in other species.
The uncorrected pairwise sequence divergences for fragments (445 bp of 16S rRNA) between L. kong and the co-occurring L. conspicillatus, L. lanjakensis sp. nov. and L. abanghamidi sp. nov. (see below) is 5.3–6.3%, 5.8–6.5%, and 8.3–8.5%, respectively (Matsui et al., 2016).
Limnonectes kong differs from L. lambirensis sp. nov. by larger ratio of disk of fourth toe to third finger (4TDW/3FDW median 1.3 vs. 1.2); from L. penerisanensis sp. nov. and L. paginatanensis sp. nov. by narrower disk of third finger (R3FDW median 2.0% vs. 2.6 and 2.7%, respectively) and fourth toe (R4TDW median 2.5%SVL vs. 3.6%SVL), and smaller ratio of disk to base of third finger (3FDW/3FDbW median 1.0 vs. 1.3 and 1.2, respectively); from L. separatus sp. nov. by smaller ratio of disk to base of third finger (3FDW/3FDbW median 1.0 vs. 1.2); from L. lanjakensis sp. nov. and L. abanghamidi sp. nov. by narrower disk of fourth toe (R4TDW median 2.5%SVL vs. 3.7%SVL and 3.2%SVL, respectively) and smaller ratio of disk to base of third finger (3FDW/3FDbW median 1.0 vs. 1.2); from L. batulawensis sp. nov. by narrower disk of third finger (R3FDW median 2.0%SVL vs. 2.5%SVL), disk of fourth toe (R4TDW median 2.5%SVL vs. 3.8%SVL), base of fourth toe disk (R4TDbW median 2.0%SVL vs. 2.9%SVL), and smaller ratio of disk to base of third finger (3FDW/3FDbW median 1.0 vs. 1.2); and from L. paulyambuni sp. nov. by narrower disk of fourth toe (R4TDW median 2.5%SVL vs. 3.6%SVL).
Range
Sarawak. Kuching Division, Kuching District, Gunung Serapi, Kubah NP, Matang 165 m asl; Bako NP, 66 m asl; Gunung Santubong, 60 m asl. Kuching Division, Lundu District, Gunung Gading NP, 50 m asl; Samunsam, 50 m asl. Serian Division, Serian District, Serian, 64 m asl. Sri Aman Division, Lubok Antu District, Lanjak Entimau, 350 m asl.
Not endemic to Sarawak, but also found on Serasan Is., Natuna Is., Indonesia (Herlambang et al., 2022).
Natural history
Other than with L. conspicillatus, L. lanjakensis sp. nov. and L. abanghamidi sp. nov., L. kong is also syntopic with ecologically quite differefnt L. cintalubang at Serian.
6. Limnonectes mocquardi Matsui, Dubois et Ohler, 2013
[English name: Kinabalu Fanged Frog]
Fig. 5C, D
Rana paradoxa Mocquard, 1890, 148.
Rana kuhlii (part) Boulenger, 1891, 342.
Rana kuhli (part) Inger, 1966, 196.
Limnonectes mocquardi Matsui, Dubois, and Ohler, 2013, 187.
Limnonectes sp. Lineage 9 Matsui et al., 2016, 308.
Lectotype
MNHNP 1889.222. an adult male from Kina Balu, State of Sabah.
Paralectotypes
MNHNP 1889.223, 224, 1889.245, 246; BMNH 1947.2.3.66. Locality probably same as the holotype.
Referred specimens
Sabah. SP 21356 from Bukit Ular, Kinabalu NP, 1700m asl. BOR 22796 on 5 August 2005 from Liwagu, Kinabalu NP, 1450 m asl. SP 21418 from Mesilau, Kinabalu NP, 1950 m asl. BOR 22674 on 30 July 2005, SP 21464–21468 Park Head Quarters, Kinabalu NP, 1600 m asl. BOR 22776 on 4 August 2005 from Power Station, Kinabalu NP, 1900 m asl. SP 21354 from Bukit Ural Trail, Kinabalu NP. KUHE 36788, 36789, 36790, 36791, 36792, 36793, 36794 on 5–8 August 1983, BOR 22645, SP 21062 (former BOR 22646), SP 21063 (former BOR 22678), SP 21064 (former BOR 22679) on 28 July 2005, BOR 22720, SP 21065 (former BOR 22721) on 31 July 2005, SP 21482 from Silau Silau, Kinabalu, 1450 m asl. SP 21603 from Tambunan, 750 m asl. BOR 12888, 12889 collected on 21 August 2003 from Kimanis, Trail 5, Crocker NP, 800 m asl. BOR 08094 on 28 August, BOR 08129, 08130 on 29 August 2002, BOR 23451 on 19 August 2005, from Kimanis, Trail 10–11, Crocker NP, 1300–1350 m asl. BOR 23450 on 19 August 2005 from Kimanis, Trail 11, Crocker NP, 1427 m asl. BOR 12639 on 9 August 2003 from Mahua, Crocker, 1200 m asl. BOR 09252 on 2 August 2004 from Tawau, more than 500 m asl.
Sarawak. KUHE 54503 on 25 February 2012, KUHE 55953 on 26 February 2015, from Camp 2, Mulu NP, 1358 m asl.; KUHE 55616, 55617, 55618, 55623 on 6 March 2013, KUHE 55836 on 22 August 2015, KUHE 55907 on 23 August 2015, KUHE 55931, 55932 on 24 August 2015, from Tapin, Mulu NP, 1600 m asl.
Etymology
The specific epithet mocquardi is dedicated to Dr. François Mocquard of the Muséum national d' histoire naturelle Paris, who described numerous herpetological taxa from not only Borneo but also Madagascar, Tonkin, Mexico, and Central America.
Diagnosis
The species can be differentiated from its relatives by the combination of first finger equal to or slightly longer than second; edges of second and third fingers with broad, non-moveable dermal fringes; outer webbing slightly, and inner one greatly excised on fourth toe (Fig. 12F). A large-sized species with adult mean SVL 65 mm in males and 63 mm in females; head long; forelimb short; hindlimb medium; tibia long; dorsal skin weakly folded, with networks of wrinkles; wrinkles very weak on head; tibia dorsally coarsely scattered with small, low warts (Fig. 11F); tip of third finger forming moderate-sized disk width slightly wider than basal phalanx (Fig. 10F); tip of fourth toe swollen into moderate-sized disk, width much wider than basal phalanx; fourth toe disk much wider than third finger disk; fourth toe webbed to disk, but narrowly distal to distal subarticular tubercle; dorsum brown without darker marking except for dark brown interorbital and continuing parietal, and discontinuous dorsolateral markings.
Description of a male topotype (BOR 22776 from Kinabalu NP. measurements in mm)
Snout-vent length (SVL) 89.0; habitus stocky; head enlarged and long, longer (HL 49.5, 55.6%SVL) than broad (HW 46.2, 51.9% SVL); snout obtusely pointed, rounded in profile, projecting beyond lower jaw; eye length (EL 12.2, 13.7%SVL) much smaller than snout length (SL 16.4, 18.4%SVL); canthus rounded; lore slightly sloping, concave; nostril dorsolateral, below canthus, slightly closer to snout than to eye; internarial distance (IND 7.2, 8.1%SVL) narrower than interorbital distance (IOD 9.1, 10.2%SVL), latter much wider than upper eyelid (UEW 5.2, 5.8%SVL); tympanum not visible; lower jaw with a pair of sharply pointed tooth-like projections (odontoid processes) near symphysis, more than twice the depth of mandible at base of projections; vocal sac and vocal slits absent.
Forelimb thick, short (FLL 48.5, 54.5%SVL; LAHL 38.0, 42.7%SVL); fingers moderately slender; first finger slightly longer than second; length of first, measured from distal edge of inner palmar tubercle (1FL 12.3, 13.8%SVL) nearly as long as length of eye; tips of fingers slightly swollen, forming moderate-sized disks without circummarginal grooves; disk width of third finger (3FDW 2.1, 2.4%SVL) slightly wider than basal phalanx; remnant of webs between fingers; inner metacarpal tubercle moderate (IMCL 4.9, 5.5%SVL) oval, elevated; middle metacarpal tubercle elongate, larger than and not contacting inner metacarpal tubercle; outer metacarpal tubercle elongate, smaller than inner metacarpal tubercle; proximal subarticular tubercles oval and elevated; distal subarticular tubercles low, but distinct; no supernumerary metacarpal tubercles; edges of second and third fingers with broad, non-moveable dermal fringes.
Hindlimb thick, medium-sized (HLL 132.8, 149.2%SVL) less than three times length of forelimb; tibia long (TL 43.2, 48.5%SVL), heels not overlapping when limbs are held at right angles to body; tibiotarsal articulation of adpressed limb reaching to center of eye; foot (FL 43.6, 49.0%SVL) slightly longer than tibia; tips of toes swollen into moderate-sized disks, disk width of fourth toe (4TDW 3.0, 3.4%SVL) much wider than basal phalanx and 3FDW; outer webbing slightly, and inner one greatly excised on fourth toe; fourth toe webbed to disk, but narrowly distal to distal subarticular tubercle; a flap of skin along outer edge of fifth toe freely movable; subarticular tubercles oval and distinct; an elongate inner metatarsal, length (IMTL 6.8, 7.6%SVL) more than half length of first toe (1TOEL 11.8, 13.3%SVL); no outer metatarsal tubercle.
Dorsal skin weakly folded, with networks of wrinkles; wrinkles weak on head; weak transverse fold between inner margins of upper eyelids; temporal fold from eye to above insertion of upper arm; warts around anus fine; side of trunk reticulated with fine wrinkles; dorsal surface of tibia coarsely scattered with small, low warts; tarsus with a thick dermal ridge extending proximally from metatarsal tubercle; throat and chest with weak wrinkles; abdomen smooth; distinct yellow-brownish tinge, but without asperities, forming a nuptial pad covering medial surface of first finger from its base to level of subarticular tubercle.
Color
In preservative, dorsum brown with a cream-colored mid-dorsal stripe, and without darker marking except for dark brown interorbital and continuing parietal, and discontinuous dorsolateral markings; a cream bar anterior to interorbital bar: a wide, oblique dark brown temporal stripe on and along supratympanic fold from behind eye to above arm insertion; side of head below canthus and supratympanic fold light brown dusted with dark brown, and dark brown bars on upper and lower lips unclear; lateral side of trunk lighter than dorsum; throat cream slightly dusted with light brown; chest to abdomen cream; ventral side of limbs cream, peripherally dotted with brown.
Variation
Neither SVL nor the ratio to SVL differed between the sexes (Table 1).
Snout may be slightly pointed or very slightly pointed, and truncate in profile; some with slightly visible tympanum; first finger may be longer than or similar to second in length; fourth toe web fairly excised in inner and outer sides, fairly well in outer side, or slightly in inner and outer sides; dorsum may with few warts, or scattered with small warts; sometimes with evident warts laterally; weak or strong dorsolateral ridge may be present anteriorly; side of trunk may be covered with fine warts; tibia may be dorsally nearly smooth, few small warts distally, distally small warts with white tip, or small warts forming row of ridges.
Dorsum brown with irregular large darker marking, uniformly clay brown, or yellow brown with several irregular large, darker marking; usually, cream middorsal stripe may be absent (Matsui, 1979); canthus rostralis totally or partly dark brown; head light colored posterior to eye or below canthus; upper lip bar may be clear and wide, or absent; lower lip bar may be clear and wide or weak; throat may be spotted with brown; chest may be moderately or weakly spotted with brown; abdomen may be with brown spots; dark bars on limb faint, evident or very faint; ventral side of thigh moderately or weakly dusted with brown spots; ventral side of tibia moderately or weakly mottled with light brown; dark mark on inner side of upper arm only distally or totally.
Eggs and tadpoles
Matsui (1979) reported that females collected from Headquarters in March and August had large ova with pigmented hemisphere. Morphology of tadpoles (Matsui, 1979) well agrees with the previous description of the species (Inger, 1966).
Comparisons
Sympatric with L. barioensis sp. nov. in Mahua and Tambunan, L. separatus sp. nov. in CRP and KNP, and L. paulyambuni sp. nov. in Mahua. The uncorrected pairwise sequence divergences for fragments (445 bp of 16S rRNA) between L. mocquardi and the co-occurring L. barioensis, L. separatus sp. nov., and L. paulyambuni sp. nov. are 5.5–8.0, 3.3–4.5, and 5.5–7.0%, respectively (Matsui et al., 2016).
Morphometrically, L. mocquardi differs from L. lambirensis sp. nov. by larger ratios of disk to base of fourth toe (4TDW/4TDbW median 1.5 vs. 1.2); from L. penerisanensis sp. nov. by narrower disk of third finger (R3FDW median 2.1% vs. 2.6%); from L. lanjakensis sp. nov. by narrower disk of fourth toe (R4TDW median 2.9% vs. 3.7%); from L. batulawensis sp. nov. by shorter thigh (RTHIGHL median 49.3% vs. 55.1%) in females, and by smaller ratios of base of fourth toe disk (R4TDbW median 1.9% vs. 2.9%); and from L. paulyambuni sp. nov. by shorter thigh (RTHIGHL median 49.3% vs. 55.2%) in females.
Range
Sabah. West Coast Division, Ranau District, KNP, Liwagu, 1450 m asl; Silau Silau, 1450 m asl; PHQ, 1600 m asl; Bukit Ular, 1700 m asl; Power Station, 1900 m asl; Mesilau, 1950 m asl. West Coast Division, Papar District, CRC, Kimanis, Trail 5, 800 m asl. Tawau Division, Tawau District, Tawau, >500 m asl. Interior Division, Keningau District, CRC, Trail 10–11, 1100 m asl, Trail 11, 1427 m asl. Interior Division, Tambunan District, Tambunan, 750 m asl; Mahua, 1200 m asl.
Sarawak. Miri Division, Marudi District, Gunung Mulu NP, Camp 3, 1358 m asl; Tapin, 1600 m asl.
Natural history
According to Matsui (1979), females collected from Headquarters in March and August had large ova and the active breeding season is supposed to last long. Around Headquarters, two distinct size groups of tadpoles and metamorphosing young were seen in mid March. These larvae were found in ditches along roads in logged forest or in the places where small streams form small pools (WT 16.5°C). They hid themselves by day under submerged stones. In the shaded pools, kuhli tadpoles were seen with larvae of Leptobrachium montanum. Metamorphosing frogs were seen hopping by day in ditches or near small streams. Transformed larger frogs were found under stones and logs immediate vicinity of water (WT 17.5°C) and some were found at night hopping on mossy banks.
Males were calling in a ditch densely covered by grasses at Kundasan on 3 August 1983 at 21:35 h at the ground and water temperature of 18.5°C and 19.0°C, respectively. Several gravid females were found passing the road near the place. Callings were also heard in December at the HQ of KNP.
7. Limnonectes penerisanensis Matsui, Nishikawa et Shimada sp. nov.
[English name: Penrissen Fanged Frog]
Fig. 6A, B
Limnonectes sp. Lineage 10 Matsui et al., 2016, 308.
Holotype
SFC-GRB-00604 (former KUHE 54427) an adult male from Batu Panggah, Gunung Penrissen, Padawan, Kuching District, Sarawak (01°07′21″ N, 110°13′43″ E, 1035 m asl), collected on 19 February 2012 by K. Nishikawa and M. Matsui.
Paratypes
Sarawak. SFC-GRB-00605 (former KUHE 53915) a juvenile collected on 2 September 2010, SFC-GRB-00606 (former KUHE 54424) an adult female on 19 February 2012, SFC-GRB-00607 (former KUHE 54467) an adult male on 21 February 2012, all from the type locality.
Referred specimens
Sarawak. KUHE 48541, 48547 collected on 20 December 2013 by M. Matsui, K. Nishikawa, and T. Shimada, KUHE 55638, 55641 on 12 March 2013, all from the type locality.
Etymology
The specific epithet penerisanensis is derived from Gunung (=Mt.) Penerisan, another name of Gunung Penrissen, located at the Indonesian border of Sarawak, where this species occurs.
Diagnosis
The new species can be differentiated from its relatives by the combination of tibia dorsally with ridges of wrinkles, and small, low warts restricted to distal region (Fig. 11G); first finger longer than second; tip of third finger forming large disk width wider than basal phalanx (Fig. 10G); tip of fourth toe swollen into large disk much wider than basal phalanx; fourth toe broadly webbed to disk. A large-sized species with adult mean SVL 58 mm in males; head medium; forelimb short; hindlimb long; tibia long; dorsal skin with networks of wrinkles running in all directions, with fine warts only around anus; outer edge of second and third fingers with freely movable, narrow ridges of skin; fourth toe disk much wider than third finger disk; inner and outer webbing of fourth toe slightly excised (Fig. 12G); chest dark brown reticulated with cream; abdomen and ventral side of limbs cream, dusted with brown.
Description of holotype (measurements in mm)
Snout-vent length (SVL) 73.8; habitus stocky; head medium-sized, as long (HL 33.8, 45.8%SVL) as broad (HW 33.8, 45.8% SVL); snout slightly pointed, rounded in profile, projecting beyond lower jaw; eye length (EL 9.8, 13.3%SVL) smaller than snout length (SL 11.4, 15.5%SVL); canthus distinct; lore slightly sloping, concave; nostril dorsolateral, below canthus, slightly closer to snout than to eye; internarial distance (IND 7.1, 9.6%SVL) narrower than interorbital distance (IOD 7.8, 10.6%SVL), latter much wider than upper eyelid (UEW 5.8, 7.9%SVL); pineal spot visible; tympanum indistinct; lower jaw with a pair of sharply pointed tooth-like projections near symphysis, more than twice the depth of mandible at base of projections; vocal sac and vocal slits absent.
Forelimb short (FLL 41.4, 56.1%SVL; LAHL 32.8, 44.4%SVL); fingers moderately slender; first finger longer than second; length of first, measured from distal edge of inner palmar tubercle (1FL 9.1, 12.3%SVL) shorter than length of eye; tips of fingers slightly swollen, forming large disks without circummarginal grooves; disk width of third finger (3FDW 1.9, 2.6%SVL) wider than basal phalanx; remnant of webs between fingers; inner metacarpal tubercle moderate (IMCL 3.6, 4.9%SVL) oval, elevated; middle metacarpal tubercle oval, as large as and not contacting inner metacarpal tubercle; outer metacarpal tubercle elongate, smaller than inner metacarpal tubercle; proximal subarticular tubercles oval and elevated; distal subarticular tubercles low, but distinct; no supernumerary metacarpal tubercles; outer edge of second and third fingers with freely movable, narrow ridges of skin; other finger edges with not freely movable dermal fringes.
Hindlimb thick, long (HLL 114.5, 155.1%SVL) less than three times length of forelimb; tibia long (TL 36.0, 48.8%SVL), heels not overlapping when limbs are held at right angles to body; tibiotarsal articulation of adpressed limb reaching to center of eye; foot (FL 37.1, 50.3%SVL) slightly longer than tibia; tips of toes swollen into large disks, disk width of fourth toe (4TDW 2.7, 3.7%SVL) much wider than basal phalanx and 3FDW; inner and outer webbing of fourth toe slightly excised; fourth toe broadly webbed to disk; a flap of skin along outer edge of fifth toe freely movable; subarticular tubercles oval and distinct; an elongate inner metatarsal, length (IMTL 5.7, 7.7%SVL) more than half length of first toe (1TOEL 9.2, 12.5%SVL); no outer metatarsal tubercle.
Dorsal skin with networks of wrinkles running in all directions, with fine warts only around anus; weak wrinkles on eyelid, and top of snout; weak transverse fold between inner margins of upper eyelids; temporal fold from eye to above insertion of upper arm; side of trunk reticulated with fine wrinkles; throat covered with networks of weak wrinkles; chest, and abdomen smooth; anus with few, fine warts; dorsal surface of tibia with ridges of wrinkles, and small, low warts restricted to distal region; tarsus with a thick dermal ridge extending proximally from metatarsal tubercle; distinct brownish tinge, but without asperities, forming a nuptial pad covering medial surface of first finger from its base to level of subarticular tubercle.
Color
In preservative, dorsum reddish brown without darker marking except for dark brown markings on interorbital; a narrow oblique dark brown supratympanic stripe from behind eye to above arm insertion; side of head without pale marking; brown color of lateral side of trunk gradually fading towards ventrum; upper and lower lips without marking; throat and chest dark brown reticulated with cream; abdomen and ventral side of limbs cream, dusted with brown; limbs with faint, dark crossbars dorsally; ventral side of lower arm dusted with dark brown.
Variation
Due to small sample size, sexual dimorphism could not be examined.
First finger may be same as second in length; outer and inner edges of third finger or outer and inner edges of second and third fingers may be with freely movable flap of skin; webbing of fourth toe may be slightly incised on inner side or little incised on both sides; warts may be present on dorsum posterolaterally; tibia may be with small warts scattered mainly distally.
Dorsum may be clay brown heavily mottled with dark brown; dorsum may have irregular dark blotches or dorsolateral marking anteriorly; dark interorbital bar may be preceded by light colored bar; canthus rostralis may be dark brown; supratympanic stripe may be moderately wide or absent; upper lip bar may be indistinct, and lower lip bar may be distinct; throat may be slightly dusted with brown or heavily mottled with brown; chest may be cream slightly dusted with brown; abdomen cream, coarsely spotted anteriorly or slightly dusted with brown; ventral side of limbs may be spotted with brown.
Comparisons
Limnonectes penerisanensis sp. nov. is sympatric with L. conspicillatus on Gunung Penrissen, but has wider digital disks as shown below. The uncorrected pairwise sequence divergence for fragments (445 bp of 16S rRNA) between the two species is 7.8–8.0% (Matsui et al., 2016).
Limnonectes penerisanensis sp. nov. differs from L. tawauensis sp. nov. by longer inner metatarsal tubercle (RIMTL median 8.4%SVL vs. 7.2%SVL) in males, wider disk of third finger (R3FDW median 2.6%SVL vs. 1.8%SVL), of fourth toe (R4TDW median 3.6%SVL vs. 2.3%SVL), and larger ratio of disk to base of third finger (3FDW/3FDbW median 1.3 vs. 1.0); from L. barioensis sp. nov. by wider disk of third finger (R3FDW median 2.6%SVL vs. 1.8%SVL) and larger ratio of disk to base of third finger (3FDW/3FDbW median 1.3 vs. 1.0); from L. conspicillatus by wider disk of third finger (R3FDW median 2.6%SVL vs. 2.0%SVL), of fourth toe (R4TDW median 3.6%SVL vs. 2.7%SVL), and larger ratio of disk to base of third finger (3FDW/3FDbW median 1.3 vs. 1.0); from L. lambirensis sp. nov. by wider disk of third finger (R3FDW median 2.6%SVL vs. 2.1%SVL) and fourth toe (R4TDW median 3.6%SVL vs. 2.5%SVL), and larger ratios of disk to base of third finger (3FDW/3FDbW median 1.3 vs. 1.0); from L. kong by longer first toe (R1TOEL median 15.0%SVL vs. 12.0%SVL) in males, wider disk of third finger (R3FDW median 2.6%SVL vs. 2.0%SVL), of fourth toe (R4TDW median 3.6%SVL vs. 2.5%SVL), and larger ratio of disk to base of third finger (3FDW/3FDbW median 1.3 vs. 1.2); from L. separatus sp. nov. by longer first toe (R1TOEL median 15.0%SVL vs. 13.3%SVL), tibia (RTL median 50.6%SVL vs. 47.8%SVL), and foot (RFL median 51.6%SVL vs. 47.2%SVL) in males; from L. lanjakensis sp. nov. by longer foot (RFL median 51.6%SVL vs. 49.4%SVL) and first toe (R1TOEL median 15.0%SVL vs. 13.4%SVL), and shorter forelimb (RFLL median 56.9%SVL vs. 60.5%SVL) in males.
Range
Endemic to Sarawak. Kuching Division, Kuching District, Padawan Subdistrict, Gunung Penrissen, 1035 m asl.
Fig. 6.
Dorsal (A, C) and ventral (B, D) views of male holotypes of Limnonectes penerisanensis sp. nov. (SFC-GRB-00604 [=former KUHE 54427], A, B) and L. paginatanensis sp. nov. (BOR 22492, C, D). Scale bar=10 mm.
8. Limnonectes paginatanensis Matsui, Nishikawa et Shimada sp. nov.
[English name: Paginatan Fanged Frog]
Fig. 6C, D
Limnonectes sp. Lineage 11 Matsui et al., 2016, 308.
Holotype
BOR 22492, an adult male from Paginatan, between Ranau and Telupid, Sabah (5°46′N, 116°49′E, 120 m asl), collected on 17 March 2005 by T. Shimada.
Paratypes
Sabah. BOR 22488, 22491, 22493, 22494, 22496 data same as the holotype.
Referred specimens
Sabah. BOR 22799 from Sg. Kipungit 1, 22801, 22807, SP 21069 (former BOR 22802) from Sg. Kipungit 2, BOR 22804 from near Poring Hot Spring, KNP (06°02′ N, 116°42′ E, 400 m asl), collected on 7 August 2005 by Matsui, Nishikawa, Shimada, and Yambun. SP 01553, 01555, 01556, 01557, 01564 collected in July 1995 from Poring by Zoology Unit, Sabah Parks.
Etymology
The specific epithet paginatanensis is derived from the village of Paginatan, Sabah, where the new species was collected.
Diagnosis
The new species can be differentiated from its relatives by the combination of dorsal skin extremely folded, with networks of wrinkles running in all directions, scattered with warts posterior to sacrum; tibia dorsally coarsely scattered with small warts with white tips (Fig. 11H); first finger slightly longer than second; tip of third finger forming large disk width slightly wider than basal phalanges (Fig. 10H); tip of fourth toe swollen into large disk much wider than basal phalanx; fourth toe broadly webbed to disk. A medium-sized species with adult mean SVL 55 mm in males and 56 mm in females; head short, forelimb and hindlimb medium; tibia short: outer edges of second and third finger with moveable dermal flaps; fourth toe disk much wider than third finger disk; inner and outer webbing of fourth toe slightly excised (Fig. 12H); dorsum dark brown without marking, throat and chest brown reticulated with cream.
Description of holotype (measurements in mm)
Snout-vent length (SVL) 56.0; habitus moderately stocky; head enlarged and short, slightly shorter (HL 24.7, 44.1%SVL) than broad (HW 25.4, 45.4% SVL); snout slightly pointed dorsally and laterally, projecting beyond lower jaw; eye length (EL 7.3, 13.0%SVL) slightly smaller than snout length (SL 7.8, 3.9%SVL); canthus distinct; lore slightly sloping, concave; nostril dorsolateral, below canthus, midway between snout and eye; internarial distance (IND 4.5, 8.0%SVL) narrower than interorbital distance (IOD 6.1, 10.9%SVL), latter wider than upper eyelid (UEW 3.9, 7.0%SVL); pineal spot visible; tympanum not visible; lower jaw with a pair of sharply pointed tooth-like projections near symphysis, more than twice the depth of mandible at base of projections; vocal sac and vocal slits absent.
Forelimb medium-sized (FLL 30.8, 55.0%SVL; LAHL 25.5, 45.5%SVL); fingers slender; first finger slightly longer than second; length of first, measured from distal edge of inner metacarpal tubercle (1FL 7.1, 12.7%SVL) slightly shorter than length of eye; tips of fingers slightly swollen, forming large disks without circummarginal grooves, disk width of third finger (3FDW 1.3, 2.2%SVL) slightly wider than basal phalanx; remnant of webs between fingers; inner metacarpal tubercle moderate (IMCL 3.1, 5.5%SVL) oval, slightly elevated; middle metacarpal tubercle oval, smaller than and not contacting inner metacarpal tubercle; outer metacarpal tubercle elongate, larger than inner metacarpal tubercle; proximal subarticular tubercles oval and elevated; distal subarticular tubercles low, but distinct; no supernumerary metacarpal tubercles; outer edges of second and third finger with moveable dermal flaps, inner edges with non-moveable dermal fringes.
Hindlimb medium-sized (HLL 84.9, 151.6%SVL) less than three times length of forelimb; tibia short (TL 26.7, 47.7%SVL), heels not overlapping when limbs are held at right angles to body; tibiotarsal articulation of adpressed limb reaching to center of eye; foot (FL 27.2, 48.6%SVL) slightly longer than tibia; tips of toes swollen into large disks (disk width of fourth toe [4TDW] 1.6, 2.9%SVL) much wider than basal phalanx and 3FDW; inner and outer webbing of fourth toe slightly excised; fourth toe broadly webbed to disk; a flap of skin along outer edge of fifth toe freely movable; subarticular tubercles oval and distinct; an elongate inner metatarsal, length (IMTL 4.8, 8.6%SVL) more than half length of first toe (1TOEL 7.9, 14.1%SVL); no outer metatarsal tubercle.
Dorsal skin extremely folded, with networks of wrinkles running in all directions, although wrinkles weak on head, including eyelid and top of snout; dorsum scattered with warts posterior to sacrum; very weak transverse fold between inner margins of upper eyelids; temporal fold from eye to above insertion of upper arm; anus dorsally surrounded by fine warts; side of trunk reticulated with fine wrinkles; throat weakly wrinkled irregularly; chest, and abdomen smooth; dorsal surface of tibia coarsely scattered with small warts with white tips; tarsus with a thick dermal ridge extending proximally from metatarsal tubercle; distinct brownish tinge, but without asperities, forming a nuptial pad covering medial surface of first finger from its base to level of subarticular tubercle.
Color
In preservative, dorsum dark brown without darker marking, except for interorbital bar; a wide, oblique, dark brown supratympanic fold from behind eye to above arm insertion; side of head without paler marking; lateral side of trunk lighter than dorsum covered by reticulation of lighter colored wrinkles; upper and lower lips without marking; throat and chest brown reticulated with cream; abdomen cream; limbs without dark crossbars dorsally; ventral side of limbs mottled with brown; ventral side of lower arm distal half dusted with dark brown.
Variation
SVL did not differ between the sexes, and the ratio to SVL was sexually dimorphic in RHW (median 43.0%SVL in males larger than 38.8%SVL in females: Table 1).
Snout pointed or slightly pointed; snout laterally pointed or truncate; in some, tympanum visible; anus may be slightly surrounded by warts; first and second fingers may be nearly same in length; outer webbing slightly, or webbing of both sides fairly well incised on fourth toe; dorsum may be totally scattered with warts from where wrinkles originating, or nearly smooth with very weak wrinkles; wrinkles on side of body may be with few warts; warts on tibia may be small anterodistally, and few in proximal half.
Head and body may be dorsally scattered with small dark spots; upper lip bar slightly clear or not clear; lower lip irregularly barred or not clear; throat may be mottled with brown spots; abdomen dotted, slightly dotted, or only laterally dotted with brown; ventral side of thigh dotted or slightly dotted with brown; tibia ventrally heavily spotted or only dusted with brown; ventral side of upper arm may be heavily spotted with dark brown in distal half or totally.
Comparisons
Limnonectes paginatanensis sp. nov. is sympatric with L. tawauensis sp. nov. in Paginatan and Poring, but is different in digital disks and tibial warts.
The uncorrected pairwise sequence divergence for fragments (445 bp of 16S rRNA) between L. paginatanensis sp. nov. and the co-occurring L. tawauensis sp. nov. is 7.8–8.3% (Matsui et al., 2016).
Limnonectes paginatanensis sp. nov. differs from L. tawauensis sp. nov. by wider disk of third finger (R3FDW median 2.7%SVL vs. 1.8%SVL) and fourth toe (R4TDW median 3.6%SVL vs. 2.3%SVL); from L. conspicillatus by wider upper eyelid (RUEW median 8.4%SVL vs. 7.3%SVL) in females, and by wider disk of fourth toe (R4TDW median 3.6%SVL vs. 2.7%SVL) and larger ratio of disk to base of third finger (3FDW/3FDbW median 1.2 vs. 1.0); from L. lambirensis sp. nov. by wider internarial (RIND median 8.5%SVL vs. 7.6%SVL) in females, and by wider disk of third finger (R3FDW median 2.7%SVL vs. 2.1%SVL) and of fourth toe (R4TDW median 3.6%SVL vs. 2.5%SVL), larger ratios of disk to base of third finger (3FDW/3FDbW median 1.2 vs. 1.0) and of disk to base of fourth toe (4TDW/4TDbW median 1.6 vs. 1.2); from L. kong by wider disk of third finger (R3FDW median 2.7%SVL vs. 2.0%SVL) and of fourth toe (R4TDW median 3.6%SVL vs. 2.5%SVL), and larger ratio of disk to base of third finger (3FDW/3FDbW median 1.2 vs. 1.0); from L. batulawensis sp. nov. by narrower head (RHW (median 38.8%SVL vs. 41.4%SVL), shorter thigh (RTHIGHL median 49.2%SVL vs. 55.1%SVL), and inner metatarsal tubercle (RIMTL median 6.8%SVL vs. 8.6%SVL) in females; from L. paulyambuni sp. nov. by shorter head (RHL median 40.4%SVL vs. 42.2%SVL) and thigh (RTHIGHL median 49.2%SVL vs. 55.2%SVL) in females.
Range
Endemic to Sabah. West Coast Division, Ranau District, Paginatan, 120 m asl; Poring, KNP, 400 m asl.
Fig. 7.
Dorsal (A, C) and ventral (B, D) views of holotype of female Limnonectes separatus sp. nov. (BOR 23415, A, B) and male L. lanjakensis sp. nov. (SFC-GRB-00608 [=former KUHE 17483], C, D). Scale bar=10 mm.
9. Limnonectes separatus Matsui, Nishikawa et Shimada sp. nov.
[English name: Separated Fanged Frog]
Fig. 7A, B
Limnonectes sp. Lineage 13 Matsui et al., 2016, 308.
Holotype
BOR 23415 an adult female from Trail 4 of UMS 2002 expedition to the Crocker Range (05°29′28″N, 116°00′49″E, 754 m asl), Ulu Kimanis, Papar, Sabah, collected on 18 August 2005 by M. Matsui, K. Nishikawa, T. Shimada and P. Yambun.
Paratypes
Sabah. BOR 23416, 23417, 23418 data same as the holotype. BOR 08805 from the type locality collected on 12 September 2002 by M. Matsui
Referred specimens
Sabah. BOR 08121 from Base Camp of UMS 2002 expedition to the Crocker Range (05°32′N, 116°00′E, 155 m asl), Ulu Kimanis, Papar collected on 28 August 2002. BOR 08176, 08177, 08413 from Trail 5 of UMS 2002 expedition to the Crocker Range (05°29′12″N, 116°00′50″E, 820 m asl), Ulu Kimanis, Papar on 1–2 September 2002. SP 21075 (former BOR 23406) from Crocker NP, Sg. Kilanpung, Tenom, 380 m asl on 17 August 2005. SP 21066 (former BOR 22722), SP 21067 (former BOR 22723) from Silau Silau, Kinabalu NP, 1450 m asl on 31 July 2005.
Sarawak. KUHE 55301–55303, 55325–55327 on 4 March 2013, and KUHE 48930–48933, 48935 on 2 March 2014 from Camp 1 of Gunung Mulu NP, Miri Division, 197 m asl, collected on 4 March 2013. KUHE 48960, 48961 from the point between HQ and Camp 1 of Gunung Mulu NP, collected on 3 March 2014. KUHE 55954 from Camp 2 of Gunung Mulu NP (04°02′31″N, 114°52′16″E, 509 m asl) collected on 26 August 2015.
Etymology
The specific epithet separatus refers to the disjunct distribution of the species in the mountain ranges of the Crocker in Sabah and Mulu in Sarawak
Diagnosis
The new species can be differentiated from its relatives by the combination of first finger slightly longer than second; both edges of second and third, and inner edge of fourth fingers with freely movable dermal fringes; tip of third finger forming large disk, width much wider than basal phalanx (Fig. 10I); inner and outer webbing of fourth toe shallowly excised (Fig. 12I). A medium-sized species with adult mean SVL 48 mm in males and 50 mm in females; head long; forelimb long; hindlimb short; tibia short; dorsal skin extremely folded, with networks of wrinkles running in all directions, and posteriorly scattered with small warts; wrinkles weak on eyelid, and top of snout; tibia dorsally coarsely scattered with small, conical warts (Fig. 11I); tip of fourth toe swollen into large disk, width much wider than basal phalanx; fourth toe disk wider than third finger disk; fourth toe broadly webbed to disk; dorsum dark brown without darker marking
Description of holotype (measurements in mm)
Snout-vent length (SVL) 51.4; habitus moderately stocky; head not enlarged and long, slightly longer (HL 22.2, 43.2%SVL) than broad (HW 21.0, 40.9% SVL); snout slightly rounded, rounded in profile, projecting beyond lower jaw; eye length (EL 8.4, 16.3%SVL) larger than snout length (SL 7.4, 14.4%SVL); canthus distinct; lore slightly sloping, concave; nostril dorsolateral, below canthus, slightly closer to snout than to eye; internarial distance (IND 4.3, 8.4%SVL) slightly narrower than interorbital distance (IOD 4.5, 8.8%SVL), latter wider than upper eyelid (UEW 3.3, 6.4%SVL); pineal spot visible; tympanum not visible; lower jaw with a pair of low projections near symphysis, about twice the depth of mandible at base of projections; vocal sac and vocal slits absent.
Forelimb long (FLL 30.9, 60.1%SVL; LAHL 24.3, 47.3%SVL); fingers moderately slender; first finger slightly longer than second; length of first, measured from distal edge of inner metacarpal tubercle (1FL 6.9, 13.4%SVL) shorter than length of eye; tips of fingers slightly swollen, forming large disks without circummarginal grooves; disk width of third finger (3FDW 1.4, 2.7%SVL) much wider than basal phalanx; remnant of webs between fingers; inner metacarpal tubercle moderate (IMCL 2.7, 5.3%SVL) oval, only slightly elevated; middle metacarpal tubercle flat, as large as and not contacting inner metacarpal tubercle; outer metacarpal tubercle indistinct, smaller than inner metacarpal tubercle; proximal subarticular tubercles oval and elevated; distal subarticular tubercles low, but distinct; no supernumerary metacarpal tubercles; both edges of second and third, and inner edge of fourth fingers with freely movable dermal fringes; other finger edges with narrow ridges of skin.
Hindlimb thick, short (HLL 78.6, 152.9%SVL) less than three times length of forelimb; tibia short (TL 24.1, 46.9%SVL), heels not overlapping when limbs are held at right angles to body; tibiotarsal articulation of adpressed limb reaching to center of eye; foot (FL 23.8, 46.3%SVL) slightly shorter than tibia; tips of toes swollen into large disks, disk width of fourth toe (4TDW 1.7, 3.3%SVL) much wider than basal phalanx; inner and outer webbing of fourth toe shallowly excised; fourth toe broadly webbed to disk; a flap of skin along outer edge of fifth toe freely movable; subarticular tubercles oval and distinct; an elongate inner metatarsal, length (IMTL 3.9, 7.6%SVL) more than half length of first toe (1TOEL 6.4, 12.5%SVL); no outer metatarsal tubercle.
Dorsal skin extremely folded, with networks of wrinkles running in all directions, and posteriorly scattered with small warts; wrinkles weak on eyelid, and top of snout; very weak transverse fold between middle of eyelids; low temporal fold from eye to above insertion of upper arm; warts around anus fine; side of trunk covered with small warts; dorsal surface of tibia and tarsus coarsely scattered with small, conical warts; tarsus with a thick dermal ridge extending proximally from metatarsal tubercle (Fig. 10I); throat coarsely covered with longitudinal wrinkles; chest, and abdomen smooth.
Color
In preservative, dorsum dark brown with a cream-colored mid-dorsal stripe, and without darker marking; interorbital bar dark brown, with anterior light bar; a moderately wide, oblique dark brown temporal stripe on and along supratympanic fold from behind eye to above arm insertion; side of head from behind eye to inguinal area paler brown; lateral side of trunk coarsely spotted brown; upper and lower lips with vague dark bars; limbs with faint dark crossbars dorsally; throat and chest cream irregularly mottled with light brown; abdomen cream; ventral side of limbs cream, spotted with brown on posterior thigh; ventral side of lower arm dusted with dark brown.
Variation
SVL did not differ between the sexes, but the ratio to SVL was sexually dimorphic in RHW (median 43.6%SVL in males larger than 39.5%SVL in females: Table 1).
Snout pointed or slightly pointed; dorsum may be scattered with warts from wrinkles; wrinkles on throat may be weak; tibia may have a few ridges and a few small warts or small and minute warts; movable dermal fringes may be on outer edge of second and third, or outer edge of third finger; incision of web on fourth toe slight or fairly strong on inner and outer sides, or slightly on inner and fairly strong on outerside; anus dorsally with fine warts or with very few warts.
Dorsum may be brown or yellow brown with irregular darker marking; upper lip bar absent or obscure; lower lip bar may be clear or unclear; throat may be heavily mottled or spotted with dark brown; abdomen may be slightly mottled dark.
Comparisons
Limnonectes separatus sp. nov. is sympatric with L. tawauensis sp. nov. at low to moderate elevations of Crocker RP, L. mocquardi at moderate elevations of Crocker RP and KNP, and L. batulawensis sp. nov. at moderate elevations of Mulu NP, and the uncorrected pairwise sequence divergences for fragments (445 bp of 16S rRNA) between L. separatus sp. nov. and the co-occurring L. tawauensis sp. nov., L. mocquardi, and L. batulawensis sp. nov. are 6.8–7.3, 3.3–4.5, and 3.3–3.5%, respectively (Matsui et al., 2016).
Limnonectes separatus sp. nov. differs from L. tawauensis sp. nov. by shorter first finger (R1FL median 13.1%SVL vs. 14.2%SVL) in males; from L. lambirensis sp. nov. by wider internarial (RIND median 8.4%SVLvs. 7.6%SVL) in females, and by larger ratios of disk to base of third finger (3FDW/3FDbW median 1.2 vs. 1.0) and of disk to base of fourth toe (4TDW/4TDbW median 1.4 vs. 1.2); from L. kong by larger ratio of disk to base of third finger (3FDW/3FDbW median 1.2 vs. 1.0); from L. penerisanensis sp. nov. by shorter foot (RFL median 47.2%SVL vs. 51.6%SVL), first toe (R1TOEL median 13.3%SVL vs. 15.0%SVL), and tibia (RTL median 47.8%SVL vs. 50.8%SVL) in males; from L. lanjakensis sp. nov. by longer inner metacarpal tubercle (RIMCL median 5.2%SVL vs. 5.1%SVL) in males; from L. batulawensis sp. nov. by narrower base of fourth toe disk (R4TDbW median 2.4%SVL vs. 3.8%SVL); and from L. paulyambuni sp. nov. by shorter thigh (RTHIGHL median 51.0%SVL vs. 52.4%SVL) in males.
Range
Sabah. West Coast Division, Papar District, CRP, Base Camp, 133 m asl; Kilanpung, 380 m asl; Kimanis, Trail 4, 754 m asl; Kimanis, Trail 5, 800 m asl. West Coast Division, Ranau District, Kinabalu NP, Silau Silau, 1450 m asl.
Sarawak. Miri Division, Marudi District, Gunung Mulu NP, Camp 1, 197 m asl; Camp 2, 509 m asl.
10. Limnonectes lanjakensis Matsui et Nishikawa sp. nov.
[English name: Labang's Fanged Frog]
Fig. 7C, D
Limnonectes sp. Lineage 14 Matsui et al., 2016, 308.
Holotype
SFC-GRB-00608 (former KUHE17483, an adult male from Sungai Jelak, a branch of Sungai Engkari, Bukit Lanjak, Sri Aman Division, Sarawak (01°20′N, 112°00′E, 250 m asl), collected on 25 August 1993 by M. Matsui.
Paratype
Sarawak. SFC-GRB-00609 (former KUHE 17443), an adult female collected on 28 August 1993 from the type locality collected by David Labang.
Referred specimens:
Sarawak. KUHE 10578 collected on 16 January 1990 from Sungai Bloh, Song (01°38′N, 112°20′E). KUHE 42571, 42572, 42573 from Kanowit (02°01′35″ N, 112°08′27″ E, 31 m alt), Sarawak, collected on 21 November 2008 by K. Nishikawa and D. Belabut.
Etymology
The specific epithet lanjakensis is derived from Bukit Lanjak in the Lanjak Entimau Wildlife Sanctuary in southern Sarawak, where this species was found.
Diagnosis
The new species can be differentiated from its relatives by the combination of first finger as long as or shorter than second; outer edges of second and third fingers with freely movable ridges of skin; inner and outer webbing of fourth toe moderately excised (Fig. 12J). A medium-sized species with adult mean SVL 53 mm in males and 52 mm in females; head long, forelimb, hindlimb and tibia long; dorsal skin extremely folded, with networks of wrinkles originating small warts and running in all directions; wrinkles very weak on head; tibia dorsally coarsely scattered with small, low warts (Fig. 11J); tip of third finger forming large disk, width much wider than basal phalanx (Fig. 10J); tip of fourth toe swollen into large disk width much wider than basal phalanx; fourth toe disk much wider than third finger disk; fourth toe broadly webbed to disk; dorsum light brown with dark brown markings on interorbital, upper eyelid, and canthus.
Description of holotype (measurements in mm)
Snout-vent length (SVL) 53.0; habitus stocky; head enlarged, elevated and long, as long (HL 34.8, 65.7%SVL) as broad (HW 34.7, 65.5% SVL); snout slightly pointed, truncate in profile, projecting beyond lower jaw; eye length (EL 7.3, 13.8%SVL) smaller than snout length (SL 7.6, 14.8%SVL); canthus distinct; lore slightly sloping, concave; nostril dorsolateral, below canthus, slightly closer to snout than to eye; internarial distance (IND 5.1, 9.6%SVL) wider than interorbital distance (IOD 4.8, 9.1%SVL), latter wider than upper eyelid (UEW 3.7, 7.0%SVL); pineal spot visible; tympanum not visible; lower jaw with a pair of sharply pointed tooth-like projections near symphysis, more than twice the depth of mandible at base of projections; vocal sac and vocal slits absent.
Forelimb long (FLL 32.0, 60.0%SVL; LAHL 24.8, 46.8%SVL); fingers moderately slender; first finger as long as second; length of first, measured from distal edge of inner metacarpal tubercle (1FL 6.7, 12.6%SVL) shorter than length of eye; tips of fingers slightly swollen, forming large disks without circummarginal grooves; disk width of third finger (3FDW 1.3, 2.4%SVL) much wider than basal phalanx; remnant of webs between fingers; inner metacarpal tubercle moderate (IMCL 2.7, 5.1%SVL) oval, slightly elevated; middle metacarpal tubercle oval, smaller than and not contacting inner metacarpal tubercle; outer metacarpal tubercle elongate, as large as inner palmar tubercle; proximal subarticular tubercles oval and elevated; distal subarticular tubercles low, but distinct; no supernumerary metacarpal tubercles; outer edges of second and third fingers with freely movable ridges of skin; other finger edges with not freely movable dermal fringes.
Hindlimb long (HLL 83.1, 156.8%SVL) less than three times length of forelimb; tibia long (TL 26.6, 50.2%SVL), heels not overlapping when limbs are held at right angles to body; tibiotarsal articulation of adpressed limb reaching to center of eye; foot (FL 26.2, 49.4%SVL) slightly shorter than tibia; tips of toes swollen into large disks, disk width of fourth toe (4TDW 1.7, 3.2%SVL) much wider than basal phalanx; inner and outer webbing of fourth toe moderately excised; fourth toe broadly webbed to disk; a flap of skin along outer edge of fifth toe freely movable; subarticular tubercles oval and distinct; an elongate inner metatarsal, length (IMTL 4.8, 9.1%SVL) more than half length of first toe (1TOEL 7.3, 13.8%SVL); no outer metatarsal tubercle.
Dorsal skin extremely folded, with networks of wrinkles originating small warts and running in all directions; wrinkles very weak on head; weak transverse groove between upper eyelids; temporal fold from eye to above insertion of upper arm; dorsal surface of tibia coarsely scattered with small, low warts; tarsus with a thick dermal ridge extending proximally from metatarsal tubercle; throat covered with weak wrinkles; chest, and abdomen smooth; distinct yellow-brownish tinge, but without asperities, forming a nuptial pad covering medial surface of first finger from its base to level of subarticular tubercle.
Color
In preservative, dorsum light brown without darker marking except for dark brown markings on interorbital, upper eyelid, and canthus rostralis; a narrow oblique dark brown supratympanic stripe from behind eye to above arm insertion; side of head paler than dorsum, but dusted with brown; upper lip with large dark brown bars; bars on lower lip indistinct; throat cream irregularly mottled with light brown; chest to abdomen cream; limbs with faint brown crossbars dorsally; ventral side of thigh cream, spotted laterally; ventral side of tibia cream, laterally faintly spotted with light brown; ventral side of lower arm dark brown.
Variation
SVL did not differ between the sexes, but the ratio to SVL was sexually dimorphic in RSL (median 15.9%SVL in males vs. 14.2%SVL in females), RLAHL (median 46.5%SVL in males vs. 43.6%SVL in females), RFLL (median 60.5%SVL in males vs. 56.2%SVL in females), RTL (median 49.8%SVL in males vs, 45.6%SVL in females), RFL (median 49.4%SVL in males vs. 43.9%SVL in females), RHLL (median 159.5%SVL in males vs. 146.1%SVL in females), and RIMTL (median 8.3%SVL in males vs. 7.5%SVL in females: Table 1).
Snout may be pointed or slightly rounded; freely movable flap may be on outer edge of third finger; web of fourth toe incised slightly on both sides, or slightly outer and fairly well inner; some with weak dorsolateral fold on anterior half of dorsum; anus without tubercles or with few, minute warts; tibia may be with few small warts, ridges and warts, or scattered with small and medium-sized warts.
Dorsum may be reddish brown with small spots, yellow brown with irregular small spots; width of supratympanic stripe may be medium, wide, or very wide; lateral side of snout may be totally dark brown; upper lip bar may be absent or clear; lower lip bar may be clear; throat may be spotted with dark brown; bar on forelimb and thigh may be dark and clear.
Comparisons
Limnonectes lanjakensis sp. nov. is sympatric with L. kong and L. abanghamidi sp. nov. in Lanjak, but differs from them in many morphometric characteristics (see below).
The uncorrected pairwise sequence divergences for fragments (445 bp of 16S rRNA) between L.lanjakensis sp. nov. and the co-occurring L. kong are 5.8–6.5% and L. abanghamidi sp. nov. were 5.0–5.5% (Matsui et al., 2016).
Limnonectes lanjakensis sp. nov. differs from L tawauensis sp. nov. by longer forelimb (RFLL median 60.5%SVL vs. 56.8%SVL) and inner metatarsal tubercle (RIMTL median 8.3%SVL vs. 7.2%SVL), and shorter eye (REL median 14.1%SVL vs. 15.4%SVL) in males, and by wider disk of third finger (R3FDW median 2.6%SVL vs. 1.8%SVL) and of fourth toe (R4TDW median 3.7%SVL vs. 2.3%SVL); from L. barioensis sp. nov. by wider disk of fourth toe (R4TDW median 3.7%SVL vs. 2.7%SVL) and larger ratio of disk to base of fourth toe (4TDW/4TDbW median 1.6 vs. 1.2); from L. conspicillatus by longer lower arm and hand (RLAHL median 46.5%SVL vs. 43.7%SVL) and forelimb (RFLL median 60.5%SVL vs. 55.8%SVL) in males, and by wider disk of fourth toe (R4TDW median 3.7%SVL vs. 2.7%SVL), and larger ratios of disk to base of third finger (3FDW/3FDbW median 1.2 vs. 1.0) and of disk to base of fourth toe (4TDW/4TDbW median 1.6 vs. 1.3); from L. lambirensis sp. nov. by wider disk of fourth toe (R4TDW median 3.7%SVL vs. 2.5%SVL) and base of fourth toe disk (R4TDbW median 2.3%SVL vs. 2.1%SVL), and larger ratios of disk to base of third finger (3FDW/3FDbW median 1.2 vs. 1.0) and of disk to base of fourth toe (4TDW/4TDbW median 1.6 vs. 1.2); from L. kong by wider disk of fourth toe (R4TDW median 3.7%SVL vs. 2.5%SVL), and larger ratio of disk to base of third finger (3FDW/3FDbW median 1.2 vs. 1.0); from L. mocquardi by wider disk of fourth toe (R4TDW median 3.7%SVL vs. 2.9%SVL); from L. penerisanensis sp. nov. by longer forelimb (RFLL median 60.5%SVL vs. 56.9%SVL) and narrower upper eyelid (RUEW median 7.0%SVL vs. 8.2%SVL), shorter foot (RFL median 49.4%SVL vs. 51.6%SVL) and first toe (R1TOEL median 13.4%SVL vs. 15.0%SVL) in males; from L. separatus sp. nov. by shorter inner metacarpal tubercle (RIMCL median 5.1%SVL vs. 5.2%SVL) in males; from L. batulawensis sp. nov. by narrower base of fourth toe disk (R4TDbW median 2.3%SVL vs. 2.9%SVL) and larger ratio of disk to base of fourth toe (4TDW/4TDbW median 1.6 vs. 1.3); and from L. paulyambuni sp. nov. by longer forelimb (RFLL median 60.5%SVL vs. 56.4%SVL) in males.
Range
Endemic to Sarawak. Sri Aman Division, Lubok Antu District, Lanjak Entimau, 250 m asl. Sibu Division, Kanowit District, Kanowit, 31 m asl.
11. Limnonectes abanghamidi Matsui sp. nov.
[English name: Abang's Fanged Frog]
Fig. 8A, B
Limnonectes sp. Lineage 15 Matsui et al., 2016, 308.
Holotype
SFC-GRB-00610 (former KUHE 17484) an adult female from Sungai Jelak, a branch of Sungai Engkari, Bukit Lanjak, Sri Aman Division, Sarawak (01°20′N, 112°00′E, 250 m asl, on 25 August 1993 by M. Matsui.
Paratypes
Sarawak. SFC-GRB-00611 (former KUHE 17453) a juvenile collected on 31 August 1993 from the type locality.
Referred specimen
Sarawak. KUHE 17417 collected on 31 August 1993 from the type locality.
Etymology
The specific epithet abanghamidi is dedicated to the late Abang Abdul Hamid of Forest Department of Sarawak, who greatly helped M. Matsui in earlier surveys in Sarawak, including collection of the new species in preliminary surveys of then proposed Lanjak Entimau Wildlife Sanctuary.
Diagnosis
The new species can be differentiated from its relatives by the combination of first finger as long as second; outer edge of third finger with non-movable, narrow ridges of skin; inner and outer webbing of fourth toe not much excised (Fig. 12K). A small-sized species with mean female SVL 45 mm; head short; forelimb medium; hindlimb medium; tibia medium-sized; dorsal skin extremely folded, with networks of wrinkles running in all directions, but few warts; wrinkles very weak on eyelid, and top of head and snout nearly smooth; surface of tibia coarsely covered with wrinkles (Fig. 11K); tip of third finger forming moderate-sized disk, width slightly wider than basal phalanx (Fig. 10K); tip of fourth toe swollen into large disk much wider than basal phalanx; fourth toe disk much wider than third finger disk; fourth toe broadly webbed to disk; dorsum light brown with dark brown markings dorsolaterally, irregularly on dorsum, and on interorbital.
Description of holotype (measurements in mm)
Snout-vent length (SVL) 55.4; habitus moderately stocky; head short and not enlarged, longer (HL 24.0, 43.3%SVL) than broad (HW 22.8, 41.2% SVL); snout rounded dorsally and laterally, projecting beyond lower jaw; eye length (EL 8.5, 15.3%SVL) slightly larger than snout length (SL 8.0, 14.4%SVL); canthus distinct; lore slightly sloping, concave; nostril dorsolateral, below canthus, slightly closer to snout than to eye; internarial distance (IND 5.0, 9.0%SVL) wider than interorbital distance (IOD 4.3, 7.8%SVL), latter slightly wider than upper eyelid (UEW 4.1, 7.4%SVL); tympanum indistinct; lower jaw with a pair of low projections near symphysis, about twice the depth of mandible at base of projections; vocal sac and vocal slits absent.
Forelimb medium-sized (FLL 29.8, 53.8%SVL; LAHL 24.4, 44.0%SVL); fingers moderately slender; first finger as long as second; length of first, measured from distal edge of inner metacarpal tubercle (1FL 7.1, 12.8%SVL) shorter than length of eye; tips of fingers slightly swollen, forming moderate-sized disks without circummarginal grooves; disk width of third finger (3FDW 1.1, 2.2%SVL) slightly wider than basal phalanx; remnant of webs between fingers; inner metacarpal tubercle moderate (IMCL 3.7, 6.7%SVL) oval, slightly elevated; middle metacarpal tubercle oval, smaller than and not contacting inner metacarpal tubercle; outer metacarpal tubercle elongate, as large as middle metacarpal tubercle; proximal subarticular tubercles oval and elevated; distal subarticular tubercles low; no supernumerary metacarpal tubercles; outer edge of third finger with freely movable, narrow ridges of skin; inner edges of third and outer edge of second finger with not freely movable dermal fringes.
Hindlimb medium-sized (HLL 85.8, 154.9%SVL) less than three times length of forelimb; tibia medium-sized (TL 36.4, 65.7%SVL), heels not overlapping when limbs are held at right angles to body; tibiotarsal articulation of adpressed limb reaching to center of eye; foot (FL 36.1, 65.2%SVL) slightly shorter than tibia; tips of toes swollen into large disks, disk width of fourth toe (4TDW 1.8, 3.2%SVL) much wider than basal phalanx; fourth toe broadly webbed to disk; inner and outer webbing of fourth toe little excised; a flap of skin along outer edge of fifth toe freely movable; subarticular tubercles oval and distinct; an elongate inner metatarsal, length (IMTL 4.1, 7.4%SVL) more than half length of first toe (1TOEL 6.9, 12.5%SVL); no outer metatarsal tubercle.
Dorsal skin extremely folded, with networks of wrinkles running in all directions, but few warts; wrinkles very weak on eyelid, and top of head and snout nearly smooth; weak transverse groove between upper eyelids; temporal fold from eye to above insertion of upper arm; throat, chest, and abdomen smooth; skin of gular region not modified; warts around anus weak; dorsal surface of limbs coarsely covered with wrinkles; tarsus with a thick dermal ridge extending proximally from metatarsal tubercle.
Color
In preservative, dorsum light brown with dark brown markings dorsolaterally, irregularly on dorsum, and on interorbital; a dark brown stripe below canthus in front of eye, continuing oblique dark brown supratympanic stripe of medium width; side of head pale brown with obscure brown marking; upper and lower lips light brown with obscure white spots; throat cream very lightly spotted with light brown; chest to abdomen cream; limbs with dark crossbars dorsally; ventral side of limbs cream, not spotted with brown, except for dark brown ventral surfaces of hand and foot.
Variation
Morphometric sexual dimorphism is unknown because of the paucity of specimens.
Snout may be slightly pointed; dorsum may have almost no warts; anus may lack surrounding warts; tibia may have several ridges and few warts.
Dorsal ground color may be dark brown; dark interorbital bar may anteriorly with light brown bar, or sometimes connecting dark marking; dark medial marking may be present between dorsolateral dark stripes brown crossbars on limbs may be weak.
Comparisons
Limnonectes abanhamidi sp. nov. is sympatric with L. kong and L. lanjakensis sp. nov. in Lanjak. The uncorrected pairwise sequence divergence for fragments (445 bp of 16S rRNA) between L. abanghamidi sp. nov. and the co-occurring L. kong was 8.3–8.5%, and L. lanjakensis sp. nov. was 5.0–5.5% (Matsui et al., 2016).
Limnonectes abanhamidi sp. nov. differs from L. tawauensis sp. nov. by wider disk of fourth toe (R4TDW median 3.2%SVL vs. 2.3%SVL); from L. conspicillatus by larger ratio of disk to base of third finger (3FDW/3FDbW median 1.2 vs. 1.0); from L. lambirensis sp. nov. by wider disk of fourth toe (R4TDW median 3.2%SVL vs. 2.5%SVL), larger ratios of disk to base of third finger (3FDW/3FDbW median 1.2 vs. 1.0) and of disk to base of fourth toe (4TDW/4TDbW median 1.5 vs. 1.2); from L. kong by wider disk of fourth toe (R4TDW median 3.2%SVL vs. 2.5%SVL) and larger ratios of disk to base of third finger (3FDW/3FDbW median 1.5 vs. 1.2); from L. batulawensis sp. nov. by narrower base of fourth toe disk (R4TDbW median 2.2%SVL vs. 2.9%SVL).
Range
Endemic to Sarawak. Sri Aman Division, Lubok Antu District, Lanjak Entimau, 250 m asl.
Natural history
The female holotype emitted calls in the container.
Fig. 8.
Dorsal (A, C) and ventral (B, D) views of female holotype of Limnonectes abanghamidi sp. nov. (SFC-GRB-00610 [=former KUHE 17484], A, B) and female of L. batulawensis sp. nov. (KUHE 53536, C, D). Scale bar=10 mm.
12. Limnonectes batulawensis Matsui, Nishikawa et Eto sp. nov.
[English name: Sarawak Mountain Fanged Frog]
Fig. 8C, D
Limnonectes sp. Lineage 16 Matsui et al., 2016, 308.
Holotype
SFC-GRB-00612 (former KUHE 12372) an adult female from Pa Belaban, Bario, Miri Division, Sarawak (03°51′N, 115°31′E, 1150 m asl) collected on 18 January 1991 by M. Matsui
Paratypes
Sarawak. SFC-GRB-00613 (former KUHE 12371), juvenile female, and SFC-GRB-00614 (former KUHE 12373) subadult female, data same as the holotype.
Referred specimens
Sarawak. KUHE 53535, 53536 from New Dam, Bario, Miri Division (03°45′N, 115°26′E, 1150 m asl) collected on 11 August 2010 by M. Matsui. KUHE 55303, 55329 from Camp 2 of Gunung Mulu NP, Miri Division (04°02′31″N, 114°52′16″E, 509 m asl) collected on 4 March 2013 by K. Nishikawa and K. Eto.
Etymology
The specific epithet batulawensis is derived from the Batu Lawi Hills, a twin-peaked mountain in the Kelabit Highlands of Sarawak, where this species inhabits.
Diagnosis
The new species can be differentiated from its relatives by the combination of tibia dorsally with ridges, and scattered with small, low warts (Fig. 11L); tip of third finger forming large disk slightly wider than basal phalanx (Fig. 10L); tip of fourth toe swollen into large disk, width wider than basal phalanx; fourth toe broadly webbed to disk. A medium-sized species with adult mean SVL 49 mm in males and 54 mm in females; head long; forelimb medium; hindlimb medium; tibia medium-sized; dorsum dark brown without darker marking; first finger slightly longer than second; outer edge of second finger and both edges of third fingers with freely movable, narrow ridges of skin; fourth toe disk much wider than third finger disk; inner and outer webbing of fourth toe excised (Fig. 12L).
Description of holotype (measurements in mm)
SVL 51.8; habitus moderately stocky; head long, not enlarged, longer (HL 22.1, 42.7%SVL) than broad (HW 21.2, 40.9% SVL); snout slightly pointed, rounded in profile, slightly projecting beyond lower jaw; eye length (EL 8.2, 15.8%SVL) slightly smaller than snout length (SL 8.7, 16.8%SVL); canthus distinct; lore slightly sloping, concave; nostril dorsolateral, below canthus, slightly closer to snout than to eye; internarial distance (IND 4.6, 8.9%SVL) slightly wider than interorbital distance (IOD 4.4, 8.5%SVL), latter wider than upper eyelid (UEW 3.8, 7.3%SVL); pineal spot between anterior corners of eyes; tympanum indistinct but visible, oval, diameter (TD 2.8, 8.8% SVL) more than half eye length and separated from eye (T-EL 1.3, 4.1% SVL) by half of tympanum diameter; lower jaw with a pair of low projections near symphysis, about twice the depth of mandible at base of projections; vocal sac and vocal slits absent.
Forelimb medium-sized (FLL 32.2, 62.2%SVL; LAHL 24.3, 46.9%SVL); fingers moderately slender; first finger slightly longer than second; length of first, measured from distal edge of inner metacarpal tubercle (1FL 7.6, 14.7%SVL) shorter than length of eye; tips of fingers slightly swollen, forming large disks without circummarginal grooves; disk width of third finger (3FDW 1.1, 2.1%SVL) slightly wider than basal phalanx; remnant of webs between fingers; inner metacarpal tubercle moderate (IMCL 3.1, 6.0%SVL) oval, slightly elevated; middle metacarpal tubercle oval, smaller than and not contacting inner metacarpal tubercle; outer metacarpal tubercle elongate, smaller than inner metacarpal tubercle; proximal subarticular tubercles oval and elevated; distal subarticular tubercles low; no supernumerary metacarpal tubercles; outer edge of second finger and both edges of third fingers with freely movable, narrow ridges of skin; other finger edges with not freely movable dermal fringes.
Hindlimb medium-sized (HLL 91.8, 177.2%SVL) less than three times length of forelimb; tibia medium-sized (TL 28.2, 54.4%SVL), heels not overlapping when limbs are held at right angles to body; tibiotarsal articulation of adpressed limb reaching to anterior corner of eye; foot (FL 30.3, 58.5%SVL) longer than tibia; tips of toes swollen into large disks, disk width of fourth toe (4TDW 1.8, 3.4%SVL) wider than basal phalanx; fourth toe broadly webbed to disk; inner and outer webbing of fourth toe excised; a flap of skin along outer edge of fifth toe freely movable; subarticular tubercles oval and distinct; an elongate inner metatarsal, length (IMTL 4.6, 8.9%SVL) more than half length of first toe (1TOEL 8.6, 16.6%SVL); no outer metatarsal tubercle.
Dorsal skin with networks of wrinkles running in all directions, but with few warts; wrinkles very weak on eyelid, and top of snout nearly smooth; very weak transverse fold between posterior margins of eyes; temporal fold from eye to above insertion of upper arm; throat not covered with wrinkles; chest, and abdomen smooth; side of trunk scattered with fine warts with white tips; anus with very fine warts; dorsal surface of tibia and tarsus with longitudinal, low ridges, and scattered with small, low warts; tarsus with a thick dermal ridge extending proximally from metatarsal tubercle.
Color
In preservative, dorsum brown without darker marking except for dark brown markings on interorbital and upper eyelid; a narrow, oblique dark brown supratympanic stripe from behind eye to above arm insertion; canthus rostralis dark brown; side of head from the level of posterior end of eye to inguinal area cream brown with a dark brown marking; lateral side of trunk lighter without spots; upper lip with vague dark brown bars; lower lip dark brown with narrow white bars; limbs with a few dark crossbars dorsally; throat totally and chest partly covered with brown marking; abdomen cream; ventral side of limbs spotted with brown, especially heavily on posterior thigh and tibia; anterior and posterior thigh mottled with dark brown;: ventral side of lower arm dark brown.
Variation
SVL did not differ between the sexes, but the ratio to SVL was sexually dimorphic in RTHIGHL (median 50.7%SVL in males smaller than 55.1%SVL in females) and R1FL (median 13.3%SVL in males smaller than 14.3%SVL in females: Table 1).
Some have a pointed snout; first and second fingers may be nearly same in length; outer edges of second and third fingers may be with movable ridges of skin; web may be incised slightly on outer side and fairly well on inner side, or slightly on both sides; lateral body finely wrinkled in some; in some, throat weakly wrinkled; anus may have almost no warts.
Color of dorsum variable, some light brown with irregular dark markings, some including dorsolateral one, and some with dark spots on warts; some with a wide, cream middorsal stripe; usually a light brown bar anterior to dark brown interorbital bar; width of supratympanic band maybe moderately wide to wide; dark bar on upper lip sometimes continuous, or clear; dark bar on lower lip variable from indistinct, irregular to clear; lateral side of trunk may be slightly spotted or mottled with dark brown; throat may be cream; dark bar on limbs may be evident or unclear; in some, ventral side of forelimb and tibia dusted with brown.
Comparisons
Limnonectes batulawensis sp. nov. is sympatric with L. barioensis sp. nov. in Bario and L. separatus sp. nov. in Mulu.
The uncorrected pairwise sequence divergences for fragments (445 bp of 16S rRNA) between L. batulawensis sp. nov. and the co-occurring L. barioensis sp. nov. and L. separatus sp. nov. were 7.8–8.5% and 3.3–3.5%, respectively (Matsui et al., 2016).
Limnonectes batulawensis sp. nov. differs from L. tawauensis sp. nov. by wider internarial (RIND median 9.0%SVL vs. 7.8%SVL), longer snout (RSL median 16.2%SVL vs. 15.5%SVL), and longer forelimb (RFLL median 58.3%SVL vs. 56.8%SVL) in males and by wider disk of third finger (R3FDW median 2.5%SVL vs. 1.8%SVL), of fourth toe (R4TDW median 3.8%SVL vs. 2.3%SVL), and base of fourth toe disk (R4TDbW median 2.9%SVL vs. 1.6%SVL); from L. barioensis sp. nov. by longer foot (RFL median 55.5%SVL vs. 47.4%SVL), and inner metatarsal tubercle (RIMTL median 8.6%SVL vs. 6.6%SVL), longer thigh (RTHIGHL median 55.1%SVL vs. 48.9%SVL), and tibia (RTL median 53.6%SVL vs. 47.2%SVL) in females, and by wider base of fourth toe disk (R4TDbW median 2.9%SVL vs. 2.2%SVL); from L. conspicillatus by wider disk of fourth toe (R4TDW median 3.8%SVL vs. 2.7%SVL) and base of fourth toe disk (R4TDbW median 2.9%SVL vs. 2.0%SVL); from L. lambirensis sp. nov. by wider internarial (RIND median 9.0%SVL vs. 7.6%SVL), longer tibia (RTL median 53.6%SVL vs. 46.7%SVL), thigh (RTHIGHL median 55.1%SVL vs. 48.1%SVL), and inner metatarsal tubercle (RIMTL median 8.6%SVL vs. 7.0%SVL) in females, and by wider disk of third finger (R3FDW median 2.5%SVL vs. 2.1%SVL), of fourth toe (R4TDW median 3.8%SVL vs. 2.5%SVL) and base of fourth toe disk (R4TDbW median 2.9%SVL vs. 2.1%SVL), and larger ratio of disk to base of third finger (3FDW/3FDbW median 1.2 vs. 1.0); from L. kong by longer thigh (RTHIGHL median 55.1%SVL vs. 48.5%SVL) in females, and by wider disk of third finger (R3FDW median 2.5%SVL vs. 2.0%SVL), of fourth toe (R4TDW median 3.8%SVL vs. 2.5%SVL) and base of fourth toe disk (R4TDbW median 2.9%SVL vs. 2.0%SVL), and larger ratio of disk to base of third finger (3FDW/3FDbW median 1.2 vs. 1.0); from L. mocquardi by longer thigh (RTHIGHL median 55.1%SVL vs. 49.3%SVL) in females, and by wider base of fourth toe disk (R4TDbW median 2.9%SVL vs. 1.9%SVL); from L. paginatanensis sp. nov. by wider head (RHW median 41.4%SVL vs. 38.6%SVL), longer thigh (RTHIGHL median 55.1%SVL vs. 49.2%SVL), and inner metatarsal tubercle (RIMTL median 8.6%SVL vs. 6.8%SVL) in females; from L. separatus sp. nov. by wider base of fourth toe disk (R4TDbW median 2.9%SVL vs. 2.4%SVL); from L. lanjakensis sp. nov. by wider upper eyelid (RUEW median 8.2%SVL vs. 7.0%SVL), longer eye (REL median 16.3%SVL vs. 14.1%SVL) and first toe (R1TOEL median 14.6%SVL vs. 13.4%SVL), but shorter forelimb (RFLL median 58.3%SVL vs. 60.5%SVL) in males, and by wider base of fourth toe disk (R4TDbW median 2.9%SVL vs. 2.3%SVL) and smaller ratio of disk to base of fourth toe (4TDW/4TDbW median 1.3 vs. 1.6); and from L. abanghamidi sp. nov. by wider base of fourth toe disk (R4TDbW median 2.9%SVL vs. 2.2%SVL).
Range
Endemic to Sarawak. Miri Division, Miri District, Bario Subdistrict, Bario, 1150 m asl; Miri Division, Marudi District, Gunung Mulu NP, Camp 2, 509 m asl.
Fig. 9.
Dorsal (A) and ventral (B) views of female holotype of Limnonectes paulyambuni sp. nov. (BOR 12714, A, B). Scale bar=10 mm.
13. Limnonectes paulyambuni Matsui, Nishikawa et Shimada sp. nov.
[English name: Paul's Fanged Frog]
Fig. 9A, B
Limnonectes sp. Lineage 17 Matsui et al, 2016, 308.
Holotype
BOR 12714, an adult female from TBC (Taman Banjaran Crocker=CRP HQ), Kimanis, Interior Division, Sabah (05°23′41″N, 116°06′15″E, 960 m as.), collected on 12 August 2003 by M. Matsui, K. Nishikawa, and T. Shimada.
Paratypes
Sabah. BOR 12713, 12716, data same as the holotype. BOR 12792 collected on 15 August 2003 and BOR 12855 on 20 August 2003 from the type locality by M. Matsui, K. Nishikawa, and T. Shimada.
Referred specimens
Sabah. BOR 12429, 12430, 12431 collected on 4 August 2003, BOR 12485 on 6 August 2003, BOR 12553 on 7 August 2003, BOR 12571, 12572 on 8 August 2003, and BOR 23511 on 21 August 2005, all from Mahua substation of CRP, Tambunan District, Interior Division (05°48′00″N, 116°24′05″E, 1200 m asl) by M. Matsui, K. Nishikawa, and T. Shimada. BOR 22979, 23012 on 12 August 2005 from Sayap substation of KNP, Kota Belud (06°12′N, 116°33′E, 909 m asl), by M. Matsui, K. Nishikawa, and T. Shimada. BOR 22393 collected from Agatis Camp, Maliau Basin (04°54′N, 116°53′E, 1050 m asl) on 5 March 2005 by T. Shimada.
Etymology
The specific epithet paulyambuni is dedicated to Mr. Paul Yambun Imbun of Sabah Parks, for his great help in our herpetological surveys in Sabah.
Diagnosis
The new species can be differentiated from its relatives by the combination of first finger as long as second; outer edge of second and third fingers with freely movable, narrow ridges of skin; tip of third finger forming moderate-sized disk, slightly wider than basal phalanx (Fig. 10M); inner and outer webbing of fourth toe slightly excised (Fig. 12M). A medium-sized species with adult mean SVL 50 mm in males and 55 mm in females; head medium, forelimb short, hindlimb medium; tibia medium-sized; dorsal skin extremely folded, with networks of wrinkles running in all directions, but with few warts; wrinkles very weak on eyelid, and top of snout nearly smooth; tibia dorsally coarsely scattered with small, low warts with white tips (Fig. 11M); tip of fourth toe swollen into large disk, wider than basal phalanx; fourth toe disk much wider than third finger disk; fourth toe broadly webbed to disk; dorsum dark brown without darker marking.
Description of holotype (measurements in mm)
Snout-vent length (SVL) 67.5; habitus moderately stocky; head medium-sized, not enlarged, slightly longer (HL 29.9, 44.3%SVL) than broad (HW 28.6, 42.4% SVL); snout slightly rounded, rounded in profile, projecting beyond lower jaw; eye length (EL 10.7, 15.9%SVL) slightly larger than snout length (SL 10.2, 15.1%SVL); canthus distinct; lore slightly sloping, concave; nostril dorsolateral, below canthus, slightly closer to snout than to eye; internarial distance (IND 5.5, 8.1%SVL) narrower than interorbital distance (IOD 6.1, 9.0%SVL), latter wider than upper eyelid (UEW 4.9, 7.3%SVL); tympanum not visible; vomerine teeth in oblique groups, between medial rims of choanae, groups closely set from one another, and from choana by half length of one group; lower jaw with a pair of low projections near symphysis, about twice the depth of mandible at base of projections; vocal sac and vocal slits absent.
Forelimb moderately thick, short (FLL 39.6, 58.7%SVL; LAHL 31.6, 46.8%SVL); fingers moderately slender; first finger as long as second; length of first, measured from distal edge of inner metacarpal tubercle (1FL 8.9, 13.2%SVL) shorter than length of eye; tips of fingers slightly swollen, forming moderate-sized disks without circummarginal grooves; disk width of third finger (3FDW 1.5, 2.2%SVL) slightly wider than basal phalanx; remnant of webs between fingers; inner metacarpal tubercle moderate (IMCL 4.3, 6.4%SVL) oval, only slightly elevated; middle metacarpal tubercle flat, smaller than and not contacting inner metacarpal tubercle; outer metacarpal tubercle elongate, smaller than inner metacarpal tubercle; proximal subarticular tubercles oval and elevated; distal subarticular tubercles low, but distinct; no supernumerary metacarpal tubercles; outer edge of second and third fingers with freely movable, narrow ridges of skin; other finger edges with not freely movable dermal fringes.
Hindlimb thick, medium-sized (HLL 107.9, 159.9%SVL) less than three times length of forelimb; tibia medium-sized (TL 33.9, 50.2%SVL), heels not overlapping when limbs are held at right angles to body; foot (FL 35.2, 52.2%SVL) slightly longer than tibia; tips of toes swollen into large disks, disk width of fourth toe (4TDW 2.3, 3.4%SVL) wider than basal phalanx; inner and outer webbing of fourth toe slightly excised; fourth toe broadly webbed to disk; a flap of skin along outer edge of fifth toe freely movable; subarticular tubercles oval and distinct; an elongate inner metatarsal, length (IMTL 5.9, 8.7%SVL) more than half the length of first toe (1TOEL 10.3, 15.3%SVL); no outer metatarsal tubercle.
Dorsal skin extremely folded, with networks of wrinkles running in all directions, but with few warts; wrinkles very weak on eyelid, and top of snout nearly smooth; no transverse fold between posterior margins of eyes; temporal fold from eye to above insertion of upper arm; warts around anus fine, tipped with white; side of trunk finely reticulated by wrinkles and scattered with low warts with white tips; dorsal surface of tibia and tarsus coarsely scattered with small, low warts with white tips; tarsus with a thick dermal ridge extending proximally from metatarsal tubercle; throat covered with weak wrinkles; chest, and abdomen smooth; skin of gular region not modified.
Color
In preservative, dorsum dark brown with a cream-colored mid-dorsal stripe, and without darker marking; an oblique dark brown supratympanic stripe from behind eye to above arm insertion; canthus dark brown; side of head from posterior half of lore to inguinal area cream brown with a dark brown marking; lateral side of trunk lighter than dorsum; upper lip with dark brown bars; lower lip dark brown with white spots; throat cream dusted with brown; chest to abdomen cream; limbs with a few dark crossbars dorsally; ventral side of limbs cream spotted with brown, especially heavily on posterior thigh; underside of lower arm dark brown.
Variation
SVL did not differ between the sexes, but the ratio to SVL was sexually dimorphic in thigh length (RTHIGHL median 52.4%SVL in males smaller than 55.2%SVL in females, Table 1).
Some with pointed snout; some with eye shorter than snout; some has internarial wider than interorbital, which is narrower than upper eyelid: some has visible pineal spot, and tympanum partly visible: some with first finger slightly longer than second; males with dark brown nuptial pad; some with foot slightly shorter than tibia: incision on fourth toe web variable, fairly well on inner side and slightly on outer side, fairly well on both sides, and slightly on both sides; dorsum wrinkled with few warts, and wrinkles from scattered small warts; some with tuberculated dorsum; some slightly wrinkled snout; unlike holotype, some with transverse fold between posterior margins of eyes; posterodorsal texture of tibia variable, covered with small white-tipped warts, ridges and few warts, and ridge and warts forming longitudinal rows.
Dorsum brown or light brown with irregular dark brown marking: some with wider middorsal stripe than holotype, but others without mid-dorsal stripe; dark interorbital bar and anterior light bar usually present; supratympanic stripe moderately wide or fairly wide; upper lip bar indistinct, distinct, or wide, and lower lip bar distinct, indistinct, or continuous; throat mottled, dusted or spotted brown; chest sometimes spotted with brown; lateral side of body becoming paler gradually or abruptly; tibia dusted with brown ventrally or mainly laterally.
Comparisons
Limnonectes paulyambuni sp. nov. is sympatric with L. barioensis sp. nov. and L. mocquardi in Mahua (CRP). The uncorrected pairwise sequence divergences for fragments (445 bp of 16S rRNA) between L. paulyambuni sp. nov. and the co-occurring L. barioensis sp. nov. were 8.3–10.0%, and L. mocquardi were 5.5–7.0% (Matsui et al., 2016).
Limnonectes paulyambuni sp. nov. differs from L. tawauensis sp. nov. by longer thigh (RTHIGHL median 52.4%SVL vs. 48.7%SVL in males and 55.2%SVL vs. 49.0%SVL in females) and longer inner metatarsal tubercle (RIMTL median 7.9%SVL vs. 7.2%SVL) in males, and by wider disk of fourth toe (R4TDW median 3.6%SVL vs. 2.3%SVL); from L. barioensis sp. nov. by longer lower arm and hand (RLAHL median 46.0%SVL vs. 43.8%SVL) in females; from L. conspicillatus by longer thigh (RTHIGHL median 52.4%SVL vs. 49.5%SVL in males and 55.2%SVL vs. 49.4%SVL in females); from L. lambirensis sp. nov. by longer head (RHL median 42.2%SVL vs. 41.7%SVL) and thigh (RTHIGHL median 55.2%SVL vs. 48.1%SVL) in females, and by wider disk of fourth toe (R4TDW median 3.6%SVL vs. 2.5%SVL), larger ratios of disk to base of third finger (3FDW/3FDbW median 1.1 vs. 1.0), and of disk to base of fourth toe (4TDW/4TDbW median 1.4 vs. 1.2); from L. kong by longer thigh (RTHIGHL median 52.4%SVL vs. 48.9%SVL in males and 55.2%SVL vs. 48.5%SVL in females), and by wider disk of fourth toe (R4TDW median 3.6%SVL vs. 2.5%SVL); from L. mocquardi by longer thigh (RTHIGHL median 55.2%SVL vs. 49.3%SVL) in females; from L. paginatanensis sp. nov. by longer head (RHL median 42.2%SVL vs. 40.4%SVL) and thigh (RTHIGHL median 55.2%SVL vs. 49.2%SVL) in females; from L. separatus sp. nov. by longer thigh (RTHIGHL median 52.4%SVL vs. 51.0%SVL) in males; from L. lanjakensis sp. nov. by shorter forelimb (RFLL median 56.4%SVL vs. 60.5%SVL) in males.
Range
Endemic to Sabah. Interior Division, Keningau District, TBC (=CRP HQ), 960 m asl. Interior Division, Tambunan District, Mahua, 1200 m asl. West Coast Division, Kota Belud District, Sayap substation of KNP, 909 m asl. Sandakan Division, Tongod District, Agatis Camp, Maliau Basin, 1050 m asl.
Fig. 10.
Ventral views of hand of A: Limnonectes tawauensis sp. nov. (BOR 08104); B: L. barioensis sp. nov. (SFC-GRB-00599); C: L. conspicillatus (KUHE 54524); D: L. lambirensis sp. nov. (SFC-GRB-00602); E: L. kong (KUHE 53824); F: L. mocquardi (SP 21468); G: L. penerisanensis sp. nov. (SFC-GRB-00604); H: L. paginatanensis sp. nov. (BOR 22492); I: L. separatus sp. nov. (BOR 23415); J: L. lanjakensis sp. nov. (SFC-GRB-00608); K: L. abanghamidi sp. nov. (SFC-GRB-00610); L: L. batulawensis sp. nov. (SFC-GRB-00612); M: L. paulyambuni sp. nov. (BOR 12553). Not to scale.
Fig. 11.
Dorsal views of tibia of A: Limnonectes tawauensis sp. nov. (BOR 12848); B: L. barioensis sp. nov. (SFC-GRB-00600); C: L. conspicillatus (KUHE 54524); D: L. lambirensis sp. nov. (KUHE 53687); E: L. kong (KUHE 17158); F: L. mocquardi (BOR 22776); G: L. penerisanensis sp. nov. (KUHE 55638); H: L. paginatanensis sp. nov. (BOR 22492); I: L. separatus sp. nov. (BOR 23415); J: L. lanjakensis sp. nov. (SFC-GRB-00608); K: L. abanghamidi sp. nov. (SFC-GRB-00610); L: L. batulawensis sp. nov. (KUHE 53536); M: L. paulyambuni sp. nov. (BOR 12716). Not to scale.
Fig. 12.
Ventral views of foot of A: Limnonectes tawauensis sp. nov. (SP 01554); B: L. barioensis sp. nov. (SFC-GRB-00600); C: L. conspicillatus (KUHE 54524); D: L. lambirensis sp. nov. (KUHE 53601); E: L. kong (KUHE 42642); F: L. mocquardi (BOR 22776); G: L. penerisanensis sp. nov. (SFC-GRB-00604); H: L. paginatanensis sp. nov. (BOR 22807); I: L. separatus sp. nov. (SP 21075); J: L. lanjakensis sp. nov. (KUHE 42573); K: L. abanghamidi sp. nov. (SFC-GRB-00610); L: L. batulawensis sp. nov. (KUHE 53536); M: L. paulyambuni sp. nov. (BOR 12855). Not to scale.
Discussion
Results of the molecular phylogenetic analyses indicated that the L. kuhlii-like fanged frogs were split into three clades that geographically correspond to continental, Javanese, and Bornean regions (Matsui et al., 2016). In the Bornean clade, at least 17 distinct lineages were recognized, and 13 of which, from the Malaysian part were examined morphologically in the present study.
Sympatric occurrence of different lineages (Matsui et al., 2016) supports their independent species statuses. Only lineage 7 (now L. lambirensis sp. nov.) was distributed singly, and the distribution of two or more species was found sympatrically in eight of 29 localities in Sabah and six of 17 localities in Sarawak. In two localities, Mahua, Sabah and Lanjak Entimau, Sarawak, three lineages were found sympatrically.
However, because of highly uniform morphology of lineages treated here, their taxonomic revision was very difficult. Among them, Lin. 6, 8, and 9 were assigned to known species. Matsui et al. (2013) fixed nomenclatural status and designated the lectotypes in each of L. conspicillatus and L. mocquardi, and from frequent occurrence in their type localities, DNA lineages of 6 and 9 in Matsui et al. (2016), respectively, were assigned to these species. Another named species L. kong was also assigned to Lin. 8 by Matsui et al. (2016) based on unique, incomplete fourth toe webbing and localities recorded (Dehling and Dehling, 2017).
As shown above, the remaining 10 genetic lineages proved to be diagnosable also morphologically. The mitochondrial DNA lineages 7 and 8, and 13 and 14, which Matsui et al. (2016) failed to diagnose by nuclear sequences, were differentiated by multivariate analyses, except for males of Lin. 7 and Lin. 8. Each of these lineages is separated by moderately large geographic distance (minimum straight line distance between Lin. 7 and Lin. 8 is about 310 km, and between Lin. 13 and 14 is 400 km), which would prevent present inter-species hybridization. Future analyses of nuclear DNA markers such as SNPs would be useful to reassess species delimitation and genetic introgression between these lineages.
High geographic variations shown by Inger (1966) in L. kuhlii (as Rana kuhli) are now regarded as interspecific, and not intraspecific. All the 13 species shown above, except for L. kong, are at present thought to be endemic to Malaysian Borneo. Limnonectes kong is distributed in Sarawak and not in Sabah, but it also occurs on a small Indonesian island (see below). Of these, three species, L. barioensis sp. nov., L. mocquardi, and L. separates sp. nov. are distributed in both Sabah and Sarawak states, and of the remaining species, three, L. tawauensis sp. nov., L. paginatanensis sp. nov., and L. paulyambungi sp. nov., are endemic to Sabah, while six, L. conspicillatus, L. lambirensis sp. nov., L. penerisanensis sp. nov., L. lanjakensis sp. nov., L. abanghamidi sp. nov., and L. batulawensis sp. nov. are endemic to Sarawak.
Additionally, mtDNA lineages of 2 and 12, not treated herein, occur in Sabah (Matsui et al., 2016). Thus, eight species occur in Sabah and 10 (including L. kong) in Sarawak. Furthermore, L. hikidai, L. cintalubang, and L. sinuatodorsalis are known from Sarawak as the species closely related to the L. kuhlii-like fanged frogs. Limnonectes hikidai (treated as Rana laticeps, in apposition to R. kuhli by Inger, 1966) is morphologically distinct, but genetically so close to some of 13 lineages as to be embedded in one of two major genetic clades (Matsui et al., 2016). Limnonectes cintalubang is morphologically further distinct and formed a distinct clade with the Bornean L. kuhlii-like fanged frogs (cf. Fig. 1). Limnonectes sinuatodorsalis is not endemic to Sarawak but also occurs in neighboring East Kalimantan, Indonesia (Matsui, 2015).
Higher numbers of species in Sarawak (13), than in Sabah (eight), may be related to larger total areas of Sarawak (124,450 km2) than Sabah (73,904 km2), although Sabah has a complex geomorphology with Mt. Kinabalu, the highest mountain of the island. The total area of East Malaysia (Sabah and Sarawak), 198,354 km2, represents approximately 26% of the total area of Borneo. Thus, the remaining part of the island, Indonesian Kalimantan, is nearly three times as wide as Malaysian part and expected to contain many more species than East Malaysia.
However, only L. asperatus, L. rhacodus, L. sinuatodorsalis and Lin. 3 and 4 of Matsui et al. (2016), are known by now in Kalimantan. Limnonectes asperatus formed a monophyletic group with Lin. 7 and Lin. 8 in mtDNA tree of Matsui et al. (2016). Each of two lineages not treated herein (Lin. 3 and Lin. 4 in Matsui et al., 2016) is most probably distinct species like the Malaysian lineages demonstrated here. Another species, L. rhacodus (Inger, Boeadi and Taufik, 1996) also occurs in Kalimantan. This frog was recently misidentified with Occidozyga berbeza Matsui, Nishikawa, Eto, Hamidy, Hossman and Fukuyama, 2021, simply because of its superficial resemblance in body shape and color by Pui et al. (2013). However, in describing O. berbeza, Matsui et al. (2021) clearly demonstrated the generic status of L. rhacodus by showing the paired lateral tusks on the mandible in the holotype. Members of Occidozyga have a single cusp but lack lateral cusps on the mandible, and if actually examined, nobody would misidentify the generic status of the specimens. Notwithstanding this information, the species is still placed in the genus Occidozyga (Frost, 2024). Anyhow, the number of known members from Indonesian Borneo is very small compared with Malaysian Borneo, and future intensive surveys in Kalimantan is highly advocated.
Matsui et al. (2014a) surmised that the monophyletic Bornean clade of the L. kuhlii-like fanged frogs is endemic to the island. Later, L. kong was found on Serasan Island, part of the Natuna Islands in Indonesia (Herlambang et al., 2022). However, the island is only about 70 km apart from the western border of Malaysian Sarawak and Indonesian Kalimantan, on Borneo. Thus, the idea that the Bornean lineage is endemic to this island would be maintained.
With nearly 20 species, the diversity of the Bornean clade of the L. kuhlii-like fanged frogs seems to be higher than Leptobrachella (Matsui et al., 2017, as Leptolalax; Eto et al., 2018) and Meristogenys (Shimada et al., 2015) that are known for being highly diversified anuran genera on Borneo, and future taxonomic revisions of the L. kuhlii-like fanged frogs would further contribute to increase herpetofaunal diversity on this island.
Key for typical specimens
1(16) First finger usually longer than second
2(3) Tibial tubercles evidently large and dense L. tawauensis sp. nov.
3(2) Tibial tubercles not evident
4(5) Two phalanges free of web on fourth toe L. kong
5(4) Webbing to terminal phalanx on fourth toe
6(9) Disk on third finger small
7(8) Webs on fourth toe deeply excised L. conspicillatus
8(7) Webs on fourth toe little excised L. barioensis sp. nov.
9(6) Disk on third finger moderate to large
10(11) Disk on fourth toe small L. lambirensis sp. nov.
11(10) Disk on fourth toe moderate to large
12(13) Dorsum posteriorly with asperities L. paginatanensis sp. nov.
13(12) Dorsum without asperities
14(15) Disk on fourth toe wider than basal phalanx L. batulawensis sp. nov.
15(14) Disk on fourth toe much wider than basal phalanx L. penerisanensis sp. nov.
16(1) First finger as long as or shorter than second
17(20) Edges of third finger with non-moveable dermal ridges
18(19) Webs on fourth toe deeply excised L. mocquardi
19(18) Webs on fourth toe shallowly excised L. abanghamidi sp. nov.
20(17) Edges of third finger with moveable dermal fringes
21(24) Webs on fourth toe shallowly excised
22(23) Disk on third finger slightly wider than basal phalanx L. paulyambuni sp. nov.
23(22) Disk on third finger wider than basal phalanx L. separatus sp. nov.
24(21) Webs on fourth toe moderately excised L. lanjakensis sp. nov.
Acknowledgments
We thank the Economic-Planning Unit (former Socio-Economic Research Unit) of Malaysia, the State Government of Sarawak, and Sabah Parks, for kindly permitting to conduct the project, Universiti Malaysia Sabah, JICA, and the Sarawak Forestry Corporation and the Sarawak Biodiversity Centre (former Forestry Department, Sarawak), for kindly providing for all the facilities in conducting research. We also thank the Sarawak Government for the names for the new species from the state. We are grateful to the following for their encouragements and/or permission to conduct research and export specimens, and field companionship: H. Akiyama, L. Apin, K. Araya, D. Belabut, The late A.-A. Hamid, Y. Hashimoto, T. Hikida, H. Ota, A. H. Kassim, J. J. Kendawong, K. B. Kueh, T. Kusano, D. Labang, M. B. Lakim, M. Maryati, L.-H. Seng, T. Tachi, N.-S. Wong, Datu Haji Len Talif Salleh, Haji ali Bin Yusop, Marker Nyogin, Mohd. B. Kohdi, Mohd. Shabudin Sabki, Uning, Haji Abang Mohamad Mohtar Bin Abang Pawozan, Paulus Ak Meleng, T. Ichioka, S. T. Yeo, and N. Ahmad. We thank McCarthy C. and B. T. Clarke (BM), and A. Dubois and A. Ohler (MNHN) for allowing us to examine specimens under their care. We thank anonymous reviewers and Dr. Christine Kaiser for improving an earlier version of the manuscript. Field trips were made possible by grants from the Monbusho International Scientific Research Program (Field Research, 01041051, 02041051, 03041044, 04041068, 06041066, 08041144), the Monbukagakusho through the Japanese Society for the Promotion of Sciences (JSPS: Field Research, 15370038, 20405013, 23405014), JSPS Core-to-Core Program B, the Kondo Grant of the Asahi Glass Foundation, Shikata Memorial Trust for Nature Conservation, and JST/JICA, SATREPS.
© 2024 by The Herpetological Society of Japan
