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A New Unstriped Ichthyophis (Amphibia: Gymnophiona: Title Ichthyophiidae) from Mt. Kinabalu, Sabah, Malaysia

Author(s) Nishikawa, Kanto; Matsui, Masafumi; Yambun, Paul

Citation Current Herpetology (2012), 31(2): 67-77

Issue Date 2012-12

URL http://hdl.handle.net/2433/216843

Type Journal Article

Textversion publisher

A New Unstriped Ichthyophis (Amphibia: Gymnophiona: Ichthyophiidae) from Mt. Kinabalu, Sabah, Malaysia

1 1 2 KANTO NISHIKAWA *, MASAFUMI MATSUI , AND PAUL YAMBUN

1 Graduate School of Human and Environmental Studies, Kyoto University, Yoshida- Nihonmatsu-cho, Sakyo-ku, Kyoto 606–8501, Japan 2 Research and Education Division, Sabah Parks, P.O. Box 10626, Kota Kinabalu 88806, Sabah, Malaysia

Abstract: A new unstriped Ichthyophis is described based on one adult male and five larval specimens collected from the northwestern slope of Mt. Kinabalu, Sabah, Malaysia. The new species is distinguished from all other unstriped congeners by a combination of characters that includes position of tentacles and number of annuli, scale rows, splenial teeth, and vertebrae. The anterior phallodeum morphology is described for the new species. The evolution of large larvae of unstriped Ichthyophis is discussed briefly.

Key words: Caecilian; Ichthyophis; Taxonomy; New species; Borneo

INTRODUCTION Although the presence or absence of splenial teeth proved to be invalid for dividing the From the region of Southeast Asia, only one genera, these characteristics are still useful for family of caecilians, the Ichthyophiidae, has species identification in Ichthyophis. been recorded. This family has been regarded After synonymizing Caudacaecilia with as consisting of three genera, Caudacaecilia Ichthyophis, the genus Ichthyophis includes Taylor, 1968, Ichthyophis Fitzinger, 1826, and 44 species, of which 27 are known from Uraeotyphlus Peters, 1880 (Frost, 2011). Southeast Asia (Frost, 2011; Nishikawa et al., However, based on molecular phylogenetic 2012b). The species of Ichthyophis can be analyses, Nishikawa et al. (2012a) recently divided into two color types: one has a pair of showed that Caudacaecilia and Ichthyophis yellow or cream-colored lateral stripes (striped form a clade and the species of the two genera type); the other lacks such stripes (unstriped are mutually paraphyletic. Therefore, Cauda- type; Nishikawa et al., 2012a). Division of caecilia should be relegated to a junior syn- these two color types is not supported by the onym of Ichthyophis. Taylor (1968) desig- results of molecular phylogenetic analyses nated Caudacaecilia solely on the absence of (Gower et al., 2002; Nishikawa et al., 2012a), the splenial teeth in adults, in contrast to but the presence or absence of stripes is Ichthyophis, which retains the teeth in adults. extremely useful for species identification (Taylor, 1968; Wilkinson et al., 2007). * Corresponding author. TEL: +81–75–753–6848; In 2005 and 2006, we collected specimens Fax: +81–75–753–2891; of an unstriped species of Ichthyophis with E-mail address: [email protected] splenial teeth from Sayap station of Kinabalu 68 Current Herpetol. 31(2) 2012

National Park, Sabah, Malaysian part of lower jaw to jaw angle; snout-2nd collar Borneo Island. In Sabah and its vicinity, four groove length (S2CL), measured ventrally; unstriped Ichthyophis with splenial teeth are snout-3rd collar groove length (S3CL), mea- known: I. dulitensis Taylor, 1960 from sured dorsally; 1st collar length (1CL), mea- Sarawak, Malaysia; I. glandulosus Taylor, sured laterally; 2nd collar length (2CL), mea- 1923 from Basilan and Mindanao Islands, the sured laterally; head width (HW) at jaw angle; Philippines; I. mindanaoensis Taylor, 1960 maximum head width (MXHW); body width from Mindanao Island, the Philippines; and I. at middle (BWM); tail width at posterior vent monochrous (Bleeker, 1858) from Sarawak of (TAW); interorbital distance (IOD); intertenta- Malaysia, Kalimantan of Indonesia, and Bru- cle distance (ITD); internarial distance (IND); nei. The present Ichthyophis from Sabah has eye-nostril distance (END); eye-tentacle dis- a distinctive combination of morphological tance (ETD); tentacle-nostril distance (TND); characteristics that distinguishes it from the and eye-jaw angle distance (EJD). four known species, as well as all the other The following meristic characters were unstriped congeners with splenial teeth. We counted: total annuli (TA); annuli interrupted therefore describe this caecilian as a new by vent (VA); post-vent annuli (PVA); dorsal species. transverse grooves on 2nd collar (DTG); premaxillary-maxillary teeth (PMM); vomeropa- MATERIALS AND METHODS latine teeth (VP); dentary teeth (DE); splenial teeth (SP); and vertebrae (VER). The number Field surveys were made at the Sayap station of vertebrae was counted from a soft X-ray of Kinabalu National Park, Kota Belud photograph using Fuji Medical X-Ray Film district, Sabah, Malaysia in 2005 and 2006. (RX-U). Of the specimens collected, one adult was Since the single adult proved to be a male, sexed by direct observation of the phallodeum, its phallodeum was everted after anesthetiza- and larvae were ascertained by the presence of tion and fixed by 10% formalin injection. For gills and tail fin. The larval digestive organs describing the everted morphology of the were partly dissected in order to examine prey anterior phallodeum, we followed the termi- items. After tissues were taken for genetic nology of Gower and Wilkinson (2002) and analysis, specimens were fixed in 10% forma- Kupfer and Müller (2004). lin, transferred to 70% ethanol, and identified We examined the mitochondrial DNA genes by measuring and counting morphological of 12S rRNA and 16S rRNA and complete characters. The voucher specimens are stored cytochrome b from the male holotype together at the Graduate School of Human and Envi- with three congeneric species from Borneo ronmental Studies, Kyoto University (KUHE), and the Philippines. Methods of DNA prepa- and the Institute for Tropical Biology and ration and data analyses are as reported in Conservation, University Malaysia Sabah Nishikawa et al. (2012a). (BORN: BORNEENSIS). We measured the following morphometric SYSTEMATICS characters to the nearest 0.1 mm with a dial caliper following Nishikawa et al. (2012b): Ichthyophis lakimi sp. nov. total length (TL); head length (HL) from tip of Figs. 1–4 snout to first collar groove, measured dorsally; Ichthyophis monochrous: Inger, 1964, p. 46; trunk length (TRL) from first collar groove to 1966, p. 355 (part); Malkmus et al., 2002, p. posterior end of vent; tail length (TAL) from 219. posterior end of vent to tail tip; vent length Ichthyophis sp. 3: Nishikawa et al., 2012a, p. (VL); snout length (SL) from tip of snout to 716. jaw angle; lower jaw length (LJL) from tip of NISHIKAWA ET AL.—NEW CAECILIAN FROM SABAH, MALAYSIA 69

FIG. 1. Holotype of Ichthyophis lakimi sp. nov. (KUHE 38275) in dorsal (top), ventral (middle), and lateral (bottom) views. Scale=20 mm.

Diagnosis Park, about 30 km southeast from the city of Ichthyophis without lateral stripe and with Kota Belud, Kota Belud District, State of splenial teeth; body uniformly slate dorsally, Sabah, Malaysia (6°03'N, 116°33'E, 960 m slightly paler ventrally; total length of the asl), collected by Kanto Nishikawa and Paul single male 292.5 mm; TL/BWM ratio=30.2; Yambun, at 14:59 h on 29 November 2006. 349 annuli, six of which in tail; 48 premaxil- The GenBank accession numbers of mtDNA lary-maxillopalatine, 45 vomeropalatine, 41 sequences are AB686159 (12S rRNA and 16S dentary, 14 splenial teeth; TND/ETD ratio= rRNA) and AB686094 (cytochrome b). 1.9; scales from anteriormost 30th annuli to end of body; scales in one row except for two Paratypes rows in posteriormost 150 annuli. KUHE 38276 (one larva), same collection date and locality as the holotype; BORN Holotype 23334–23337 (four larvae), collected by Kanto KUHE 38275, an adult male (Figs. 1–4) Nishikawa at the same locality as the holotype from Sayap station of Kinabalu National on 13 August 2005. 70 Current Herpetol. 31(2) 2012

jaw angle and narrowing anteriorly; snout rounded anterior to tentacles, slightly longer (7.8) than lower jaw (6.8); intertentacle distance (6.1) larger than interorbital distance (5.4), which in turn is much larger than internarial distance (2.9); eyes slightly protruding, almost midway between top of head and edge of mouth in lateral view, slightly inset from edge of head in dorsal view; tentacles nearly twice as far from nostril than from eyes (TND/ETD=1.9); eye-jaw angle distance (3.0) larger than eye-tentacle distance (1.3) and tentacle-nostril distance (2.5); tentacles very close to edge of mouth, long and thin in life, tip slightly protruding from tentacular sheath in preservative; second collar (3.2) longer than first collar (2.7); nostrils round, positioned closely at anterior margin of mouth in dorsal and lateral views, invisible in ventral view. Collar region slightly wider than head and anterior body in dorsal and ventral views, not higher than head and anterior body in lateral view; first collar groove evident as constriction separating head and trunk, curving slightly anteriorly towards dorsal midline, where groove becomes incomplete and tips separated; second collar groove evident ventrally but not appar- ent dorsally, parallel to first groove laterally, fading out near lateral midline; third collar groove not clearly differentiated from anteriormost annular grooves of trunk and dorsal transverse groove on second collar, but recog- nized as first groove crossing lateral to ventral body; third groove dorsally complete, curving slightly anteriorly towards dorsal midline, but tips separated midventrally; one dorsal trans- FIG. 2. Holotype of Ichthyophis lakimi sp. nov. verse groove on left side of second collar. (KUHE 38275). From top to bottom: head and Annular count 349; annular grooves com- anterior body in dorsal, ventral, and lateral views; plete dorsally, but narrowly separate ventrally posterior body in ventral view. Scale=10 mm. except for posterior three-fifths of body; dorsally, annual grooves curving slightly anteriorly Description of holotype (measurements in mm) towards midline on anterior one-fourth of Moderate size (TL 292.5); body subcylindri- body and nearly orthoplicate on posterior cal, slightly depressed dorsoventrally, tapering three-fourths of body; ventrally, grooves posteriorly, more abruptly at about one-fifth strongly angulate posteriorly towards midline, of body, ending in blunt tail tip, lacking nipple- degree of curvature decreasing posteriorly to like terminal cap; head widened slightly around becoming orthoplicate at ca. one-tenth of NISHIKAWA ET AL.—NEW CAECILIAN FROM SABAH, MALAYSIA 71 body; scales found on posterior five-sixths of Teeth on premaxillary-maxillopalatine 48, body, increasing in size posteriorly, where vomeropalatine 45, dentary 41, splenial 14; number of rows is one in the anterior half and choanae elongated, about three times as long two in the posterior half. as broad, obliquely extending posterolaterally, Longitudinal vent surrounded by small and without a flap on edge. whitish subcircular disc; denticulations on vent Anterior phallodeum with a pair of blind unclear because of everted phallodeum; no sacs laterally and longitudinal ridges dorsolat- papillae on disc; six annuli each in vent slit erally, laterally, and ventrolaterally (Fig. 3); including denticulations, and in tail. ventrolateral longitudinal ridges smaller than

FIG. 3. Anterior phallodeum of holotype of Ichthyophis lakimi sp. nov. (KUHE 38275) in dorsal (top left), ventral (top right), left lateral (bottom left), right lateral (bottom right), and distal views (center). ebs: entrance of blind sac; eu: entrance of urodeum; l.dl: left dorsolateral longitudinal ridge; l.mdk: left mid- dorsal knob; l.vl: left ventrolateral longitudinal ridge; p.ldl: posterior tuberosity of l.dl; p.lvl: posterior tuberosity of l.vl; p.rl: posterior tuberosity of right lateral longitudinal ridge; p.rdl: posterior tuberosity of right dorsolateral longitudinal ridge; p.rvl: posterior tuberosity of right ventrolateral longitudinal ridge; r.dl: right dorsolateral longitudinal ridge; r.l: right lateral longitudinal ridge; r.vl: right ventrolateral longitudinal ridge. Scale=10 mm. 72 Current Herpetol. 31(2) 2012

FIG. 4. Holotype of Ichthyophis lakimi sp. nov. (KUHE 38275) in life. dorsolateral longitudinal ridges, but larger Larvae (measurements in mm) than right lateral longitudinal ridge; left lateral Large sized (TL=121.6–245.0 mm), body longitudinal ridge lacking; each longitudinal subcylindrical, slightly depressed dorsoven- ridge having a posterior tuberosity but lacking trally, tapering posteriorly, ending in short tail distinct anterior tuberosity; no mid-dorsal fin (tail fin length: from beginning of dorsal fin longitudinal ridge; mid-dorsal knob present to tip of tail 3.3–3.7, mean=3.5); head more only on left side. flattened than in metamorph, widened slightly around jaw angle and narrowing anteriorly; Color snout rounded, slightly longer (4.0–6.7, mean= In life, ground color of dorsum uniform 6.1) than lower jaw (3.1–6.0, mean=5.3); slate; slightly paler ventrally (Fig. 4); eye labial fold evident, especially in posterior two- surrounded by narrow whitish ring; tentacles thirds of upper jaw; interorbital distance (2.4– and surrounding tentacle aperture whitish; 4.9, mean=3.9) much larger than internarial vent disc whitish. In preservative, color faded distance (1.7–3.2, mean=2.7); eyes slightly but not obviously changed. protruding, closer to top of head than to edge of mouth in lateral view, slightly inset from Variation edge of head in dorsal view; collar indistinct, The larval paratypes, lacking tentacles and absent in smaller individuals; nostril elon- possessing gills and a tail fin, are similar to the gated, obliquely extending dorsolaterally in metamorph (holotype) in shape and color, but frontal view, positioned at anterior margin of are smaller in TL (121.6–245.0 mm) and TL/ mouth in ventral view, slightly apart from mar- BWM (20.6–24.7), and have a larger number of gin in lateral view, invisible in dorsal view. TA (354–374) than the holotype (292.5 mm, Annular count 354–374 (mean=362.0), 30.2, and 349, respectively). The larval paratypes tending to be indistinct in smaller individual; form three groups in TL: 240.8–245.0 mm annular grooves complete dorsally, but nar- (KUHE 38276 and BORN 23334), 195.1– rowly separate ventrally in several anterior- 198.0 mm (BORN 23335 and 23336), and most grooves; dorsally, annual grooves curving 121.6 mm (BORN 23337) (Table 1). Tail fins slightly anteriorly towards midline on anterior are greatly reduced in the large- and medium- one-tenth of body and nearly orthoplicate on sized groups. Collars are absent in the medium posterior nine-tenths of body; ventrally, grooves and small-sized groups. First collar groove is strongly angulate posteriorly towards midline, indistinct in the small-sized group. degree of curvature decreasing posteriorly to becoming orthoplicate at ca. one-fifth of body. NISHIKAWA ET AL.—NEW CAECILIAN FROM SABAH, MALAYSIA 73 le ID wak P0046 Mt. Mulu NP, Sara- NP, 67349 Lawas, Lawas, Lawas, FMNH FMNH Sarawak Kali- wang, Sinka- BMNH mantan 63.12.4.5* 50976 FMNH FMNH 50972 FMNH FMNH 50971 FMNH FMNH nd BORN, refer to the text. refer nd BORN, 50970 FMNH FMNH 50969 FMNH FMNH 50968 FMNH FMNH 50964 FMNH 50963 FMNH 50961 FMNH 50960 FMNH anao Mindanao Todaya, 50957 Mind- Davao, FMNH anao Mind- 50958* FMNH FMNH Todaya, Todaya, CAS losus mindanaoensis I. monochrous I. Abung 60073* Basilan Abung, I. glandu- ensis I. dulit- I. BMNH Sarawak 92.6.3.23* Mt. Dulit, Mt. Dulit, from Borneo and Philippines. *Data from original descriptions and Taylor (1968). BMNH: British from Borneo *Data from original Museum of Natural His- and Philippines. descriptions and Taylor 23337 BORN BORN 23336 Ichthyophis BORN BORN sp. nov. 23335 BORN BORN 23334 BORN BORN Ichthyophis lakimi Ichthyophis 38276 KUHE 38275 KUHE 1. Measurements of unstriped ABLE T TLHLTRLTALVL 292.5SL 12.6 245.0 275.8LJL 240.8 232.3S2CL13.38.911.1———13.2NA15.015.710.89.3—11.0——11.812.112.913.5NA12.113.0 4.1 8.3S3CL 198.0 227.7 2.01CL2.72.72.6———NANANA2.93.43.7—2.9——3.03.82.43.1NA3.03.6 195.1 4.4 184.6 9.22CL3.23.03.2———NANANA3.93.94.7—3.2——3.34.43.03.5NA3.44.9 7.8 6.8 121.6 182.5HW 2.3 3.9 17.5 9.7MXHW 6.7 235.0 5.8BWM 2.6 — 14.0 3.7 9.3TAW 6.7 250.0 6.0 218.4IOD 15.6 9.2 2.0 7.6 3.3ITD6.1—————NANANA7.3——————————NA5.47.6 276.0 — 6.6 231.3 14.7 9.7IND 5.9 8.4 316.0 1.5 7.5 2.7END 4.4 11.0 6.5 257.6 14.1 207.5ETD1.3—————1.51.31.52.1——————————1.01.71.9 9.9 5.8 9.0 5.4 1.4 7.8 297.7TND2.5—————NA3.53.63.7——————————2.53.13.1 180.1 3.7 5.6 12.5 4.0 9.4 10.6EJD 193.4 3.1 212.0 2.9 8.6 4.0 7.3 NA 3.7 4.0 167.2 216.5 12.0 17.0 9.6TA NA 6.2 2.9 NA 7.6 4.9 199.0 143.6VA666555NA4NA55445454344NA66 6.5 NA 2.5 4.0 13.0PVA664657NA6NA47656456654NA34 8.3 201.0 NA 141.4 NA 3.0 6.4 3.2 5.1 4.3DTG100000NANANA20000000000NA11 NA 4.1 2.7 2.9 203.8 8.9 NAPMM 5.9 20.0 — 2.1 349 5.3 NA 3.0 220.5 4.0VP 8.0 NA NA 2.7 2.5 7.7 2.2DE 21.8 228.0 374 8.0 1.7 — 8.1 5.2 2.5SP 25/23 2.4 7.2 223.0 2.3 14.5 9.1 2.0 NA 9.3VER NA 189.6 16/17 354 1.8 11.0 22/23 6.5 5.2 1.7 20/18 226.0 204.3 12.3 3.8 5.2 1.5 21/20 9.2 1.8TL/BWM 17/18 NA 18/18 NA 363 9.3 215.0 215.4 1.9 20/18TND/ETD1.9—————NA2.72.41.8——————————2.51.81.6 4.8 3.9 19/21 17.6 9.8 NA 18/18 3.8 7/7 251.0 210.1 1.9 20/19 30.2 5.8 10.4 — 111 19/18 9.1 365 3.4 16/16 NA 15.6 1.0 12.7 7.1 6.3 18/19 20/21 7/7 213.2 5.7 NA 24.7 111 1.9 18/18 354 8.7 19/19 7.6 16/18 — 11.4 6.0 NA 4.4 203.6 9.9 7.0 3.9 19/20 NA 22.7 7/7 23/23 4.9 110 23/23 NA 1.4 236.8 11.7 8.5 7.6 313 8.8 6.0 3.3 20/20 20.6 4.5 8.9 25/26 4.4 5.2 7/7 24/24 NA 110 4.0 15.4 3.0 1.4 22/21 9.8 21/21 7.7 9.5 4.3 23.5 273 3.1 24/24 4.2 8.7 3.5 7/7 5.4 18/17 16.0 111 2.9 17/18 NA 2.7 19/17 1.6 9.7 20.6 15/14 8.0 9.8 4.0 10.8 3.3 23/21 308 6/5 16.8 18/19 2.8 5.8 6.7 112 18/18 4.6 1.9 17/17 2.1 1.4 19/19 6.3 29.4 6.1 13/13 9.4 4.3 17.0 6.5 4.0 302 15/15 2.5 7.2 2.8 23/23 4/4 14/12 114 6.3 2.1 2.5 23/22 2.1 6.9 22/21 6.2 22.7 12/12 319 4.6 6.8 1.7 11/11 9.0 NA 3.1 15/15 7.5 3.5 17/18 14/13 6.0 1.7 102 2.4 2.2 16/15 8.3 15/15 7.5 294 28.2 14.8 3.3 15/15 9.4 2.8 9.4 8/8 2.8 7.1 15/15 19/21 3.8 6.2 23/23 2.0 2.0 24.9 111 17.2 332 8.8 17/17 7.8 NA 17/18 12.1 3.1 9.7 3.4 6/5 19/20 2.3 18/17 NA 20/23 2.0 21.0 1.3 115 2.0 NA 328 9/10 9.1 25/25 1.4 10.2 7.3 28/25 4.2 19/19 3.5 2.1 20.2 25/24 7.2 23/24 2.1 114 1.7 325 2.5 7.0 10.1 7/7 21/21 8.2 1.6 7.9 25/23 4.3 3.5 24.4 19/19 2.9 17/17 6.9 113 320 1.4 5/4 2.4 6.0 10.0 19/18 20/20 20.0 4.6 NA 7.0 2.8 3.2 16/17 116 333 6/6 2.0 2.4 9.1 22.1 6.9 4.7 7.2 NA 3.6 117 330 7/6 12.4 1.8 20.8 2.5 12.3 9.4 3.1 116 6.0 3.4 296 5/5 21.7 2.0 NA 112 336 4.2 22.7 5.5 5/6 NA 1.9 2.7 22.4 111 8/8 6.3 247 4.1 NA 2.8 22.1 118 9/9 294 4.3 2.4 114 22.6 7/7 311 23.6 2.6 113 4/4 20.2 109 2/2 108 2/3 106 tory, CAS: California Academy of Sciences, FMNH: Field Museum of Natural History, ID: Indraneil Das’s field number. For KUHE a For field number. California ID: Indraneil Das’s Academy of Sciences, FMNH: Field Museum Natural History, CAS: tory, Sex/AgeMorphometric Male Larva Larva Larva Larva Larva Unknown Male Unknown Female Larva Larva Larva Larva Larva Larva Larva LarvaMeristic Larva Larva Unknown Juvenile Ma Ratio TypesSpecimen No. Holotype Paratype Holotype Holotype Holotype Paratype Topotype Holotype Locality Sabah Kota Belud, Sayap, 74 Current Herpetol. 31(2) 2012

Scales found on posterior two-thirds of body, acuminatus, I. husaini, I. javanicus, I. laosen- increasing in size posteriorly, with number of sis, I. sikkimensis, I. sumatranus, and I. youn- rows one in the anterior half and two in the gorum by having a smaller number of splenial posterior half, absent in the smallest larva. teeth (SP=14 vs. 44 in I. acuminatus, 33 in I. Longitudinal vent surrounded by small and husaini, 24 in I. javanicus, 32 in I. laosensis, whitish subcircular disc; denticulations on vent 20 in I. sikkimensis 26 in I. sumatranus, and unclear, one or two on posterior end; no papillae 24 in I. youngorum); from I. billitonensis and on disc; five to six annuli in vent slit including I. singaporensis by having a larger number of denticulations, and four to seven in tail. splenial teeth (14 vs. two in I. billitonensis, Teeth on premaxillary-maxillopalatine 32–38 and six in I. singaporensis); from I. bombay- (mean=35.0), vomeropalatine 34–41 (37.4), ensis by having a smaller number of vertebrae dentary 37–39 (38.2), splenial 11–14 (13.4). (VER=111 vs. 121 in I. bombayensis); and Choanae elongated, about two and a half to from I. orthoplicatus by having angulate three times as long as broad, obliquely extending grooves on the ventral body (orthoplicate in I. posterolaterally, with a flap on proximal edge. orthoplicatus). In life, ground color of dorsum uniform Finally, the uncorrected pairwise sequence slate; slightly paler ventrally, except for the divergences in 2700 bp of mitochondrial genes smallest specimen showing pale slate dorsally of 12S rRNA and 16S rRNA and 1140 bp of and pale brown ventrally; eyes surrounded by complete cytochrome b between I. lakimi and wider whitish ring than in metamorph; vent the three congeners (I. biangularis, I. cf. min- disc and tail fin whitish. In preservative, color danaoensis, and Ichthyophis sp. from Borneo faded but not obviously changed. and the Philippines) are as large as 7.1–7.4% in 12S rRNA and 16S rRNA and 8.5–11.8% in Comparisons cytochrome b genes. Ichthyophis lakimi differs from other unstriped Ichthyophis with splenial teeth from Range Borneo and the Philippines in the following Known only from the type locality at a low way (data from Bleeker, 1858; Taylor, 1923, elevation on Mt. Kinabalu. 1960, 1968): from I. dulitensis by having a uniformly slate head (head lighter than body Natural history in I. dulitensis), larger number of splenial The type locality is in primary forest domi- teeth (SP=14 vs. eight in I. dulitensis), and nated by dipterocarps. The holotype was smaller number of vertebrae (VER=110–112 collected by digging about 50 mm in wet soil vs. 114 in I. dulitensis); from I. glandulosus by close to a small tributary (45–60 cm in width lacking a lateral ridge (strong lateral ridge in I. and 5–30 mm in depth) of the Kemantis River. glandulosus); from I. glandulosus by having The streambed was sandy and the water was the tentacles closer to the eyes (TND/ETD clear. Air, water, and soil temperatures at the ratio=1.9 vs. 2.4 in I. glandulosus); from I. time of collection of the holotype were 23.5, dulitensis, I. glandulosus, I. mindanaoensis, 19.5, and 20.5 C, respectively. Information on and I. monochrous by having a larger number breeding, hatchlings, and metamorphosis is of TA (349–374) and a smaller number of lacking. The larvae were found under stones scale rows (two) (TA≤336 and scale rows≥ or rotten logs in the shallows of the stream. three in I. dulitensis, I. glandulosus, I. mind- The larva ate arthropods like larval Ephe- anaoensis, and I. monochrous). menoptera and Trichoptera and earthworms. The new species differs from other unstriped The larval life may continue more than one Ichthyophis with splenial teeth in the follow- year before metamorphosis because several ing way (data from Taylor, 1960, 1965, 1968, size groups with great difference in body size 1969; Pillai and Ravichandran, 1999): from I. (the largest individual was more than twice as NISHIKAWA ET AL.—NEW CAECILIAN FROM SABAH, MALAYSIA 75 large as the smallest) were found at the same 2004). In order to assess the utility for species time. No predators of this species are known. identification in Ichthyophis, more information must be gathered for intra- and interspe- Etymology cific variation in phallodeum morphology for The species name honors Dr. Maklarin B. many congeners. Asymmetric morphology of Lakim who is in charge of the research division the phallodeum found in I. lakimi (absence of of Sabah Parks and has supported our survey. left lateral longitudinal ridge and right mid- dorsal knob) has never been detected in I. DISCUSSION glutinous, I. paucisulcus, I. peninsularis, or I. pseudangularis, whose phallodeum has been Mt. Kinabalu, the highest mountain in described (summarized in Taylor, 1968), or in Southeast Asia, encompasses various amphib- I. monochrous from Mulu National Park, ian habitats along its extensive altitudinal Sarawak, Malaysia (examined in this study: ID range up to ca. 4100 m asl. This geographical P0046 in Table 1). feature of Mt. Kinabalu produces a rich Larvae of I. lakimi grow up to 245 mm, and amphibian fauna with at least 77 known such large size is known only in larval I. species (Malkmus et al., 2002). The amphib- mindanaoensis (up to 238 mm: Taylor, 1960) ian inventory study at Mt. Kinabalu began in from the montane region in Mindanao Island, the 1850s and precedes most other regions in the Philippines. Based on molecular data, Southeast Asia. However, caecilian diversity Matsui et al. (2010a, b) found that montane beyond doubt remains incompletely surveyed frog species of the genera Ansonia and Lepto- even on this well-surveyed mountain. In addi- brachium from Mt. Kinabalu and Mindanao tion to the new caecilian species described Island to form a clade, and suggested a past here, Nishikawa et al. (2012a) reported the geohistorical connection between these two presence of two more unidentified caecilians areas. Ichthyophis lakimi and I. mindan- from this mountain. aoensis are similar in terms of their large Ichthyophis lakimi is known only from larval size and unstriped adult body, but this Mt. Kinabalu. Ichthyophis monochrous from similarity is not ascribed to a phylogenetically 914 m asl (Inger, 1964) and Sungei (=River) close relationship. On the phylogenetic tree Kipungit (Malkmus et al., 2002), and a larval from mitochondrial DNA, the two species specimen of unstriped caecilian from 580 m (also all unstriped species examined) do not asl at Sungei Mamut deposited at the Field form a clade and paraphyly of unstriped Museum of Natural History (FMNH 130925, species is indicated (Nishikawa et al., 2012a). K. Nishikawa personal observation) probably Consequently, large larval size in I. lakimi and represent this new species. The elevations of I. mindanaoensis might have resulted from these localities are rather high compared with convergence associated with a possible long other Bornean records, where all known larval life in cool mountain streams on Mt. caecilians were reported from lowlands (Tay- Kinabalu and Mindanao Island. In order to lor, 1968) except for I. dulitensis from 610 m understand their phylogenetic relationship and (Taylor, 1960). In order to know the correct estimate the evolution of larval life history in distribution range of I. lakimi, further field Bornean and Philippine caecilians, more surveys must be conducted in mountain areas samples, especially from the Philippines, are adjacent to Mt. Kinabalu, such as the Crocker needed. Range. Descriptions of phallodeum morphology are ACKNOWLEDGMENTS rare for Ichthyophis, and taxonomic utility of the morphology remains unevaluated (Gower We thank Maryati Mohamed and Ahmad and Wilkinson, 2002; Kupfer and Müller, Sudin (ITBC, University Malaysia Sabah) and 76 Current Herpetol. 31(2) 2012

Maklarin B. Lakim and Jamili Nais (Sabah INGER, R. F. 1966. The systematics and zoogeogra- Parks) for permitting and supporting our phy of the Amphibia of Borneo. Fieldiana: research, Tomohiko Shimada for supporting Zoology 52: 1–402. our field surveys, and Maryati Mohamed and KUPFER, A. AND MÜLLER, H. 2004. On the taxon- Ahmad Sudin (BORN), Harold Voris and omy of ichthyophiid caecilians from southern Alan Resetar (FMNH), and Indraneil Das Thailand: a reevaluation of the holotype of (Universiti Malaysia Sarawak) for allowing us Ichthyophis supachaii Taylor, 1960 (Amphibia: to borrow specimens under their care. This Gymnophiona: Ichthyophiidae). Amphibia- research was conducted under research per- Reptilia 25: 87–97. missions from the Economic-Planning Unit of MALKMUS, R., MANTHEY, U., VOGEL, G., HOFFMANN, Malaysia to K. Nishikawa (Nos. 1193 and P., AND KOSUCH, J. 2002. Amphibians and 1792) and M. Matsui (Nos. 1192 and 1793), Reptiles of Mount Kinabalu (North Borneo). A. and supported by Grants-in-Aids from the R. G. Gantner Verlag, K. G., Ruggell. Japan Society for the Promotion of Science to MATSUI, M., TOMINAGA, A., LIU, W., KHONSUE, K. Nishikawa (No. 17405018) and M. Matsui W., GRISMER, L. L., DIESMOS, A. C., DAS, I., (Nos. 15370038 and 20405013) and from the SUDIN, A., YAMBUN, P., YONG, H. S., SUKUMARAN, Shikata Memorial Trust for Nature Conserva- J., AND BROWN, R. M. 2010a. Phylogenetic tion to K. Nishikawa. relationships of Ansonia from Southeast Asia inferred from mitochondrial DNA sequences: LITERATURE CITED Systematic and biogeographic implications (Anura: Bufonidae). Molecular Phylogenetics BLEEKER, P. 1858. Bestuursvergadering, gehouden and Evolution 54: 561–570. ten huize van den heer Dr Bruijn Kops den 11n MATSUI, M., HAMIDY, A., MURPHY, R. W., KHONSUE, Maart 1858. Natuurkundig Tijdschrift voor W., YAMBUN, P., SHIMADA, T., AHMAD, N., Nederlandsch Indië 16: 183–192. BELABUT, D. M., AND JIANG, J.-P. 2010b. FROST, D. 2011. Amphibian Species of the World: Phylogenetic relationships of megophryid frogs an Online Reference. Version 5.5 (31 January, of the genus Leptobrachium (Amphibia, Anura) 2011). Electronic Database accessible at http// as revealed by mtDNA gene sequences. Molecu- research. Amnh.org/herpetology/amphibian/ lar Phylogenetics and Evolution 56: 259–272. index.html. American Museum of Natural His- NISHIKAWA, K., MATSUI, M., YONG, H.-S., tory, New York, U.S.A. AHMAD, N., YAMBUN, P., BELABUT, D. M., GOWER, D. J., KUPFER, A., OOMMEN, O. V., SUDIN, A., HAMIDY, A., ORLOV, N. L., OTA, H., HIMSTEDT, W., NUSSBAUM, R. A., LOADER, S. P., YOSHIKAWA, N., TOMINAGA, A., AND SHIMADA, PRESSWELL, B., MÜLLER, H., KRISHNA, S. B., T. 2012a. Molecular phylogeny and biogeogra- BOISTEL, R., AND WILKINSON, M. 2002. A phy of caecilians from Southeast Asia (Amphibia, molecular phylogeny of ichthyophiid caecilians Gymnophiona, Ichthyophiidae), with special (Amphibia: Gymnophiona: Ichthyophiidae): out reference to high cryptic species diversity in of India or out of South East Asia? Proceedings Sundaland. Molecular Phylogenetics and Evo- of the Royal Society B 296: 1563–1569. lution 63: 714–723. GOWER, D. J. AND WILKINSON, M. 2002. Phallus NISHIKAWA, K., MATSUI, M., AND ORLOV, N. L. morphology in caecilians (Amphibia, Gym- 2012b. A new striped Ichthyophis (Amphibia: nophiona) and its systematic utility. Bulletin of Gymnophiona: Ichthyophiidae) from Kon Tum the Natural History Museum, London (Zoology) Plateau, Vietnam. Current Herpetology 31: 28– 68: 143–154. 37. INGER, R. F. 1964. Royal society expedition to PILLAI, R. S. AND RAVICHANDRAN, M. S. 1999. North Borneo 1961: Report 8, Amphibia. Gymnophiona (Amphibia) of India. A taxo- Proceedings of the Linnean Society of London nomic study. Records of the Zoological Survey 175: 45–46. of India. Occasional Paper 172: 1–117. NISHIKAWA ET AL.—NEW CAECILIAN FROM SABAH, MALAYSIA 77

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