Babina lini (Chou, 1999) and Hylarana menglaensis fei, ye et xie, 2008, two additional anuran species for the herpetofauna of Vietnam

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Two ranid species, Babina lini and Hylarana menglaensis, are recorded for the first time from Vietnam on the basis of a new amphibian collection from Dien Bien and Son La provinces. In addition, acoustic analyses of these species are also provided based on the advertisement calls recorded in Muong Nhe Nature Reserve of Dien Bien Province.

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Nội dung Text: Babina lini (Chou, 1999) and Hylarana menglaensis fei, ye et xie, 2008, two additional anuran species for the herpetofauna of Vietnam

Russian Journal of Herpetology Vol. 21, No. 4, 2014, pp. 315 – 321 Babina lini (CHOU, 1999) AND Hylarana menglaensis FEI, YE ET XIE, 2008, TWO ADDITIONAL ANURAN SPECIES FOR THE HERPETOFAUNA OF VIETNAM Dzung Trung Le,1 Anh Van Pham,1,2 Son Hung Lan Nguyen,1 Thomas Ziegler,3 and Truong Quang Nguyen4 Submitted October 10, 2014. Two ranid species, Babina lini and Hylarana menglaensis, are recorded for the first time from Vietnam on the ba- sis of a new amphibian collection from Dien Bien and Son La provinces. In addition, acoustic analyses of these species are also provided based on the advertisement calls recorded in Muong Nhe Nature Reserve of Dien Bien Province. Keywords: Babina lini; Hylarana menglaensis; new records; advertisement calls; Dien Bien Province; Son La Province INTRODUCTION and Copia Nature Reserves (Son La Province), Vietnam in November 2012, June 2013, July 2013, October 2013, Rana lini Chou, 1999 and Hylarana menglaensis Fei, February 2014, June 2014, and September 2014 (Fig. 1). Ye et Xie, 2008 were originally described from Yunnan Specimens were collected from 19:00 to 24:00. After tak- Province, China (Chou, 1999; Fei et al., 2008). Rana lini ing photographs specimens were anaesthetized in a was transferred to the genus Nidirana by Chen et al. closed vessel with a piece of cotton wool containing ethyl (2005) and subsequently placed in the genus Babina by acetate, fixed in 85% ethanol and subsequently stored in Frost et al. (2006). Both species were found at high eleva- 70% ethanol. Specimens were deposited in the Museum tions from 1000 to 1400 m above sea level and presum- of Biology, Hanoi National University of Education ably to be found in upland areas of northwestern Vietnam (HNUE), Hanoi and Tay Bac University (TBU), Son La (Chou, 1999; Fei et al., 2008; Frost, 2014). Province, Vietnam. We herein report two new records of Babina lini and Morphological examinations. Measurements were H. menglaensis from montane evergreen forests of Dien taken with a digital caliper to the nearest 0.1 mm. Abbre- Bien and Son La provinces, Vietnam. Comparison of morphological data and acoustic analyses of Vietnamese specimens and specimens from neighboring countries are also presented. MATERIAL AND METHODS Sampling: Field surveys were conducted in Muong Nhe Nature Reserve (Dien Bien Province) and Sop Cop 1 Faculty of Biology, Hanoi National University of Education, 136 Xuan Thuy, Cau Giay, Hanoi, Vietnam. 2 Faculty of Biology and Chemistry, Tay Bac University, Quyet Tam Ward, Son La City, Son La Province, Vietnam. 3 AG Zoologischer Garten Köln, Riehler Strasse 173, D-50735 Köln, Germany. 4 Institute of Ecology and Biological Resources, Vietnam Academy Fig. 1. Map showing the survey sites in northwestern Vietnam: of Science and Technology, 18 Hoang Quoc Viet Road, Hanoi, 1, Muong Nhe Nature Reserve in Dien Bien Province; 2, Copia; 3, Sop Vietnam; e-mail: nqt2@yahoo.com Cop nature reserves in Son La Province. 1026-2296/2014/2104-0315 © 2014 Folium Publishing Company
316 Dzung Trung Le et al. ger length, from articulation of proximal and intermedi- ate phalange; FL, thigh length, from vent to knee; FOL, foot length, from base of inner metatarsal tubercle to tip of fourth toe; FTL, fourth toe length, from articula- tion of proximal and intermediate phalange; IMT, length of inner metatarsal tubercle; ITL, inner toe length; TL shank length; TW maximum shank width; a.s.l., above sea level. For webbing formula we followed Glaw and Vences (2007). Acoustic analysis. Advertisement calls were re- corded with a Sony Recorder ICD-UX200F and a Para- bolic microphone Telinga Pro-4PIP. Calls were recorded A at a distance of approximately 0.2 m and ambient temper- atures at the calling site were taken immediately after re- cording using an electronic thermal hygrometer Nakata NJ-2099-TH. Calls were analyzed by using Raven Pro, version 1.3 (Cornell Laboratory of Ornithology, Ithaca, NY, USA) at resolution of 16 bit and frequency of 44.1 kHz. Spectrograms were performed with Hann win- dow type, frame length of 1024 samples, and correspond- ing 3 dB filter bandwidth of 67.4 Hz; frame overlapped 50% with time-grid resolution of 512 samples and fre- quency-grid resolution of 46.9 Hz. For each acoustic sig- nal, the following parameters were measured: call dura- tion or call length(s): duration of time between beginning and end of a call; call repetition rate (calls/sec): (total number of calls – 1)/duration of time between beginning B of the first call and end of the last call; inter-call inter- val(s): duration of time between end of the first call and Fig. 2. Babina lini from Son La Province, Vietnam (TBU PAE.386, beginning of the second call; number of notes per call: to- adult male): A, dorsolateral view; B, ventral view. tal number of notes in a call; number of pulses per note: total number of pulses within a note (in some cases); dominant frequency of call (kHz): the emphasized har- viations are as follows: SVL, snout-vent length; EL, eye monic in the spectrum (after Duellman and Trueb, 1994; length, from anterior corner to posterior corner of eye; Cocroft and Ryan, 1995). The first 10 notes of each call EN, distance from anterior corner of eye to posterior edge were removed according to research by Pröhl (2003). of nostril; HL, head length, from posterior corner of man- We calculated the coefficients of variation (CV = dible to tip of snout; HW, maximum head width at the an- = [SD/mean] × 100%) of the acoustic features measured gle of jaws; IFE, distance between anterior corners of in calls. We employed the criteria of Gerhardt (1991) and eyes; IPE, distance between posterior corners of eyes; classified as static those acoustic properties with average IN, internarial distance; IUE, minimum distance between within individual CV < 5% and dynamic those with upper eyelids; MBE, distance from posterior corner of CV > 12%, and CV from 5 – 12% was intermediate level mandible to posterior corner of eye; MFE, distance from of within-individual variation. posterior corner of mandible to anterior corner of eye; MN, distance from posterior corner of mandible to poste- rior edge of nostril; NS, distance from anterior edge of RESULTS nostril to tip of snout; SL, distance from anterior corner of eye to tip of snout; TYD, maximum tympanum diame- Taxonomic accounts Babina lini (Chou, 1999) ter; TYE, distance between anterior margin of tympanum Lin’s Montane Frog (Figs. 2 and 3) and posterior corner of eye; UEW, maximum width of upper eyelid; FLL, forearm length, from elbow to base of Specimens examined. Dien Bien Province: nine outer palmar tubercle; HAL, hand length, from base of specimens collected by D. T. Le, B. V. Nguyen and outer palmar tubercle to tip of third finger; TFL, third fin- N. T. Bui in the Pama stream (22°18.717¢ N 102°18¢ E,
New Records of Ranid Frogs from Vietnam 317 elevation 995 m a.s.l.), Leng Su Sin sector, Muong Nhe 30 A Nature Reserve: three adult males HNUE MNA.134, 20 135, 137 and two adult females HNUE MNA.105, 136, 10 kU collected on 13 June 2013; one adult male HNUE 0 MNA.185, collected on 17 October, 2013; three adult –10 males HNUE MNA.281, 360, 449, collected on 25 –20 February 2014. Son La Province: four specimens col- –30 lected by A. V. Pham and T. V. Nguyen within Sop Cop 4 Nature Reserve, near Tup Pha B Village (20°58.19¢ N B kHz 3 103°40.652¢ E, elevation 1260 m a.s.l.), Huoi Mot Com- 2 mune, Song Ma District: two adult males TBU PAE.381, 386 and two adult females TBU PAE.385, 388, collected 1 on 12 July 2013. 0.2 0.4 0.6 0.8 1 1.2 1.6 1.8 Morphological characters of specimens from Dien Time, sec Bien and Son La provinces agreed well with the descrip- Fig. 3. Advertisement call of Babina lini (HNUE MNA.136, male): tion of Chou (1999) and Chuaynkern et al. (2010). A, a 1.8-sec waveform of relative amplitude; B, corresponding 1.8-sec Body elongate (SVL 49.8 – 59.5 mm in males, n = 9 spectrogram. and 55.1 – 60.8 mm in females, n = 4). Head longer than wide (HL 18.9 – 23.9 mm, HW 16.4 – 21.8 mm, HL/SVL 0.38 – 0.41, HW/SVL 0.32 – 0.37 in males; swollen; subarticular tubercle formula 1, 1, 2, 2; palmar HL 21 – 23.1 mm, HW 18.3 – 19.8 mm, HL/SVL 0.37 – tubercles two, oval. 0.39, HW/SVL 0.31 – 0.34 in females); snout rounded, Hindlimbs slightly robust, long, thigh shorter than projecting beyond upper jaw (SL 7.7 – 9.3 mm in males tibia (FL 26.3 – 33.8 mm, FL/TL 0.88 – 0.98, FL/SVL and 8.7 – 9.7 mm in females), longer than horizontal 0.5 – 0.57 in males and FL 29.1 – 34.7 mm, FL/TL diameter of eye (EL 6 – 7.5 mm, SL/EL 1.2 – 1.48 in 0.83 – 0.95, FL/SVL 0.53 – 0.57 in females); tibia ap- males and EL 6.3 – 6.7 mm, SL/EL 1.32 – 1.54 in fe- proximately five times longer than wide (TL 29.8 – males); nostril lateral, closer to the tip of snout than to 4.4 mm, TW 6 – 7.5 mm in males and TL 34.3 – eye (IN 5.2 – 6.4 mm, NS 3.9 – 4.4 mm, EN 4 – 4.9 mm, 36.5 mm, TW 6.7 – 7.8 mm in females), shorter than dis- NS/EN 0.87 – 0.98 in males and IN 5.8 – 6.4 mm, NS tance from base of internal metatarsal tubercle to tip of 3.2 – 4.5 mm, EN 4.5 – 5.3 mm, NS/EN 0.68 – 0.85 in toe IV (FOL 31.5 – 35.7 mm in males and 33.6 – females); loreal region concave, interorbital space flat, 36.1 mm in females); toes slender, relative toe lengths broader than upper eyelid (IUE 4.1 – 5.6 mm in males I < II < V < III < IV; tips of toes swollen; webbing for- and 4.9 – 5.6 mm in females; UEW 3.2 – 4.1 mm in mula I1 – 11/3II2/3 – 2III1 – 2IV2 – 2/3V; inner metatar- males and 3.5 – 3.9 mm in females); anterior interorbital sal tubercle distinct, shorter than length of toe I (IMT distance about 70 – 80% of posterior interorbital distance 1.5 – 2 mm in males and 1.8 – 1.9 mm in females, ITL (IFE 7.7 – 9.7 mm in males and 9.7 – 10.1 mm in fe- 3.4 – 5 mm in males and 4.8 mm in females); subarticu- males, IPE 11 – 13.3 mm in males and 12.9 – 13.9 mm in lar tubercles oval, formula 1, 1, 2, 3, 2. females); tympanum distinct, round (TYD 3.8 – 4.8 mm Skin smooth dorsally, with small spinules scattered in males and 4.1 – 5 mm in females, TYD/EL 0.6 – 0.73 on posterior half; dorsolateral folds distinct, from behind in males and 0.61 – 0.79 in females); tympanum-eye dis- the eye to groin; flanks granular; spinules present around tance (TYE 1.1 – 2 mm in males and 1.6 – 1.8 mm in fe- cloaca; glandular ridge behind base of forelimb, triangu- males), about 40% of tympanum diameter; tongue large, lar, smooth, large; dermal folds long, thin, irregular on notched posteriorly; vomerine teeth present, equal in dis- dorsal surfaces of limbs; venter smooth. tance from each other as to choanae. Coloration in life. Eyes blackish brown; irises hori- Forelimbs moderately robust (FLL 9.3 – 11.6 mm, zontally elliptical, black; loreal region dark brown; tym- FLL/SVL 0.18 – 0.2 in males; FLL 10.4 – 12.8 mm, panum blackish brown; dorsal surface of head and body FLL/SVL 0.19 – 0.21 in females), shorter than the length dark brown with gray irregular vertebral stripe, pale of hand (HAL 12.7 – 16.2 mm in males and brown near dorsolateral folds; spots large, black, scat- 14.3 – 16.3 mm in females); relative finger lengths II < tered on flanks, more densely near dorsolateral folds; I < IV < III; third finger long and slender (TFL 6.7 – dorsal surface of forelimbs with black spots; thigh and 8.9 mm in males and 7.5 – 9.5 mm in females); fingers tibia with black crossbars; venter cream; vocal sacs without dermal fringe, free of webbing; tips of fingers blackish brown.
318 Dzung Trung Le et al. of 4 – 6 notes, lasting for 1.24 – 2.053 sec (1.474 ± 0.315 sec, n = 10), call repetition rate 0.069 – 0.076 calls/sec (0.073 ± 0.005, n = 2), inter-call interval 6.811 – 29.499 sec (15.520 ± 7.082, n = 8), delivered at a rate of 0.311 – 0.344 notes/sec (0.327 ± 0.024, n = 2). Each note consisted of multipulse (n = 45). The dominant frequency of the primary calls ranged from 2.153 to 3.015 kHz (2.678 ± 0.343 kHz, n = 10). Rise time of calls (mean CV = 21.37%), call repetition rate (mean CV = 6.85%), inter-call interval (mean CV = 45.63%) and dominant frequency (mean CV = 12.8%) were the most stereotyped properties. The result showed call rate, dominant frequency can be considered static properties, A while rise time and inter-call interval can be considered dynamic properties. Advertisement calls of the Vietnamese specimens are relatively similar to those from China in having a series of 4 – 6 indistinct fast-pulsed notes, lasting for 1.24 – 2.053 sec (vs. most calls consisted of 3 – 7 notes lasting 1.2 – 2.8 sec) and lengths of inter-call intervals not being constant. However, the Vietnamese specimens have the dominant frequency from 2.153 to 3.015 kHz (vs. 1.44 – 2.68 kHz) (see Chou, 1999). Hylarana menglaensis Fei, Ye et Xie, 2008 Mengla Frog (Figs. 4 and 5) Specimens examined. Dien Bien Province: five B specimens collected by D. T. Le and B. V. Nguyen from Muong Nhe Nature Reserve: two adult males HNUE Fig. 4. Hylarana menglaensis (HNUE MNA.484, adult male) from MNA.339, 345, collected on 25 February 2014, one Dien Bien Province, Vietnam: A, dorsolateral view; B, ventral view. adult male HNUE MNA.26 and one adult female HNUE MNA.138, collected on 13 June 2013, near the Pama stream of Leng Su Sin sector (22°18.717¢ N Remarks. Specimens from Vietnam differ from Chi- 102°18.250¢ E, elevation 995 m a.s.l.), one adult female nese specimens in having a larger eye in males (EL 6.5 ± HNUE MNA.484, collected on 5 June 2014, near the Y 0.5 mm vs. 5.7 ± 0.6 mm) and a narrower upper eyelid in females (UEW 3.7 ± 0.2 mm vs. 4.7 ± 0.3 mm) (see Ma Ho stream of Sin Thau sector (22°20.583¢ N Chou 1999). The Vietnamese specimens also differ from 102°12.317¢ E, elevation 1455 m a.s.l.). Son La Prov- Thai and Laotian specimens in having a larger size in ince: three specimens collected by A. V. Pham and T. V. males (SVL 54.8 ± 3.7 mm vs. 45.4 ± 1.9 mm) (see Nguyen: one adult female TBU PAE.89, collected on 22 Chuaynkern et al., 2010). October 2012 within Copia Nature Reserve, near Pha Ecological notes. Specimens were found in puddles Khuong Village, Co Ma Commune, Thuan Chau District of small streams with slow flowing water, from 20:00 to (21°21.598¢ N 103°31.223¢ E, elevation 1240 m a. s. l); 24:00. The surrounding habitat was mixed secondary for- one adult male TBU PAE.220 and one adult female TBU est of small hard wood and shrub. PAE.199, collected on 6 November 2012 within Sop Cop Distribution. This species was previously known NR, near Nam Cong River, Ta Co Village, Sop Cop Com- only from China, Laos and Thailand (Chou, 1999; mune (21°0.266¢ N 103°36.481¢ E, elevation 1080 m Chuaynkern et al., 2010). a.s.l.). Acoustic properties. Calls emitted by two males Additional frogs were encountered during our field (HNUE MNA.105, 136) from Muong Nhe Nature surveys in September 2014: two adult females in Muong Reserve were recorded at an air temperature of 21°C Nhe Nature Reserve (Dien Bien Province): one near Su and a relative humidity of 88%. The calls were composed Sin Village (22°19.658¢ N 102°20.907¢ E, at an elevation
New Records of Ranid Frogs from Vietnam 319 30 A 20 10 kU 0 –10 –20 –30 4 B kHz 3 2 Fig. 5. Advertisement call of Hylarana menglaensis (HNUE MNA.484, adult 1 male): A, a 3-sec waveform of relative amplitude; B, corresponding 3-sec spectro- 0.2 0.4 0.6 0.8 1 1.2 1.6 1.4 1.8 2 2.2 2.4 2.6 2.8 3 gram. Time, sec of 589 m) on 10 September, another one near Nam Po in females); tympanum distinct, round (TYD 3 – 3.4 mm Village (22°09.031¢ N 102°26.633¢ E, at an elevation of in males, 3.2 – 4.1 mm in females), approximately two 931 m) on 12 September; two adult males and one adult third of eye diameter (TYD/EL 0.62 – 0.67 in males and female in Copia Nature Reserve (Son La Province) near 0.6 – 0.75 in females); tympanum-eye distance (TYE Pha Khuong Village, Co Ma Commune (21°21.160¢ N 1.3 – 1.5 mm in males, TYE 1.8 – 2.2 mm in females); 103°31.225¢ E, at an elevation of 1270 m) on 14 Septem- vomerine teeth present, in two oblique ridges, equal in ber; one adult male and one adult female in Sop Cop Na- distance from each other as to choanae; tongue notched ture Reserve (Son La Province) near Kha Village, Pung posteriorly; males with vocal sac openings at corners of Banh Commune (21°00.453¢ N 103°26.02¢ E, at an ele- mouth. vation of 1200 m) on 20 September. Forelimbs slender, short (FLL 8.8 – 9.7 mm, Morphological characters of specimens from Dien FLL/SVL 0.21 – 0.23 in males; FLL9.3 – 11.1 mm, Bien and Son La agreed well with the description of Fei FLL/SVL 0.2 – 0.23 in females), about three quarters of et al. (2008) (see Table 1). the hand length (HAL 11.2 – 12.8 mm in males, HAL Body slender, females bigger than males (SVL 11.7 – 13.1 mm in females); relative finger lengths 38.9 – 44.9 mm in males, n = 4 and 44.1 – 49.3 mm in II < I < IV < III; tips of all four fingers swollen; fingers females, n = 4). Head longer than wide (HL 16.2 – without dermal fringe, free of webbing; subarticular tu- 17.1 mm, HW 14.4 – 15.7 mm, HL/SVL 0.37 – 0.42, bercle formula 1, 1, 2, 2; palmar tubercles two, oval; HW/SVL 0.32 – 0.37 in males; HL 17 – 18.1 mm, HW males with nuptial pad on finger I. 14.4 – 16.6 mm, HL/SVL 0.38 – 0.39, HW/SVL Hindlimbs long, thigh shorter than tibia (FL 0.33 – 0.34 in females); snout obtusely pointed in dorsal 19.6 – 22 mm, FL/TL 0.89 – 0.97, FL/SVL 0.49 – 0.5 in view, projecting beyond upper jaw, round in profile (SL males; FL 21.2 – 24.4 mm, FL/TL 0.89 – 0.94, FL/SVL 5.6 – 6.1 mm in males and 5.6 – 6.5 mm in females), lon- 0.48 – 0.49 in females); tibia approximately six times ger than horizontal diameter of eye (EL 4.8 – 5.3 mm, longer than wide (TL 21.9 – 24.6 mm, TW 4.2 – 4.5 mm SL/EL 1.09 – 1.2 in males and EL 5.2 – 5.8 mm, SL/EL in males and TL 23.6 – 25.9 mm, TW 3.8 – 5.2 mm in fe- 1.02 – 1.25 in females); nostril lateral, round, closer to the tip of snout than to eye (IN 3.6 – 4.8 mm, NS 2.5 – males), longer than distance from base of internal meta- 3.1 mm, EN 2.9 – 3.6 mm, NS/EN 0.86 – 0.89 in males tarsal tubercle to tip of toe IV (FOL 20.8 – 23.4 mm in and IN 4 – 4.8 mm, NS 2.3 – 3.2 mm, EN 3.2 – 3.8 mm, males and FOL 22.8 – 24.9 mm in females); toes thin, NS/EN 0.68 – 0.84 in females); canthus rostralis dis- relative toe lengths I < II < III < V < IV; tips of toes tinct, loreal region oblique, shallowly concave, interorbi- swollen; webbing formula I0 – 1II1/3 – 1III1/2 – 1IV1 – tal space flat, broader than upper eyelid (IUE 3.8 – 0V; inner metatarsal tubercle distinct (IMT 1.6 mm in 4.7 mm in males and 4 – 4.5 mm in females; UEW 2.6 – males, 1.3 – 1.5 mm in females), outer metatarsal tuber- 3.5 mm in males, 2.7 – 3.8 mm in females); anterior in- cle distinct, round; subarticular tubercles oval, formula 1, terorbital distance about 67% of posterior interorbital 1, 2, 3, 2. distance (IFE 6.1 – 7.5 mm in males and 6.8 – 8.3 mm in Dorsal surface of body and thighs, and flanks scat- females; IPE 9.5 – 11.4 mm in males and 9.9 – 12.4 mm tered granulars; humeral gland present in males; supra-
320 Dzung Trung Le et al. tympanic fold absent; dorsolateral fold weakly devel- (SL 5.9 ± 0.2 mm vs. 6.7 mm), a narrower upper eyelid oped; ventral surface smooth. (UEW 2.9 ± 0.4 mm vs. 3.8 mm) and a smaller tympa- Coloration in life. Eyes blackish brown, irises hori- num diameter (TYD 3.3 ± 0.2 mm vs. 3.8 mm) (see Fei zontally elliptical, black; loreal region dark brown; tym- et al., 2008). panum blackish brown; dorsal surface of head and body Ecological notes. Specimens were found both in day grayish brown to brown, dorsum with small black spots; time and at night, from 11:00 to 24:00, in the puddles of flanks with larger spots, more dense near dorsolateral rocky streams in secondary forest. folds; dorsal surface of forelimbs, thighs and tibiae Distribution. This species was previously reported with black crossbars; ventral surface cream; vocal sacs from Yunnan Province, China (Fei et al., 2008; Frost, blackish brown. 2014). Remarks. Specimens from Vietnam differ from Chi- Acoustic properties. Calls emitted by the male nese specimens in having a shorter snout in males (HNUE MNA.484) from Muong Nhe Nature Reserve TABLE 1. Measurements (in mm) and Proportions of Babina lini and Hylarana menglaensis from Vietnam Babina lini Hylarana menglaensis Character min – max mean ± SD min – max mean ± SD min – max mean ± SD min – max mean ± SD (n = 9x) (n = 9x) (n = 4}) (n = 4}) (n = 4x) (n = 4x) (n = 4}) (n = 4}) SVL 49.8 – 59.5 54.8 ± 3.7 55.1 – 60.8 57.6 ± 2.6 38.9 – 44.9 43.3 ± 3 44.1 – 49.3 46.7 ± 2.6 HW 16.4 – 21.8 18.2 ± 1.7 18.3 – 19.8 18.9 ± 0.7 14.4 – 15.7 14.8 ± 0.6 14.4 – 16.6 15.6 ± 1.1 HL 18.9 – 23.9 21.4 ± 1.6 21 – 23.1 22.1 ± 0.9 16.2 – 17.1 16.6 ± 0.4 17 – 18.5 17.8 ± 0.8 MN 14.8 – 19 17.5 ± 1.3 17.3 – 19 18.3 ± 0.8 13.5 – 15.1 14.6 ± 0.7 15.3 – 16.1 15.7 ± 0.4 MFE 10.5 – 14.6 13.5 ± 1.3 12.9 – 14.9 14.1 ± 0.9 10.6 – 12 11.4 ± 5.7 11.8 – 12.4 12.2 ± 0.3 MBE 6.2 – 9 8.1 ± 1.0 7.2 – 9.2 8.3 ± 0.9 5.8 – 6.7 6.3 ± 0.4 7 – 7.8 7.3 ± 0.4 IFE 7.7 – 9.7 8.9 ± 0.7 9.7 – 10.1 9.9 ± 0.2 6.1 – 7.5 6.9 ± 0.6 6.8 – 8.3 7.4 ± 0.7 IPE 11 – 13.3 12 ± 0.7 12.9 – 13.9 13.4 ± 0.4 9.5 – 11.4 10.3 ± 0.8 9.9 – 12.4 11.2 ± 1.0 IN 5.2 – 6.4 5.8 ± 0.4 5.8 – 6.4 6.1 ± 0.3 3.6 – 4.8 4.1 ± 0.5 4 – 4.8 4.4 ± 0.3 EN 4 – 4.9 4.5 ± 0.3 4.5 – 5.3 4.9 ± 0.4 2.9 – 3.6 3.4 ± 0.3 3.2 – 3.8 3.5 ± 0.3 EL 6 – 7.5 6.5 ± 0.5 6.3 – 6.7 6.5 ± 0.2 4.8 – 5.3 5.1 ± 0.2 5.2 – 5.8 5.4 ± 0.3 TYD 3.8 – 4.8 4.3 ± 0.4 4.1 – 5 4.5 ± 0.5 3 – 3.4 3.3 ± 0.2 3.2 – 4.1 3.7 ± 0.4 TYE 1.1 – 2 1.6 ± 0.3 1.6 – 1.8 1.7 ± 0.1 1.3 – 1.5 2.1 ± 0.5 1.8 – 2.2 1.9 ± 0.2 NS 3.9 – 4.4 4.2 ± 0.2 3.2 – 4.5 3.9 ± 0.6 2.5 – 3.1 2.9 ± 0.3 2.3 – 3.2 2.7 ± 0.4 SL 7.7 – 9.3 8.7 ± 0.5 8.7 – 9.7 9.2 ± 0.4 5.6 – 6.1 5.9 ± 0.2 5.6 – 6.5 5.9 ± 0.4 IUE 4.1 – 5.6 4.8 ± 0.5 4.9 – 5.6 5.3 ± 0.3 3.8 – 4.7 4.4 ± 0.4 4 – 4.5 4.2 ± 0.2 UEW 3.2 – 4.1 3.6 ± 0.3 3.5 – 3.9 3.7 ± 0.2 2.6 – 3.5 2.9 ± 0.4 2.7 – 3.8 3.2 ± 0.5 FLL 9.3 – 11.6 10.5 ± 0.9 10.4 – 12.8 11.6 ± 1.0 8.8 – 9.7 9.2 ± 0.4 9.3 – 11.1 9.9 ± 0.8 HAL 12.7 – 16.2 14.7 ± 1.2 14.3 – 16.3 15.5 ± 0.9 11.2 – 12.8 12.1 ± 0.7 11.7 – 13.1 12.2 ± 0.6 TFL 6.7 – 8.9 8.1 ± 0.8 7.5 – 9.5 8.7 ± 0.9 6.1 – 7 6.5 ± 0.4 6.3 – 7.3 6.7 ± 0.4 TL 29.8 – 34.4 31.4 ± 1.7 34.3 – 36.5 35.5 ± 0.9 21.9 – 24.6 23.3 ± 1.2 23.6 – 25.9 24.8 ± 1.1 FOL 31.5 – 35.7 33.2 ± 1.3 33.6 – 36.1 34.9 ± 1.0 20.8 – 23.4 22.2 ± 1.1 22.8 – 24.9 23.7 ± 0.9 FL 26.3 – 33.8 29.1 ± 2.5 29.1 – 34.7 31.4 ± 2.6 19.6 – 22 21.3 ± 1.1 21.2 – 24.4 22.6 ± 1.5 FTL 19.6 – 22 20.7 ± 0.9 21.8 – 22.3 22.1 ± 0.2 13 – 13.5 13.3 ± 0.2 13.4 – 15.2 14 ± 0.8 IMT 1.5 – 2 1.8 ± 0.2 1.8 – 1.9 1.8 ± 0.0 1.6 1.6 ± 0.0 1.3 – 1.5 1.4 ± 0.1 ITL 3.4 – 5 4.6 ± 0.5 4.8 4.8 ± 0.0 2.9 – 3.8 3.6 ± 0.4 3.6 – 4.1 3.9 ± 0.2 TW 6 – 7.5 6.7 ± 0.5 6.7 – 7.8 7.4 ± 0.5 4.2 – 4.5 4.3 ± 0.1 3.8 – 5.2 4.8 ± 0.6 HL/SVL 0.38 – 0.41 0.39 ± 0.01 0.37 – 0.39 0.38 ± 0.01 0.37 – 0.42 0.38 ± 0.02 0.38 – 0.39 0.38 ± 0.01 HW/SVL 0.32 – 0.37 0.33 ± 0.02 0.31 – 0.34 0.33 ± 0.01 0.32 – 0.37 0.34 ± 0.02 0.33 – 0.34 0.33 ± 0.01 SL/EL 1.2 – 1.48 1.34 ± 0.09 1.32 – 1.54 1.42 ± 0.10 1.09 – 1.20 1.15 ± 0.04 1.02 – 1.25 1.1 ± 0.10 NS/EN 0.87 – 0.98 0.93 ± 0.04 0.68 – 0.85 0.79 ± 0.08 0.86 – 0.89 0.87 ± 0.01 0.68 – 0.84 0.77 ± 0.09 TYD/EL 0.6 – 0.73 0.67 ± 0.05 0.61 – 0.79 0.69 ± 0.09 0.62 – 0.67 0.64 ± 0.02 0.6 – 0.75 0.68 ± 0.07 FLL/SVL 0.18 – 0.2 0.19 ± 0.01 0.19 – 0.21 0.20 ± 0.01 0.21 – 0.23 0.21 ± 0.01 0.2 – 0.23 0.21 ± 0.01 FL/TL 0.88 – 0.98 0.92 ± 0.04 0.83 – 0.95 0.88 ± 0.06 0.89 – 0.97 0.91 ± 0.04 0.89 – 0.94 0.91 ± 0.02 FL/SVL 0.5 – 0.57 0.53 ± 0.03 0.53 – 0.57 0.54 ± 0.02 0.49 – 0.5 0.49 ± 0.01 0.48 – 0.49 0.48 ± 0.01 Note. SD, standard deviation, for other abbreviations see Material and Methods.
New Records of Ranid Frogs from Vietnam 321 were recorded at an air temperature of 23.4°C and a rela- Field research in northwestern Vietnam was funded by the tive humidity of 93%. The calls were composed of single National Geographic Society (Grant No. 9492-14). Research of note, lasting for 0.127 – 0.201 sec (0.159 ± 0.0. 17 sec, T. Q. Nguyen was partially supported by the Alexander von n = 20), call repetition rate 0.327 calls/sec (n = 1), inter- Humboldt Foundation (VIE 114344). call interval 1.54 – 10.616 sec (3.052 ± 2.015, n = 19). Each note consisted of multipulse (n = 20). The dominant REFERENCES frequency of the primary calls ranged from 0.517 to 2.412 kHz (1.701 ± 0.846, n = 20). Rise call duration Chen L.-Q., Murphy R. W., Lathrop A., Ngo A., Orlov N. (mean CV = 10.69%), inter-call interval (mean CV = L., Ho C. T., and Somorjai I. (2005), “Taxonomic chaos in = 66.02%) and dominant frequency (mean CV = Asian ranid frogs: an initial phylogenetic resolution,” Her- = 49.74%) were the most stereotyped properties. The re- petol. J., 15, 231 – 243. sult showed only call duration can be considered static Chou W.-H. (1999), “A new frog of the genus Rana (Anura: properties. Ranidae) from China,” Herpetologica, 55(3), 389 – 400. Chuaynkern Y., Ohler A., Inthara C., Duengkae P., Mak- chai S., and Salangsingha N. (2010), “A revision of spe- DISCUSSION cies in the subgenus Nidirana Dubois, 1992, with species attention to the identity of species allocated to Rana adeno- The genus Babina currently comprises 10 species pleura Boulenger, 1909, and Rana chapaensis (Bourret, (Frost, 2014). Based on morphological, morphometrical 1937) (Amphibia: Anura: Ranidae) from Thailand and and behavioral characters, Chuaynkern et al. (2010) as- Laos,” Raffles Bull. Zool., 58(2), 291 – 310. signed Babina lini to the Rana adenopleura group. This Cocroft R. B. and Ryan M. J. (1995), “Patterns of adverti- group contains two other species: B. adenopleura (Bou- sement call evolution in toads and chorus frogs,” Anim. lenger) from Taiwan and B. caldwelli (Schmidt) from Behav., 49, 283 – 303. China. Whereas the second known species of the genus Duellman W. E. and Trueb L. (1994), Biology of Amphibians, The Johns Hopkins Univ. Press. Babina from Vietnam, B. chapaensis (Bourret), was Fei L., Ye C.-Y., Jiang J.-P., and Xie F. (2008), “Two new placed in the Rana okinavana group, together with species of the Ranidae from China, with phylogenetic rela- B. daunchina (Chang) from China and B. okinavana tionships of Hylarana (Sylvirana) nigrovittata group (Am- (Boettger) from Japan (Chuaynkern et al., 2010). phibia, Anura),” Acta Zootaxon. Sinica, 33(1), 199 – 206. Hylarana is one of the most diverse genera of the Frost D. R. (2014), Amphibian Species of the World: an family Ranidae with 84 currently recognized species on-line reference. Version 6.0. Accessed in February 2014 (Frost, 2014). H. menglaensis and H. hekouensis, both at http://research.amnh.org/herpetology/amphibia. Ameri- species described by Fei et al. (2008), were previously can Museum of Natural History, New York, USA. confused with H. nigrovittata. Therefore further studies Frost D. R., Grant T., Faivovich J., Bain R. H., Haas A., are required to verify the actual distribution of this spe- Haddad C. F. B., de Sá R. O., Channing A., Wilkin- cies, particularly in northwestern Vietnam and northeast- son M., Donnellan S. C., Raxworthy C. J., Camp- ern Laos. bell J. A., Blotto B. L., Moler P. E., Drewes R. C., Nuss- baum R. A., Lynch J. D., Green D. M., and Whee- Acknowledgments. We are grateful to the directorates of ler W. C. (2006), “The amphibian tree of life,” Bull. Am. the Muong Nhe Nature Reserve (Dien Bien Province), Copia Mus. Nat. Hist., 297, 1 – 370. and Sop Cop nature reserves (Son La Province) for support of Gerhardt H. C. (1991), “Female mate choice in treefrogs: our field work and issuing relevant permits. We thank N. T. Bui, static and dynamic acoustic criteria,” Anim. Behav., 42, B. V. Nguyen (HNUE), C. T. Pham (IEBR), H. N. Ngo 615 – 635. (VNMN), T. V. Nguyen, and H. V. Tu (TBU) for their assistance Glaw F. and Vences M. (2007), A Field Guide to the Amphib- in the field. Thanks to E. Sterling (New York, NY, USA) and K. ians and Reptiles of Madagascar. Third Edition, Frosch Koy (Berkeley, CA, USA) for providing the map. Research of Verlag, Cologne. D. T. Le was supported by the Hanoi National University of Pröhl H. (2003), “Variation in male calling behaviour and rela- Education (Small Grant No. SPHN-13-247). Field equipment tion to male mating success in the Strawberry Poison Frog was supported by the Idea Wild to D. T. Le and A. V. Pham. (Dendrobates pumilio ),” Ethology, 109, 273 – 290.