Tropical Natural History 18(1): 40–53, April 2018 2018 by Chulalongkorn University Taxonomic Status of the Endemic Andaman Bullfrog Kaloula baleata ghoshi Cherchi, 1954 (Anura: Microhylidae) with Notes on Distribution and Natural History SUMAITHANGI RAJAGOPALAN CHANDRAMOULI* AND KATTUPUTHUR VENKATARAMAN DEVI PRASAD Department of Ecology and Environmental Sciences, School of Life Sciences, Pondicherry University, Pondicherry, INDIA * Corresponding author. Sumaithangi Rajagopalan Chandramouli ([email protected]) Received: 6 June 2017; Accepted: 13 October 2017 ABSTRACT.– Taxonomic status of the Andamanese subspecies of Kaloula baleata i.e., Kaloula baleata ghoshi is re-evaluated based on a comparative analysis of morphological data from members of this species complex from different parts of Southeast Asia. The Andamanese population is shown to be a morphologically distinct, allopatric species deserving specific recognition similar to the recently recognized and named members of this species complex from other parts of Southeast Asia. Thus, the population in the Andaman Islands hitherto considered being a subspecies of Kaloula baleata is elevated to species status in the combination Kaloula ghoshi. Descriptive notes on morphology, distribution and natural history of this poorly known taxon are presented herein for the first time based on extensive field-surveys conducted in the Andaman Islands. KEY WORDS: Kaloula, Andaman Islands, species complex, subspecies, elevation, allopatry, Java INTRODUCTION group (consisting of K. verrucosa, K. borealis, K. rugifera and K. nonggangensis) Kaloula Gray, 1831 is a group of and the kalingensis group (consisting K. robustly built, Southeast Asian Microhylid kalingensis, K. kokacii, K. picta, K. walteri, frogs that are known from Northeastern K. rigida and K. conjuncta) (Fei et al., 2009; India in the West to the Lesser Sunda Mo et al. 2015). Two more members, Islands in the east. In a recent phylogenetic Kaloula aureata and K. mediolineata are study by Peloso et al. (2015), taxonomic known from Thailand and adjacent parts of status of the genus has been reassessed and Indochina, whose affinities are not known. the Indo-Ceylonese taxon taprobanica Of these, members of the Kaloula baleata which was attributed to Kaloula earlier (e.g. group and verrucosa group have been Dutta, 1997, Sengupta et al., 2009) has been subjected to several phylogenetic studies in shown to be a member of the Uperodon the recent past, highlighting the high degree clade and has thus been transferred. of cryptic diversity within the species Currently, 17 species are known within this complex (Blackburn et al., 2013; Chan et genus (Frost, 2017). Morphologically, al., 2013; Chan et al., 2014; Mo et al., members of Kaloula can be divided into the 2013), leading to the recognition of a few following species groups: the baleata group new taxa, some of which have recently been (consisting of K. baleata, K. indochinensis described. Very recently, Chan et al. (2013) and K. latidisca), pulchra group (consisting remarked on the uncertain taxonomic status K. pulchra and K. assamensis), verrucosa of Kaloula baleata ghoshi known from CHANDRAMOULI AND DEVI PRASAD — ENDEMIC ANDAMAN BULLFROG TAXONOMIC STATUS 41 South and Little Andaman Islands. This (IO, shortest distance between dorso-medial taxon was described by Cherchi (1954) margins of orbits), inter-narial distance (IN, based on two specimens collected by L. shortest distance between dorsal margins of Cipriani from River Tciongare, Little nostrils), upper arm length (UAL, on the Andaman Island. On-going fieldwork in the dorsal surface from the axilla to the elbow), Andaman Islands led to the documentation lower arm length (LAL, on the dorsal of this taxon from several areas within these surface from the posterior margin of the islands. In this paper, taxonomic status of elbow to the base of the outer metacarpal the Andamanese population regarded as a tubercle), palm length (PAL, from the subspecies of Kaloula baleata till now, is posterior border of the outer metacarpal reassessed, whereby, it shown to be a tubercle to tip of the longest finger), femur morphologically distinct, allopatric lineage length (FEL, from the anterior margin of the deserving specific recognition. hind limb at its insertion point on the body to the knee), tibia length (TBL, from the posterior surface of the knee to the base of MATERIALS AND METHODS the heel), foot length (FOL, from heel to tip of longest toe), inner metatarsal tubercle Field surveys were carried out in the length (IMTT). Characters were compared following islands: Little Andaman, South against other species, and specifically, Andaman, Rutland, Middle Andaman, Long against Kaloula indochinensis (recently Island and North Andaman during February named and geographically closest – June 2015 and July 2017. Specimens of population of the Kaloula baleata species the target species sighted were captured, complex) from Vietnam, K. latidisca from gently restrained and measured. Three dead Peninsular Malaysia, and those from the individuals encountered during the surveys type locality (Java) of the nominal taxon were collected, preserved in 70% ethanol Kaloula baleata. Measurements of type and are deposited at the Department of specimens of Kaloula indochinensis from Ocean Studies and Marine Biology Vietnam and K. latidisca from Malay (DOSMB), Pondicherry University. The Peninsula were used from their original following measurements were taken from descriptions (Chan et al., 2013; 2014). both preserved and live specimens: snout– Measurements of the syntypes of Kaloula vent length (SVL, from tip of snout to baleata housed at the Natural History anterior margin of cloaca), head length (HL, Museum, London were obtained from Bryan from posterior edge of mandible to tip of L. Stuart. A subset of the above snout), head width (HW, maximum width of measurements (HL, HW, ED, ES, IO, IN, head at the angle of the jaws), head depth FEL and TBL) from male specimens were (HD, maximum depth of head), eye standardized to SVL and subjected to diameter (ED, the greatest horizontal multivariate morphometric analyses. diameter of the orbit), eye–nostril distance Principal component analysis and (EN, from anterior border of orbit to middle hierarchical cluster analysis were carried out of nostril), eye–snout distance (ES, from using the software package PAST (Hammer anterior border of orbit to tip of snout), et al., 2000) to investigate the grouping of upper eyelid width (UEW, maximum width populations from different regions (i.e., of the upper eyelid), interorbital distance Andaman Islands, Vietnam, Peninsular 42 TROPICAL NATURAL HISTORY 18(1), April 2018 TABLE 1. Factor loadings of the PCA. Maximum loadings for each character in bold. Character PC 1 PC 2 PC 3 HL 0.46 -0.04 -0.14 HW 0.46 0.04 -0.36 ES 0.36 -0.23 0.57 ED 0.19 0.48 -0.50 IO 0.04 0.53 0.43 IN 0.48 -0.08 0.07 FEL -0.21 0.55 0.13 TBL 0.37 0.34 0.26 Eigenvalue 3.74 2.41 0.83 % variance 46.80 30.10 10.37 Cumulative 46.80 76.90 87.27 Malaysia and Java). Juvenile specimens of this species observed in stagnant puddles were excluded from the analysis. Resulting on the ground were collected and reared for factor scores from the PCA were plotted to observation of growth pattern followed by examine the distribution of specimens in release at the same site. Larval staging multivariate morphological space for follows Gosner (1960). Measurements of interpretation of the results, which were the larvae were done to the nearest independently verified using hierarchical millimetre from photographs with a scale cluster analysis, by building a UPGMA placed nearby, using AdobeTM Photoshop dendrogram from standardised morpho- version CS3. The following measurements metric dataset. Morphological comparisons were recorded: total length, head-body were made with the syntypes of Kaloula length, head-body width, tail length, head- baleata; those of the other congeners are body height and inter-orbital distance. based on original descriptions and published Colour descriptions of the tadpoles were literature. One specimen (DOSMB 05040) made based on the photographs recorded in was also radiographed to examine skeletal life. Later, they were released back at the characters and its osteology is described. site of initial observation. The distribution map of these taxa was prepared in ARC MAP v.10 based on RESULTS survey locations recorded using GarminTM GPS MAP 78s (WGS84 datum). Calls of the PCA conducted based on the target species were recorded using the abovementioned standardized measure- digital audio recorder application in a ments, extracted three factors, which, Samsung Duos G 130 E model mobile together, explained 87.27 % of variation, phone and analysed using the software observed between samples from the packages AdobeTM Soundbooth version CS3 Andaman Islands, Vietnam, peninsular and Adobe Audition version 1.5. Tadpoles CHANDRAMOULI AND DEVI PRASAD — ENDEMIC ANDAMAN BULLFROG TAXONOMIC STATUS 43 FIGURE 1. Plot of principal component analysis showing morphological distinction of Kaloula ghoshi from other congeners of the K. baleata complex. Solid black squares represent topotypes Malaysia and Java. Of these, the first factor Kaloula ghoshi Cherchi, 1954 explained by cephalic and limb dimensions stat. nov. (Fig. 3A – E) accounted for 46.8% of variation and the Kaloula baleata ghoshi Cherchi, 1954 second factor, explained by inter-orbital Kaloula pulchra ghoshi (sic!) – Das (1994: distance and thigh length accounted for 45) 30.1% of variation; the third factor, Kaloula baleata (non Bombinator baleatus explained by eye size and snout length, Müller, 1836) – Das et al. (2004: 105, 109) accounted for 10.37% of variation (Table 1). part The first two factors with eigenvalues more Kaloula baleata ghoshi – Das & Dutta than one were plotted against each other. (1998); Das (1999); Chandramouli et al. The factor scores plotted in Figure 1 (2015: 49 – 52) separated the Andamanese, Javan, Kaloula baleata goshi (sic!) – Chan et al. Vietnamese and Peninsular Malaysian (2013: 329); Chan et al. (2014: 569) populations out into discrete groups. Similarly, the hierarchical cluster analysis Type material. Two female syntypes, resulted in four distinct clusters, each of measuring 43.5 and 39.0 mm SVL, collected which corresponds to the abovementioned by L. Cipriani in March 1952 from River four populations respectively (Fig. 2). Based Tciongare in Little Andaman Island and on these results of morphometric analyses deposited at MSNG, Museo Civico di Storia and the allopatric distribution, specific Naturale, Genova, Italy. status is hereby conferred to the Andaman population as: 44 TROPICAL NATURAL HISTORY 18(1), April 2018 FIGURE 2. UPGMA dendrogram of hierarchical cluster analysis based on standardised measurements of the K. baleata complex. * indicates live, uncollected specimens Material examined. Kaloula ghoshi – indochinensis, K. latidisca and K. DOSMB 05040, DOSMB 05041, DOSMB nonggangensis); presence of two 05042 – Hut Bay, Little Andaman Island – subarticular tubercles under the fourth toe coll. S.R. Chandramouli – July 2017 (vs. three in K. baleata); absence of osseous Differential diagnosis and comparisons. tubercles on the dorsal surface of third (Tables 2, 3) fingers (vs. present in Kaloula Kaloula ghoshi is diagnosed and can be nonggangensis, verrucosa and rugifera); differentiated from currently recognized presence of a conspicuous, horizontally congeners by the combination of following elongate outer metatarsal tubercle (vs. characters: Large body size (mean SVL indistinct in Kaloula conjuncta, K. females – 59.41 mm, males – 51.1 mm) (vs. kalingensis); well-developed but incomplete smaller adult size; 24.5 – 31.5 mm in toe webbing reaching the ante-penultimate Kaloula walteri; 37.0 – 43.0 mm in Kaloula subarticular tubercle on 4th toe (vs. complete kokacii); presence of horizontally expanded in Kaloula nonggangensis; rudimentary in discs on fingers and smaller discs on toes K. kalingensis, K. picta, K. rigida and K. (vs. finger discs not expanded in borealis, mediolineata). Kaloula ghoshi differs from pulchra, picta, verrucosa, mediolineata, Kaloula aureata Nutphand, 1989, K. walteri, rigida and rugifera); absence of pulchra and K. assamensis by its bright coloured inguinal and axillary colouration: dorsum brown with a triangular blotches (vs. present in K. baleata, K. grey patch on the middle and a dark grey CHANDRAMOULI AND DEVI PRASAD — ENDEMIC ANDAMAN BULLFROG TAXONOMIC STATUS 45 FIGURE 3. Lateral (A) and dorsal (B) views of an adult male Kaloula ghoshi Cherchi, 1954 from Little Andaman Island (type locality); foot (C); palm (D) and dorsal body (E) of Kaloula ghoshi; Dorsal (F) and ventral (G) views of a syntype BMNH 1947.2.10.69 of K. baleata from Java (arrows point at the bright inguinal blotch) venter with white speckled markings in aureata; dull olive brown dorsum with Kaloula ghoshi (vs. golden brown dorsum distinct longitudinal stripes in Kaloula with yellow markings and white venter in K. assamensis and dark brown dorsum with 46 TROPICAL NATURAL HISTORY 18(1), April 2018 TABLE 2. Morphological variation between Kaloula ghoshi and other members of the K. baleata complex (mm). Values of p ≤ 0.05 in bold. K. ghoshi (Andaman) K. baleata U (p) K. latidisca (pen. U (p) K. indochinensis (Vietnam) U (p) n = 9 (Java) Malaysia) n = 7 n = 2 n = 3 M (7) F (2) M (2) M (3) M (5) F (2) SVL 37.4-59.73 40.07-59.41 40.7-42.0 49.2-54.4 46.2-50.3 46.5-52.9 (51.1±7.53) (49.74±13.6) (41.4±0.91) (52.5±2.89) (48.06±1.91) (49.7±4.2) HL:SVL 0.24-0.28 0.25 0.23-0.26 6.5 0.28-0.37 5.5 0.23-0.24 0.24-0.27 13 (0.26±0.02) (0.25±0) (0.25±0.02) (0.62) (0.34±0.05) (0.15) (0.24±0) (0.26±0.02) (0.04) HW:SVL 0.31-0.36 0.26 0.31-0.33 8.5 0.33-0.37 5 0.29-0.31 0.31-0.36 30.5 (0.34±0.01) (0.26±0) (0.32±0.01) (1) (0.35±0.02) (0.13) (0.3±0.01) (0.34±0.03) (0.95) ES:HL 0.28-0.42 0.32-0.35 0.38 8 0.43-0.45 0 0.41-0.44 0.41 5.5 (0.37±0.05) (0.34±0.02) (0.38±0) (0.9) (0.45±0.01) (0.01) (0.42±0.01) (0.41±0) (0.006) ED:HL 0.38-0.47 0.36-0.38 0.44-0.48 3.5 0.29-0.33 0 0.27-0.37 0.29-0.32 1 (0.44±0.03) (0.37±0.02) (0.46±0.03) (0.22) (0.31±0.02) (0.01) (0.31±0.04) (0.31±0.02) (0.001) IO:HL 0.44-0.52 0.36-0.38 0.48-0.49 7.5 0.35-0.43 4 0.46-0.5 0.44-0.46 30 (0.48±0.03) (0.37±0.01) (0.49±0.01) (0.81) (0.4±0.04) (0.09) (0.48±0.02) (0.45±0.02) (0.91) IN:HL 0.27-0.34 0.24-0.26 0.19-0.21 0 0.35-0.43 0 0.22-0.29 0.27-0.29 16 (0.3±0.02) (0.25±0.02) (0.2±0.01) (0.04) (0.4±0.04) (0.01) (0.26±0.03) (0.28±0.01) (0.1) FEL:SVL 0.33-0.39 0.43 0.31-0.35 0.5 0.38-0.43 6.5 0.33-0.39 0.37-0.42 7.5 (0.37±0.02) (0.43±0) (0.33±0.03) (0.05) (0.41±0.03) (0.2) (0.37±0.02) (0.39±0.03) (0.01) TBL:SVL 0.32-0.35 0.38 0.31 2 0.34-0.39 7.5 0.32-0.35 0.35-0.37 8 (0.34±0.01) (0.38±0) (0.31±0) (0.12) (0.36±0.02) (0.3) (0.34±0.01) (0.36±0.02) (0.01) yellow dorsolateral bands and a yellow- (UAL:LAL – 0.76); palm longer than lower white venter in Kaloula pulchra). arm, two distinct metacarpal tubercles Description. (based on the examined live present at the base of the palm, inner one and preserved specimens; Table 4) slender and elongate; outer larger and heart- A large species of Kaloula (mean SVL – shaped. Fingers free of webbing; finger-tips 50.8 mm); with a depressed and rounded broadened to discs with a flat anterior end; habitus. Head large (HL:SVL – 0.25); relative length of fingers – IV>III>II>I. broader than long (HL:HW – 0.78); snout Thigh a little less than half the length of the with a flattened anterior tip, not projecting body (FEL:SVL – 0.43); shank shorter than beyond mandible. Eyes large and the thighs (TBL:SVL – 0.38). Toes with protruding; a little less than half the length broadened discs at the terminus; their of the head (ED:HL – 0.42) and slightly relative lengths – IV>III>V>II>I. Webbing longer than the snout (ES:ED – 0.86). on toes moderate: webbing formula: I 0.5- Canthus rostralis short but well-defined; II III IV V. Inner metatarsal tubercle 1 0.5-1.5 1-2 2-1 nostrils closer to the snout tip than to eyes. vertically elongated; outer metatarsal Inter-narial region flat, inter-orbital region tubercle smaller than inner, but horizontally slightly concave; inter-narial distance less elongated; tarsal ridge absent. than inter-orbital distance (IN:IO – 0.64). Skin smooth to feebly pustular dorsally; Upper eyelids half as broad as inter-orbital with small granules situated along the distance. A weak, indistinct supra-tympanic dorso-lateral region; venter perfectly smooth fold commencing from post orbital region and glossy; gular region with larger fails to reach the mandible; tympanum granules, especially in the vocal sacs of hidden. Upper arm longer than lower arm males. CHANDRAMOULI AND DEVI PRASAD — ENDEMIC ANDAMAN BULLFROG TAXONOMIC STATUS 47 TABLE 3. Comparison of morphological traits between members of the Kaloula baleata species complex (mm) (+ indicates presence and – indicates absence of the character). Kaloula ghoshi Kaloula baleata Kaloula latidisca Kaloula indochinensis Mean SVL+SD 50.8+8.14 41.35+0.91 53.5+2.89 48.52+2.54 Range (n) 40.07-59.73 (9) 40.7-42.0 (2) 49.2-54.4 (3) 46.2-52.9 (7) Expanded finger + + + + discs Inguinal blotches – + + + Axillary blotches – + + + Subarticular 2 3 3 2 tubercles under toe 4 Toe webbing I II I II I II I II 0.5–1 0.5–1.5 0.5–1 0.5–2 1–2 1–3 1–1 1–2 III IV V III IV V III IV V III IV V 1–2 2–1 1–2 2–1 2–3.5 4–2 0.5–1 3–1 Variation. Sexual size dimorphism not a certain extent, it also occurs close to pronounced (largest male SVL 59.73; human habitation. This was observed in largest female SVL – 59.41). Large, smooth southern parts South and Little Andaman nuptial pads present at the base of the dorsal Islands. Kaloula ghoshi was observed to use surface of the first finger in males (vs. tree holes at a height of upto 7ft above the absent in females); gular vocal sac indicated ground level as a refuge for roosting. by dark colour and granular skin texture in Courtship and breeding activities commence males (vs. absent in females). with the onset of southwest monsoon by late Colouration in life.Dorsum bight orange- May and last till the end of the monsoon in brown with dark brown flanks and a large September. Sporadic showers during the dark brown hourglass shaped marking in the post-monsoon period were found to trigger middle, extending from the inter-orbital intermittent calling and courtship activities region till the groin, broadening posteriorly; in this species. Males call from puddles and venter light grey with white marbled pattern. other such stagnant water bodies on the Lateral regions with two dark grey bands, ground (Fig. 4A). Females are about as large each running along the flanks from sides of as males and amplexus in this species is the snout till the groin. Gular vocal sac dark axillary (Fig. 4B). Eggs of dull grey colour grey coloured in males. Limbs bear dark are laid in clumps in shallow, stagnant water grey bands. No bright spots on the axillary bodies (Fig. 4C). Xenochrophis tytleri and inguinal regions in both males and (Blyth, 1863) was observed in the breeding females. pools of this taxon and could be a potential Natural history. It is nocturnal, semi- predator. arboreal in habits and can often be seen on Description of call. (Fig. 5) The call the ground among leaf litter, surface of tree described here was recorded from a trunks and in tree holes in primary topotypical male in Hut Bay, Little evergreen, secondary and littoral forests. To Andaman Island on 12 May 2015 at 2130 h 48 TROPICAL NATURAL HISTORY 18(1), April 2018 TABLE 4. Measurements of Kaloula ghoshi from the Andaman Islands and K. baleata syntypes (BMNH) from Java (in bold). * indicates live, uncollected specimens Sex SVL HL HW ES ED IO IN FEL TBL DOSMB 05040 M 37.4 10.47 12.89 4.33 4.6 5.14 3.21 16.27 16.07 South Andaman* M 45.89 11.29 15.17 3.14 4.34 5.49 3.11 15.95 12.83 DOSMB 05041 M 49.85 14.09 17.69 4.69 6.16 6.18 3.85 22.78 19.8 Middle Andaman* M 53.1 12.94 18.46 4.74 6.12 6.73 4.35 24.43 19.9 Middle Andaman * M 55.3 14.4 19.2 5.99 6.02 6.87 4.31 21.35 21.5 North Andaman* M 56.44 13.36 20.3 5.41 6.33 6.91 4.35 27.18 23.18 DOSMB 05042 M 59.73 14.36 18.38 5.61 6.33 6.36 4.13 25.4 22.08 Rutland* F 59.41 15.1 15.5 5.3 5.78 5.68 3.99 25.84 22.73 South Andaman* F 40.07 10.02 10.42 3.21 3.61 3.61 2.40 17.23 15.23 BMNH1947.2.10.69 M 42.0 10.8 13.8 4.1 4.7 5.2 2.1 14.9 13.0 BMNH1947.2.10.70 M 40.7 9.5 12.6 3.6 4.6 4.7 2.0 12.5 12.8 at an ambient air temperature of 29.1°C. slender than coracoids. Humerus broader Calls of Kaloula ghoshi consist of a series proximally, narrower distally; longer than of pulses uttered in succession within radio-ulna. Finger tips with widely duration of 55 s. Calls were composed of expanded terminal phalanges; phalangeal five notes, each of which comprise of 7 – 25 formula – 2-2-3-3. Sacral vertebra of the pulses, with syllables resembling the sound pelvic girdle well developed with widely of a grunt. Mean amplitude of the call was dilated sacral diapophysis; ilia long; -8 db with a dominant frequency of 1 kHz. extending a little beyond the level of the Each pulse lasted for a mean duration of 0.4 sacral diapophysis; urostyle long; lacking s (range: 0.32 – 0.64 s), with the inter-pulse lateral dilations or expansions. Femur longer interval ranging between 0.24 – 0.53 s than tibiofibula; tarsus shorter than the foot; (mean 0.3 s). phalangeal formula of the toes – 2-2-3-4-3; Osteology: based on DOSMB 05040. terminal phalanges expanded, but relatively (Fig. 6) Skull broader than long; narrower than finger tips. frontoparietals broad and robust with a Larval description.– Larvae of Kaloula median suture; nasals relatively short; ghoshi of stage 33 are described in this orbital cavity large; longer than broad; section. The tadpoles measure about 11 mm maxillae and vomers edentate; vertebra in total length (range: 10.58 – 11.23 mm; bears seven presacal vertebrae, of which the mean – 10.93±0.29). Head-body nearly last three are relatively larger. Pectoral rounded in shape when viewed dorsally, girdle firmisternal in architecture; coracoids slightly longer than broad (HBL:HBW – non-overlapping; very robust with widely 1.23) and broader than deep (HBW:HBH- expanded proximal and distal ends with a 1.85); markedly distinct from the tail; relatively slender medial region. Sternum streamlined and tubular when viewed cartilaginous clavicles absent. Suprascapula laterally. Oral disc lacking keratinised CHANDRAMOULI AND DEVI PRASAD — ENDEMIC ANDAMAN BULLFROG TAXONOMIC STATUS 49 FIGURE 4. (A) a calling male Kaloula ghoshi Cherchi, 1954 (arrow points at the absence of a bright inguinal blotch); (B) pair of K. ghoshi in amplexus; (C-D) Eggs and freshly emerged larvae of K. ghoshi; (E) stage 25 larvae of K. ghoshi in lateral and dorsal views; (F-G) lateral and dorsal views of a stage 33 larva of K. ghoshi (scalebars – 2 mm) mouthparts. Eyes distinct; lateral in separated widely from each other (IO – 2.49 position, situated nearly at 1/4th of the HBL; mm ±0.34). Caudal musculature well