Research Article |
Corresponding author: Umilaela Arifin ( u.arifin@leibniz-lib.de ) Academic editor: Matthias Glaubrecht
© 2018 Umilaela Arifin, Utpal Smart, Stefan T. Hertwig, Eric N. Smith, Djoko T. Iskandar, Alexander Haas.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Arifin U, Smart U, Hertwig ST, Smith EN, Iskandar DT, Haas A (2018) Molecular phylogenetic analysis of a taxonomically unstable ranid from Sumatra, Indonesia, reveals a new genus with gastromyzophorous tadpoles and two new species. Zoosystematics and Evolution 94(1): 163-193. https://doi.org/10.3897/zse.94.22120
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The presence of an adhesive abdominal sucker (gastromyzophory) allows tadpoles of certain species of anurans to live in fast-flowing streams. Gastromyzophorous tadpoles are rare among anurans, known only in certain American bufonids and Asian ranids. To date, Huia sumatrana, which inhabits cascading streams, has been the only Sumatran ranid known to possess gastromyzophorous tadpoles. In the absence of thorough sampling and molecular barcoding of adults and larvae, it has remained to be confirmed whether other Sumatran ranid species living in similar habitats, i.e., Chalcorana crassiovis, possesses this larval type. Moreover, the taxonomic status of this species has long been uncertain and its taxonomic position within the Ranidae, previously based exclusively on morphological characters, has remained unresolved. To study the diversity and relationships of these frogs and to establish the identity of newly collected gastromyzophorous tadpoles from Sumatra, we compared genetic sequences of C. crassiovis-like taxa from a wide range of sites on Sumatra. We conducted bayesian and maximum likelihood phylogenetic analyses on a concatenated dataset of mitochondrial (12S rRNA, 16S rRNA, and tRNAval) and nuclear (RAG1 and TYR) gene fragments. Our analyses recovered C. crassiovis to be related to Clinotarsus, Huia, and Meristogenys. The DNA barcodes of the gastromyzophorous tadpoles matched adults from the same sites. Herein, we provide a re-description of adult C. crassiovis and propose “C. kampeni” as a synonym of this species. The molecular evidence, morphological features, and distribution suggest the presence of two related new species. The two new species and C. crassiovis together represent a distinct phylogenetic clade possessing unique molecular and morphological synapomorphies, thus warranting a new genus.
Pada beberapa jenis katak tertentu yang hidup di sungai berarus deras, di bagian abdomen berudunya terdapat semacam alat perekat sebagai mekanisme adaptasi pada kondisi habitat tempat tinggalnya. Tipe berudu seperti ini dikenal dengan nama gastromyzophorous dan sangat jarang ditemukan, hanya diketahui pada beberapa jenis bufonid di Amerika dan katak ranid di Asia. Hingga saat ini, hanya Huia sumatrana, dengan habitat sungai berarus deras, yang diketahui memiliki tipe berudu seperti ini di Sumatra. Tanpa survey menyeluruh dan tanpa DNA barcoding untuk katak dewasa dan kecebong, dugaan mengenai keberadaan katak jenis lain dengan tipe berudu serupa di pulau ini, misalnya Chalcorana crassiovis, masih harus dibuktikan. Di sisi lain, status taksonomi jenis ini hingga kini masih belum dapat dipastikan, dan posisi taksonominya dalam famili Ranidae hanya berdasarkan karakter morfologi saja. Oleh karena itu, untuk mengetahui keanekaragaman dan hubungan kekerabatan dari katak-katak jenis tersebut, serta untuk memastikan identitas koleksi berudu gastromyzophorous dari Sumatra, kami membandingkan data genetik dari semua taxa yang mirip dengan C. crassiovis dari berbagai lokasi di Sumatra. Kami merekonstruksi pohon filogeni dengan menganalisis sekuens DNA dari gabungan fragmen gen mitokondria (12S rRNA, 16S rRNA, dan tRNAval) dan gen inti (RAG1 dan TYR) menggunakan metode Bayesian dan Maximum Likelihood. Hasil penelitian kami membuktikan bahwa C. crassiovis berkerabat dekat dengan Clinotarsus, Huia, dan Meristogenys. Sekuens DNA dari berudu gastromyzophorous memiliki kecocokan dengan sekuens DNA katak dewasa dari lokasi yang sama. Dalam paper ini, kami menyajikan deskripsi ulang untuk C. crassiovis dan menyarankan agar “C. kampeni” menjadi junior synonym dari C. crassiovis. Bukti molekuler, karakter morfologi, dan kisaran distribusi menunjukkan bahwa terdapat dua jenis baru yang berkerabat dengan C. crassiovis. Ketiganya menunjukkan perbedaan filogenetik yang signifikan, yang dibuktikan dengan adanya synapomorphy pada karakter molekuler dan morfologi yang unik. Oleh sebab itu dibentuk genus baru untuk ketiga jenis ini.
Clinotarsus , Huia , Meristogenys , Morphology, Molecular systematics, Ranidae , Species diversity, Taxonomy
Clinotarsus , Huia , Meristogenys Morfologi, Molekular sistematik, Keanekaragaman spesies, Taksonomi
A fascinating aspect of Southeast Asian ranid frogs is that some of them possess tadpoles with large abdominal suckers. The presence of this adhesive structure has been referred to as gastromyzophory (
Members of the gastromyzophorous tadpole guild are relatively rare among anurans. They are known only in certain bufonids (e.g.,
In Asia, Amolops, Huia, and Meristogenys are all genera for which the tadpoles are known to have the gastromyzophorous type (
Chalcorana crassiovis (Boulenger, 1920) was originally described as Rana crassiovis Boulenger, 1920 based on two specimens (
To date, no studies have included Chalcorana crassiovis (or C. kampeni) in a molecular phylogenetic context, and few have included Sumatran congeners (
Considering the confusing and unstable taxonomic history of Chalcorana crassiovis and its relatives, it became clear that a thorough resampling and molecular analysis of cascade-dwelling frogs of Sumatra was necessary. Herein, we present our analyses of newly sampled material of C. crassiovis. The objectives of this study were: 1) to examine the phylogenetic relationships and taxonomic status of C. crassiovis and morphologically similar taxa based on new molecular data; 2) to evaluate the phylogenetic position and taxonomy of material topotypic with C. kampeni; 3) to assess material from extensive sampling along the longitudinal axis of Sumatra in an effort to elucidate the diversity and distribution of this group of frogs; 4) to assign samples of collected gastromyzophorous tadpoles to specific species based on molecular evidence.
We conducted rapid biological sampling (
Sampling localities of adult and larva of Chalcorana crassiovis specimens for this study. Black circles represent localities of specimens which were examined. White triangles represent localities of specimens which were examined and measured. Red stars represent localities of specimens which were examined, measured, and sequenced. Type locality of C. kampeni shown by number 1 (Bandar Baru), number 2 (Kerinci) for C. crassiovis. Provinces are shown by alphabet: A Aceh, B Sumatera Utara, C Riau, D Sumatera Barat, E Jambi, F Bengkulu, G Sumatera Selatan, H Lampung. Borders between provinces are represented by black lines. The map was prepared using GeoMapApp (
We followed the general legal guidelines of Germany (Tierschutzgesetz, https://www.gesetze-im-internet.de/tierschg/BJNR012770972.html) for handling and euthanizing the specimens. Each frog was anesthetized slowly and ultimately euthanized in an aqueous solution of chlorobuthanol. Tissue samples of muscle or liver tissue were preserved in either ethanol (96%), RNA later (Sigma Aldrich, USA) or Lysis buffer (0.5 M Tris / 0.25% EDTA / 2.5% SDS, pH 8.2) for DNA analyses. Specimens were fixed in 4% neutral-buffered formalin and then transferred to 70% ethanol for long term storage. All specimens examined in this study are deposited at one of these following museum: The Natural History Museum (
In order to uncover the true diversity of Chalcorana crassiovis, we acquired DNA sequences from tissue samples of adults (n = 20) from 19 localities across Sumatra. We selected the 20 specimens after a preliminary assessment of the qualitative morphological features of all specimens (n = 329) that were examined. Additionally, we included a subsample of four Sumatran gastromyzophorous tadpoles in the genetic analysis for identification. We followed the results of previously published studies (
We added DNA sequences of Amolops afghanus (Günther, 1858), A. indoburmanensis Dever, Fuiten, Konu & Wilkinson, 2012, A. marmoratus (Blyth, 1855), A. panhai Matsui & Nabhitabhata, 2006, Huia sumatrana Yang, 1991, H. cavitympanum (Boulenger, 1893), H. masonii (Boulenger, 1884), H. melasma Stuart & Chan-ard, 2005, Meristogenys jerboa (Günther, 1872) and M. kinabaluensis (Inger, 1966) because these taxa have reliably recognizable gastromyzophorous larvae. Finally, we included Odorrana hosii (Boulenger, 1891) and O. livida (Blyth, 1856) as additional species. Odorrana hosii lives syntopically in the same streams with C. crassiovis. Sequences of M. jerboa, C. megalonesa, Hyl. macrodactyla, Hydr. malabaricus, Hydr. leptoglossa, and O. livida were obtained from Genbank. The remaining ingroup sequences were generated by this project. The list of voucher specimens (n = 46) comprising the genetic data set is provided in Suppl. material
We extracted DNA from tissue samples (liver, muscle) using Crystal DNA mini Kit (Biolab), PeqGOLD Tissue Kit (Peqlab), or Qiagen DNeasy Blood and Tissue Kit. We then amplified mitochondrial genes (12S rRNA, 16S rRNA, and tRNAval) and nuclear genes (recombination-activating gene 1, RAG1, tyrosinase exon 1, TYR) for all frog samples. For tadpoles, we sequenced the 12S rRNA and 16S rRNA (which include tRNAval) genes as barcode tool to associate them with adults. Primer information and PCR annealing temperatures applied for this study are provided in Table
Gene markers, primer sequences, annealing temperatures and sequence length information.
Markers | Sequence | Annealing temp (°C) | Length (bps) | Citation |
---|---|---|---|---|
12S | 12SZ-L: AAAGGTTTGGTCCTAGCCTT 12SK-H: TCCRGTAYRCTTACCDTGTTACGA | 52 | 825 |
|
16S+ tRNAval | 12sm: GGCAAGTCGTAACATGGTAAG 16sd: CTCCGGTCTGAACTCAGATCACGTAG | 51 | 1406 |
|
RAG1 | Rag1 1F: GCMTTGCTSCCRGGGTATCA Rag1 2R: TCAATGGACGGAAGGGTTTCAATAA | 50 | 801 |
|
TYR | Tyr1A: AGGTCCTCTTRAGCAAGGAATG Tyr1G: TGCTGGGCRTCTCTCCARTCCCA | 57 | 579 |
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We ran PARTITION FINDER v.1.1 (
Bayesian (on the right) and Maximum Likelihood (on the left) trees showing the phylogenetic relationship of the crassiovis-group. A, B, C are distinct lineages within crassiovis-group. Black circles represent well supported nodes (PP ≥ 0.95 and BS ≥ 70). Red branches represent relationship between Clinotarsus and Huia melasma. Tadpole sequences named with specimen number_Tad_locality (province). Adult sequences named with specimen number_locality (province).
We measured a total of 175 adult Chalcorana crassiovis group frogs (males = 133, females = 42). These represent a subsample of all specimens examined (n = 329, Appendix 1). Measurements were taken with digital calipers with 0.01 mm reading accuracy. The subsample of 175 specimens included the sequenced specimens (except for MVZ271526, tissue only). Measurements were taken by UA, following current standards for morphological measurements of frogs (e.g.,
Standard measurement for adult specimens used in this study. See Suppl. materials
Acronym | Characters | Explanation |
---|---|---|
SVL | Snout Vent Length | From tip of snout to vent |
HL | Head Length | From tip of snout to angle of jaw |
HW | Head Width | Maximum width of the head at angle of jaw |
SL | Snout Length | From tip of snout to the anterior corner of eye |
SN | Snout Narial distance | From tip of snout to center of nares |
ED | Eye Diameter | Maximum distance between anterior and posterior corners of eye |
EN | Eye Narial distance | From center of naris to anterior circumference of eye |
IND | Internarial Distance | Distance between centers of nares |
IOD | Interorbital Distance | Minimum distance between upper eyelids |
UEW | Upper Eyelid Width | Maximum transverse width of upper eyelid |
TYv | vertical Tympanum diameter | Maximum vertical diameter, from the outer edges of tympanic annulus |
TYh | horizontal Tympanum diameter | Maximum horizontal diameter, from the outer edges of tympanic annulus |
ET | Eye-Tympanum distance | From posterior corner of eye to the anterior edge of tympanum |
LAL | Lower Arm Length | From the tip of the elbow to the proximal edge of the palmar tubercle |
HAL | Hand Length | From the proximal edge of the palmar tubercle to the tip of Finger III |
FE | Femur Length | From center of vent to lateral of knee |
TL | Tibia Length | Distance between anterior point of knee and posterior surface of heel with both tibia and tarsus flexed |
FL | Foot Length | From proximal end of inner metatarsal tubercle to tip of Toe IV |
IMTL | Inner Metatarsal Tubercle Length | Maximum distance between anterior and posterior tip of inner metatarsal tubercle |
F1L | Finger I Length | From the proximal edge of subarticular tubercle of Finger I to the tip of Finger I |
F2L | Finger II Length | From the proximal edge of subarticular tubercle of Finger II to the tip of Finger II |
F3DW | Finger III Disc Width | Maximum width of Finger III disc |
T4DW | Toe IV Disc Width | Maximum width of Toe IV disc |
We collected tadpoles from rocks in fast flowing water using a fishnet and followed the procedures suggested in
We followed the morphological terminology of
Standard measurement for tadpole specimens used in this study. See Suppl. materials
Acronym | Character | Explanation |
---|---|---|
BL | Body Length | From snout to the point where the axis of the tail (horizontal septum of myotomes) meets the body wall |
BH | Body Height | Maximum body height at trunk |
BW | Body Width | Maximum body width |
EN | Eye Narial distance | From center of eye to the center of naris |
ED | Eye Diameter | Diameter of eye measured horizontally |
ES | Eye Snout distance | From tip of snout to the anterior circumference of the eye |
IND | Inter Narial Distance | Distance between center of nares |
IOD | Inter Orbital Distance | Minimum distance between eyeballs |
LFH | Lower Fin Height | Measured at point of maximum tail height |
MTH | Maximum Tail Height | Measured from the maximum point of upper fin to the maximum point of lower fin |
NL | Narial Length | Maximum aperture of narial opening in dorsal view |
ODW | Oral Disc Width | Maximum width of oral disc |
SN | Snout Narial distance | From snout to the center of naris |
SS | Snout Spiracle distance | From snout to end of spiracle tube |
SUL | Sucker Length | From anterior end to posterior end of abdominal sucker |
SUW | Sucker Width | Maximum width of abdominal sucker |
SSL | Snout and Sucker Length | From the tip of snout and to posterior end of abdominal sucker |
TTL | Total Length | From tip of snout to tip of the tail |
TAL | Tail Length | Calculated as: Total Lenght (TTL) – Body Length (BL) |
TMH | Tail Muscle Height | Maximum tail muscle height at body-tail junction |
TMW | Tail Muscle Width | Maximum tail muscle width at body-tail junction |
UFH | Upper Fin Height | Measured at point of maximum tail height |
We inferred optimal phylogenetic trees from our concatenated dataset (3611 bps) comprising all gene markers (12S rRNA+16S rRNA+tRNAval+RAG1+TYR), of which 12.16% gaps and undetermined characters state. The best log likelihood of ML tree was -25426.240268.
The tree topologies recovered from ML and BI, respectively, were identical, except for the arrangement of Clinotarsus and Huia melasma (Fig.
With the exception of the incongruence in the position of Clinotarsus and Huia melasma, both the ML and BI trees confirmed the existence of two major clades each with strong nodal support (Fig.
Our results further corroborate previous studies (
Within the clade of the crassiovis-group (Fig.
Comparison of three lineages within Clade 1 based on the coloration of iris, the coloration of rear of thigh, and nuptial pad. Clade 1A (a–c), Clade 1B (c–d) and Clade 1C (g–i). Photographs were taken from
Frogs in Clade A share a similar elevational range (425–1545 m a.s.l.) and a similar habitat type (primary forest or good secondary forest) with Clade C (314–1000 m a.s.l.). Clade A also overlaps in elevational range with Clade B (1190–2033 m a.s.l.). In Aceh, we observed specimens of Clade A and Clade B at the same stream (1190 m a.s.l.), as well as frogs of Clade A and Clade C in another stream (1000 m a.s.l.). These observations suggest independent evolution occurring with the syntopic species. Two genetic samples (
Three of the four tadpoles sequenced belonged to Clade A and one tadpole belonged to Clade C. Morphological characters such as shape of the jaw sheath and number of keratodont rows showed distinct separation Clades A and C (see below) and were in accordance with the genetically justified assignment.
Variation of rear of thigh pattern and webbing on toes of the specimens within Clade 1A. Photographs were taken from
Herein we adopt the Unified Species Concept (
Rana crassiovis Boulenger, 1920, Syntypes: two adult females, BMNH1947.2.3.99 and BMNH1947.2.4.1.
Sumaterana gen. n. belongs to a group of ranid torrent frogs, along with Huia and Meristogenys that possess gastromyzophorous larvae (
Sumaterana gen. n., Huia, Meristogenys, and Amolops can be distinguish from Chalcorana, Clinotarsus, Hydrophylax, Hylarana, Odorrana, and all other ranids (except, Rana sauteri,
Adult Sumaterana gen. n. can be distinguished from Huia, Meristogenys, and Amolops by: lacking posttympanic fold (present in Huia, Meristogenys and Amolops;
Sumaterana is a compound generic epithet created from the Indonesian proper noun Sumatera, the Indonesian name for the island of Sumatra, and rana, the feminin Latin word for frog. Sumatera itself is named after the kingdom of Samudra Pasai, which was located along the coast of Aceh, Sumatra from the 13th to the 16th centuries CE. Samudra is a sanskrit word that means gathering of the seas, a place where the Andaman, Java, and South China seas meet the Indian Ocean. Rana, was also the very first generic name to be assigned to a member of the S. crassiovis group, endemic to the island of Sumatra.
Sumatran Cascade Frogs (English) and Katak Jeram Sumatra (Bahasa Indonesia).
Sumaterana gen. n. is a node-based genus that consists of three known species: Sumaterana crassiovis comb. n. (Fig.
Species of Sumaterana gen. n. inhabit riparian habitats in primary or secondary forest in Sumatra, Indonesia. Inhabited streams are typically fast flowing, 5 m wide or less, dominated by big rocks (diameter > 1 m). The known elevational range is from 314–2033 m a.s.l.. Adult frogs of these genus usually perched on rocks or vegetation at the stream. Tadpoles of these frogs can be found in groups attached to the top or sides of rocks in fast moving water.
Rana pantherina Van Kampen, 1910.
Rana crassiovis Boulenger, 1920.
Rana (Hylorana) kampeni Boulenger, 1920.
Rana (Hylorana) crassiovis Boulenger, 1920.
Rana (Hylarana) kampeni Van Kampen, 1923.
Rana (Hylarana) crassiovis Van Kampen, 1923.
Rana (Chalcorana) kampeni Dubois, 1992.
Rana (Chalcorana) crassiovis Dubois, 1992.
Hydrophylax
kampeni
Hydrophylax
crassiovis
Hylarana
kampeni
Hylarana
crassiovis
Chalcorana
kampeni
Chalcorana
crassiovis
Two adult females (BMNH1947.2.3.99 and BMNH1947.2.4.1-Fig.
262 adults (128 of them: 96 males and 32 females; were measured) and 21 tadpoles collected from Aceh up to Lampung (Appendix 1).
Specimens were assigned to Sumaterana crassiovis comb. n. based on comparison of material from Kabupaten Kerinci. Sumaterana crassiovis comb. n. is described by the following combination of characters: a medium sized species, SVL in males 30.03–48.87 mm, females 40.98–83.99 mm; head width subequal to head length; snout rounded, obtusely pointed in dorsal view, slightly protruding in lateral view; nostril closer to snout than to eye; vomerine teeth present, in oblique groups, between choanae; tongue lanceolate; loreal area deeply concave; canthus rostralis sharp, constricted behind nostrils; rictal ridge present; tympanum distinct, translucent (not transparent); interorbital distance 75.96–124.80% width of upper eyelid in females, 68.26–120.31% width of upper eyelid in males; pineal spot visible; dorsolateral fold absent; supratympanic fold thick, posttympanic fold absent; dorsum finely granulated with scattered tubercles, variable in size and density; flanks coarsely granulated with few tubercles; venter smooth, granulated posteriorly; rear of thigh usually barred as continuation of thigh dorsal pattern; arm slender, lower arm length 19.03–24.18% SVL in females and 19.58–25.46% SVL in males; hand length 31.54–36.98% SVL in females and 31.77–39.23% SVL in males; fingers long, without webbing; fingertips expanded into discs, diamond-shaped, with circummarginal groove; Finger I < Finger II, Finger III longest; fringes present on the outer phalanges of all fingers; subarticular tubercles distinct; width of Finger III disc > width of Toe IV disc; hindlimbs long, articulation of the heels reaching beyond tip of snout, when limb aligned to body; relative femur length 85.39–94.32% tibia length in females, 85.82–95.02% tibia length in males; length of tibia 60.17–70.52% SVL in females, 58.78–76.44% in males; toes slender and long; tip of toe extended into disc, diamond-shaped, with circummarginal grooves; toe lengths: I < II < III < V < IV, Toe V only slightly longer than Toe III; Toes I, II, III, and V fully webbed, webbing of Toe IV usually one phalanx free (I(1+/-―1+/-)II(1+/-―1+/-)III(1+/-―2+/-)IV(2+/-―1+/-)V); subarticular tubercles distinct; inner metatarsal tubercle distinct, oval, 92.07–212.77% T4DW in males and 98.80–150.00% in females; outer metatarsal tubercle absent; tarsal fold absent. (Measurements: Tables
Dorsal skin background green in life, with dark blotches around tubercles, lighter areas on the dorsum forming irregular network pattern; dark line connects the eye and the snout; the upper and lower lips with dark blotches on a light background; iris golden yellow, reddish anteriorly and posteriorly, with a dark netting pattern; tympanum pale brown, encircled by a dark line; flanks lighter than dorsum, lighter ventrad and with dark spots; venter whitish, throat and chest with or without dark marking; distinct cross-bars on dorsal limbs; the rear of thigh with dark vertical bars (usually a continuation from dorsal surface and separated by narrow lighter areas) or mottling (dark marking on lighter background); ventral legs are dusted with brown pigment; webbing color brown. In preservative, dorsal background light brown; flanks becoming gray; iris changed to gray.
(1) number of tubercles on dorsum and flanks: few to dense; (2) size of tubercles on dorsum: small and round to larger and elongated; (3) dorsolateral fold absent, but row of few small tubercles form incomplete dorsolateral series, dorsal to the posterior of trunk (not in continuation of tympanic fold); (4) dorsal coloration: dark blotches on green background vary from few and isolated, to dense, and forming irregular green background network between the dark blotches; (5) flank color yellowish-green to green (as dorsum), lighter ventrad, with distinct spots; (6) upper and lower lips: whitish to greenish, with dark markings, small distinct bars to wide and connected, lip markings absent or very thin in few individuals; (7) ventral dark markings: from none (ventral side whitish) to dark on throat and reaching venter, pale to dark; (8) rear of thigh with dark bars, complete or broken, or occasionally dark mottling on whitish/grayish background (Fig.
Males significantly smaller than females. Tympanum diameter 45.27–71.68% ED in males, 33.33–48.51% ED in females. Male with distinct undivided nuptial pads, covering base of the first finger to subarticular tubercle in dorsal and medial surface, paired subgular vocal sacs, humeral glands absent.
We propose Kerinci Cascade Frogs as the common English name (to replace the old spelling in “Korinchi Frog”, Iskandar and Mumpuni 2004) and Katak Jeram Kerinci as the Indonesian name.
This species is widespread on the island of Sumatra, ranging from the northern part of Provinsi Aceh to Kabupaten Pasawaran, the southern part of Provinsi Lampung (Fig.
Tadpoles were identified (100%) using 12S rRNA+16S rRNA+tRNAval barcoding with adult samples from the type locality. We examined total of 21 tadpoles. Stage 25:
Head and trunk approximately oval in dorsal view and dorsoventrally depressed and streamlined, in lateral view; maximum body width 64.40% body length; snout expanded and broadly rounded with emargination laterally setting off snout from body; eyes positioned dorsolaterally, oriented laterally; ED = 2.31 mm; IND/IOD = 48.22%; SN/EN = 44.82%; nostril open without raised rim; positioned anterodorsally and anterolaterally directed; two glands clusters present, infraorbital glands (five on each side) and postorbital glands (one on each side); oral disc ventral, a groove separating upper lip from snout, ODW/BW = 66.33%; oral disc marginal papillae short, arranged in single row; marginal papillae of upper lip present only on sides, on lower lip in uninterrupted row; two short submarginal papillae in lateral area of upper lip; LTRF: 9(6–9)/9(1); upper jaw sheath broad and heavily keratinized, smooth, undivided, thick but with distinct thinner medial section; lower jaw sheath undivided, V-shaped, smooth, and thick; both jaw sheaths finely serrated along their edges; very large abdominal sucker adjoining oral disc posteriorly, SUL/BL = 76.61%, SUW/BW = 89.03%; spiracle sinistral, tube long and posterior half free from body wall, opening directed posteriorly or posterodorsally; anal tube median, free from tail fin, directed posteriorly; strongly muscular tail: TAL/BL = 165.71%, TMH/BH = 71.87%, TMH/MTH = 63.00%; upper fin convex; maximum upper fin height is 30.57% maximum tail height at 49.19% of tail length; tail tip pointed.
In life (Fig.
Morphological comparison of (i) dorsal, (ii) ventral, (iii) palmar, and (iv) plantar regions of Sumaterana gen. n. species. (a) S. crassiovis comb. n.,
Morphometric values from all specimens of Sumaterana gen. n. examined in this study. Information given for each character as follows: average±st.deviation (first line), min–max (second line).
Character | S. crassiovis comb. n. | S. montana sp. n. | S. dabulescens sp. n. | |||
(males, n = 96) | (females, n = 32) | (males, n = 10) | (females, n = 7) | (males, n = 27) | (females, n = 3) | |
SVL | 37.58±4.01 30.03–48.87 | 67.43±10.42 40.98–83.99 | 29.98±1.14 27.94–31.56 | 55.07±2.58 51.61–59.60 | 37.65±1.45 34.69–40.86 | 57.30±7.58 48.03–66.60 |
HL | 14.73±1.76 11.92–19.66 | 26.84±4.04 16.44–32.44 | 12.01±0.40 11.53–12.83 | 21.61±0.99 20.42–25.35 | 14.86±0.53 13.81–15.73 | 24.13±2.71 20.79–27.43 |
HW | 13.52±1.66 10.96–18.61 | 24.43±3.72 14.14–29.68 | 10.88±0.53 9.74–11.79 | 19.61±1.09 18.04–21.65 | 14.00±0.59 12.99–15.20 | 23.03±2.78 19.41–26.18 |
SL | 5.85±0.71 4.52–7.82 | 10.80±1.66 6.76–13.61 | 4.99±0.38 4.47–5.53 | 8.76±0.59 7.83–9.59 | 5.82±0.22 5.22–6.26 | 9.55±0.98 8.35–10.74 |
SN | 2.26±0.26 1.78–2.99 | 3.92±0.64 2.50–5.82 | 2.15±0.35 1.73–2.77 | 3.95±0.60 3.11–4.80 | 2.21±0.14 1.94–2.47 | 3.39±0.40 2.88–3.85 |
EN | 3.45±0.35 2.62–4.44 | 6.30±0.95 4.17–8.16 | 2.70±0.24 2.29–3.14 | 4.86±0.31 4.58–5.55 | 3.38±0.13 3.10–3.62 | 5.33±0.46 4.71–5.80 |
IND | 3.78±0.44 3.03–5.17 | 6.52±0.94 3.79–7.90 | 3.50±0.33 3.06–4.01 | 6.10±0.75 5.04–7.58 | 3.79±0.19 3.44–4.26 | 5.95±0.50 5.25–6.40 |
IOD | 3.49±0.34 2.90–4.53 | 6.13±0.88 4.05–7.99 | 3.23±0.19 2.96–3.51 | 5.21±0.40 4.72–5.94 | 3.41±0.16 3.02–3.76 | 4.93±0.70 4.03–5.74 |
UEW | 4.07±0.62 2.72–6.05 | 6.84±1.10 4.18–8.48 | 2.96±0.18 2.72–3.22 | 5.21±0.40 4.65–6.00 | 4.02±0.34 3.41–4.67 | 5.63±0.56 4.90–6.26 |
ED | 5.62±0.61 4.59–7.70 | 9.10±1.42 5.68–11.40 | 4.41±0.35 3.80–4.97 | 7.23±0.59 6.64–8.29 | 5.40±0.37 4.76–6.39 | 7.96±1.06 6.63–9.22 |
TYv | 3.23±0.37 2.39–3.97 | 3.86±0.59 2.46–4.82 | 3.08±0.31 2.43–3.40 | 3.69±0.14 3.50–3.92 | 3.21±0.23 2.88–3.86 | 2.99±0.58 2.26–3.67 |
TYh | 3.22±0.36 2.39–4.29 | 3.84±0.63 2.46–4.82 | 3.02±0.30 2.44–3.50 | 3.43±0.14 3.19–3.57 | 3.12±0.28 2.27–3.70 | 2.78±0.17 2.58–3.00 |
ET | 1.14±0.29 0.74–2.90 | 2.74±0.64 1.44–4.01 | 0.92±0.12 0.70–1.17 | 2.14±0.17 1.87–2.31 | 1.20±0.11 1.01–1.50 | 2.07±0.19 1.90–2.33 |
LAL | 8.26±0.75 6.89–10.06 | 14.43±2.03 9.00–17.13 | 7.05±0.31 6.49–7.58 | 11.63±0.74 10.08–12.45 | 8.11±0.31 7.74–9.11 | 12.23±1.23 10.71–13.73 |
HAL | 13.14±1.34 10.77–16.82 | 23.27±3.34 14.90–30.32 | 10.85±0.46 10.26–11.72 | 18.70±0.98 17.41–20.79 | 12.48±0.42 11.62–13.33 | 18.25±1.58 16.11–19.87 |
FE | 22.33±2.10 19.29–28.55 | 40.35±5.89 24.25–50.36 | 19.75±0.96 18.16–21.14 | 35.94±1.49 33.97–38.66 | 22.42±0.81 21.18–24.29 | 32.44±4.06 27.55–37.50 |
TL | 24.52±2.61 20.74–31.85 | 44.61±6.31 27.83–55.96 | 22.17±0.90 20.96–24.20 | 40.69±1.13 38.29–42.08 | 23.74±0.72 22.30–25.30 | 36.01±3.32 31.46–39.28 |
FL | 20.68±2.34 16.26–27.71 | 38.11±5.57 23.64–49.14 | 18.82±0.51 18.19–19.53 | 34.85±1.53 32.30–37.54 | 19.63±1.31 14.41–22.04 | 30.27±3.27 25.94–33.85 |
IMTL | 1.75±0.27 1.28–2.62 | 3.20±0.57 1.72–4.29 | 1.50±0.13 1.30–1.70 | 2.70±0.30 2.30–3.27 | 1.83±0.16 1.51–2.10 | 2.74±0.26 2.38–2.96 |
F1L | 3.88±0.51 3.02–5.30 | 7.77±1.34 4.62–10.90 | 3.46±0.18 3.19–3.84 | 6.78±0.55 6.07–7.73 | 3.78±0.18 3.28–4.05 | 5.62±1.50 3.52–6.96 |
F2L | 4.85±0.59 3.92–6.74 | 8.89±1.39 5.85–11.79 | 3.66±0.19 3.30–3.96 | 6.99±0.53 6.26–8.00 | 4.55±0.22 4.17–5.19 | 7.03±0.80 6.01–7.97 |
F3DW | 2.00±0.35 1.29–3.01 | 3.62±0.62 2.26–5.06 | 1.16±0.20 0.93–1.54 | 1.82±0.25 1.40–2.13 | 2.03±0.16 1.64–2.27 | 3.00±0.48 2.33–3.46 |
T4DW | 1.36±0.30 0.92–2.26 | 2.71±0.46 1.72–3.47 | 1.08±0.21 0.78–1.40 | 1.82±0.17 1.63–2.20 | 1.58±0.13 1.30–1.77 | 2.43±0.32 1.99–2.76 |
Morphometric ratios from all specimens of Sumaterana gen. n. examined in this study. Information given for each character as follows: average±st.deviation (first line), min–max (second line).
Character | S. crassiovis comb. n. | S. montana sp. n. | S. dabulescens sp. n. | |||
---|---|---|---|---|---|---|
(males, n = 96) | (females, n = 32) | (males, n = 10) | (females, n = 7) | (males, n = 27) | (females, n = 3) | |
HW/ HL | 91.80%±2.75% 86.44%–100.30% |
90.97%±2.85% 84.36%–97.32% |
90.61%±3.99% 82.85%–95.08% |
90.72%±2.30% 87.54%–94.49% |
94.21%±2.01% 88.32%–96.87% |
95.37%±1.61% 93.36%–97.31% |
SL/ ED | 104.32%±8.80% 77.76%–125.45% |
119.03%±7.66% 106.07%–138.71% |
113.90%±13.48% 94.66%–145.53% |
121.99%±14.12% 103.02%–144.43% |
108.08%±7.18% 94.05%–120.59% |
120.50%±3.99% 116.49%–125.94% |
EN/ SN | 153.27%±12.86% 119.60%–187.64% |
162.54%±10.76% 141.08%–187.96% |
127.22%±14.95% 107.60%–157.23% |
125.25%±16.53% 100.00%–150.80% |
153.19%±9.46% 140.27%–177.84% |
157.58%±5.31% 150.65%–163.54% |
IND/ IOD | 108.15%±6.51% 95.83%–143.79% |
105.48%±6.82% 91.11%–121.35% |
108.01%±5.99% 99.71%–121.88% |
116.74%±8.06% 106.78%–128.66% |
111.38%±5.47% 102.65%–121.94% |
121.74%±7.76% 111.50%–130.27% |
IOD/ UEW | 86.87%±9.24% 68.26%–120.31% |
91.20%±9.72% 75.96%–124.80% |
109.33%±3.46% 102.17%–114.14% |
98.60%±6.15% 89.33%–105.48% |
84.68%±7.10% 72.38%–100.00% |
87.24%±3.88% 82.24%–91.69% |
TYv/ ED | 57.76%±5.57% 46.53%–71.68% |
42.59%±3.72% 36.75%–56.83% |
74.01%±10.69% 52.31%–89.47% |
50.57%±6.19% 43.91%–60.47% |
59.63%±4.62% 51.82%–72.94% |
37.90%7±.28% 28.18%–45.70% |
TYh/ ED | 57.45%±5.37% 45.27%–71.68% |
42.33%±3.80% 33.33%–56.83% |
73.07%±11.60% 52.31%–92.89% |
46.46%±4.08% 41.54%–54.67% |
58.61%±4.30% 51.82%–69.36% |
35.29%±2.68% 32.54%–38.91% |
F1L/ F2L | 80.08%±4.24% 70.56%–90.80% |
86.72%±3.25% 78.97%–93.54% |
94.55%±4.18% 87.67%–101.82% |
97.05%±2.62% 93.46%–100.89% |
83.41%±4.24% 78.03%–94.16% |
78.45%±14.09% 58.57%–89.47% |
F3DW/T4DW | 148.51%±15.60% 113.73%–197.03% |
133.13%±9.69% 112.08%–160.09% |
108.13%±8.45% 91.04%–120.00% |
93.19%±11.74% 73.68%–108.12% |
128.79%±8.42% 105.13%–144.53% |
122.94%±4.16% 117.09%–126.38% |
FE/ TL | 91.16%±2.33% 85.82%–95.02% |
90.39%±1.87% 85.39%–94.32% |
89.10%±2.63% 85.17%–94.12% |
88.33%±2.47% 85.09%–93.45% |
94.43%±1.96% 89.40%–97.55% |
89.85%±4.00% 86.51%–95.47% |
HL/ SVL | 39.17%±1.20% 36.22%–42.03% |
39.88%±1.24% 37.52%–43.53% |
40.09%±1.51% 37.83%–42.88% |
38.84%±1.03% 37.16%–40.28% |
39.49%±1.13% 37.66%–42.67% |
42.22%±0.86% 41.19%–43.29% |
HW/ SVL | 35.96%±1.46% 33.06%–39.40% |
36.27%±1.36% 33.57%–39.68% |
36.31%±1.91% 33.66%–39.33% |
35.22%±0.59% 34.16%–35.97% |
37.20%±1.11% 34.95%–39.01% |
40.26%±0.72% 39.31%–41.05% |
SL/ SVL | 15.56%±0.61% 13.99%–17.05% |
16.01%±0.65% 14.70%–17.53% |
16.65%±1.23% 14.95%–18.73% |
15.74%±0.88% 14.42%–17.04% |
15.49%±0.59% 14.46%–16.55% |
16.73%±0.52% 16.13%–17.38% |
SN/ SVL | 6.02%±0.41% 4.81%–7.50% |
5.77%±0.24% 5.31%–6.13% |
7.18%±1.11% 5.66%–8.86% |
7.09%±0.98% 6.01%–8.66% |
5.89%±0.38% 5.04%–6.62% |
5.93%±0.11% 5.78%–6.02% |
EN/ SVL | 9.18%±0.47% 8.27%–10.75% |
9.37%±0.63% 8.41%–11.02% |
9.00%±0.73% 7.44%–10.17% |
8.72%±0.25% 8.30%–9.07% |
9.00%±0.40% 8.32%–9.64% |
9.36%±0.47% 8.71%–9.81% |
IND/ SVL | 10.06%±0.61% 8.67%–12.62% |
9.69%±0.68% 8.05%–10.81% |
11.66%±1.01% 10.62%–13.52% |
10.91%±0.73% 9.75%–11.96% |
10.04%±0.43% 9.23%–11.02% |
10.46%±0.60% 9.61%–10.93% |
IOD/ SVL | 9.31%±0.46% 8.04%–10.75% |
9.21%±0.64% 7.26%–10.33% |
10.78%±0.51% 10.10%–11.91% |
9.36%±0.42% 8.78%–9.96% |
9.03%±0.49% 8.17%–10.13% |
8.60%±0.16% 8.39%–8.78% |
UEW/ SVL | 10.81%±0.98% 7.73%–12.90% |
10.15%±0.68% 7.73%–11.24% |
9.87%±0.59% 8.90%–10.85% |
9.50%±0.32% 8.99%–9.90% |
10.72%±0.81% 9.18%–12.17% |
9.87%±0.34% 9.40%–10.20% |
ED/ SVL | 14.99%±1.06% 12.82%–19.09% |
13.50%±0.84% 11.92%–15.40% |
14.72%±1.06% 12.16%–16.10% |
13.00%±1.02% 11.80%–14.73% |
14.37%±0.85% 12.64%–15.84% |
13.88%±0.09% 13.80%–14.00% |
TYv/ SVL | 8.67%±0.83% 6.80%–10.79% |
5.72%±0.45% 4.83%–6.63% |
10.80%±1.12% 8.42%–12.96% |
6.81%±0.39% 6.42%–7.54% |
8.55%±0.52% 7.78%–9.67% |
5.26%±0.98% 3.95%–6.31% |
TYh/ SVL | 8.62%±0.80% 6.42%–10.47% |
5.68%±0.42% 4.84%–6.64% |
10.73%±1.24% 8.42%–12.36% |
6.28%±0.36% 5.68%–6.88% |
8.41%±0.55% 7.65%–10.21% |
4.90%±0.36% 4.50%–5.37% |
ET/ SVL | 3.03%±0.79% 2.23%–9.66% |
3.98%±0.52% 3.12%–5.08% |
3.05%±0.36% 2.38%–3.79% |
3.83%±0.19% 3.62%–4.14% |
3.18%±0.24% 2.78%–3.79% |
3.65%±0.35% 3.32%–4.14% |
LAL/ SVL | 22.05%±1.22% 19.58%–25.46% |
21.41%±1.12% 19.03%–24.18% |
23.53%±0.70% 22.48%–24.48% |
20.92%±1.52% 19.44%–24.12% |
21.61%±0.83% 20.04%–23.05% |
21.44%±0.69% 20.62%–22.30% |
HAL/ SVL | 35.01%±1.51% 31.77%–39.23% |
34.47%±1.49% 31.54%–36.98% |
36.20%±1.35% 34.17%–38.93% |
33.61%±1.47% 30.93%–35.85% |
33.26%±1.18% 31.08%–36.00% |
32.06%±1.60% 29.83%–33.54% |
FE/ SVL | 59.54%±2.76% 53.83%–67.33% |
59.84%±2.37% 54.62%–63.19% |
65.86%±1.38% 63.23%–68.32% |
64.63%±2.85% 60.35%–67.80% |
59.65%±2.52% 54.95%–64.69% |
56.67%±0.49% 56.31%–57.36% |
TL/ SVL | 65.32%±2.72% 58.78%–75.37% |
66.22%±2.71% 60.17%–70.52% |
73.97%±2.34% 70.88%–78.39% |
73.29%±4.83% 65.28%–79.67% |
63.17%±2.51% 58.08%–68.81% |
63.20%±2.99% 58.98%–65.50% |
FL/ SVL | 55.06%±2.44% 49.18%–63.85% |
56.46%±2.27% 50.91%–60.23% |
62.82%±1.71% 59.52%–65.32% |
62.69%±3.42% 57.38%–67.51% |
52.25%±3.14% 39.59%–56.93% |
53.01%±1.54% 50.83%–54.18% |
IMTL/ T4DW | 131.80%±22.06% 92.07%–212.77% |
117.46%±14.34% 98.80%–150.00% |
144.27%±33.28% 97.86%–212.82% |
139.17%±19.24% 111.36%–171.78% |
115.89%±10.10% 98.75%–138.69% |
113.49%±6.59% 104.35%–119.60% |
Morphological variation within Sumaterana crassiovis comb. n. (a)
See Appendix 1.
(1) medium sized frog, SVL males (n = 10) 27.94–31.56 mm and females (n = 7) 50.11–63.37 mm; (2) dorsum skin finely granulated, color generally brown with scattered light spots; (3) tympanum distinct and translucent, slightly deep, supratympanic fold present, posttympanic fold absent; (4) dorsolateral fold present, thin, continuation of supratympanic fold to the level of pelvic joint, uninterrupted or broken; (5) venter smooth, white or yellowish; (6) tibia length 69.63–79.67% SVL; (7) Finger I 87.67–10.18% Finger II; (8) width of disc of Finger III 73.68–120.00% width of disc of Toe IV; (9) rear of thigh mottled; (10) approx. a quarter of the upper part of iris golden brown and the remaining iris with dense bright red stippling on black background; (11) webbing formula: I(0+―11/2)II(0+―2)III(0+―3+)IV(3-―0+)V; (12) outer metatarsal tubercle absent, inner metatarsal tubercle present; (13) males with paired vocal sacs, undivided nuptial pad, humeral gland absent.
Sumaterana montana sp. n. differs from S. crassiovis comb. n. (character in parentheses) in these characters: dorsum color brown with scattered light blotches (green background with dark markings on tubercles, lighter area forming irregular network pattern); iris golden brown in the upper quadrant, below with dense bright red stippling on back background (golden yellow with reddish color in the anterior and posterior sector and dark netting pattern); rear of thigh mottled, light spots on dark background (usually with vertical dark bars on lighter background, as continuation of dorsal thigh); dorsal texture shagreened, generally without tubercles (finely granulated with scattered tubercles); length of Finger I ≈ Finger II (Finger I < Finger II); disc width of Finger III ≈ disc width of Toe IV (disc width of Finger III > disc width of Toe IV); dorsolateral fold present, thin (absent); webbing formula: I(0+―11/2)II(0-―2)III(0-―3+)IV(3-―0+)V (I(1+/-―1+/-)II(1+/-―1+/-)III(1+/-―2+/-)IV(2+/-―1+/-)V).
Adult female, gravid; body relatively slender; head width 91.93% head length; snout rounded, slightly pointed in dorsal view, and slightly protruding in lateral view; vomerine teeth present, in oblique groups, between choanae; loreal area deeply concave; canthus rostralis sharp, constricted behind nostrils; rictal ridge present; eye-nostril distance 133.41% of snout-nostril distance; interorbital distance 99.00% width of upper eyelid; tympanum distinct, translucent, slightly set deep, diameter < 50% ED (TYv/ED = 49.31%, TYh/ED = 44.91%); supratympanic fold present, posttympanic fold absent; pineal spot visible; dorsolateral fold thin, starting in line with supratympanic fold anteriorly to the level of pelvic joint; dorsum and flank skin shagreened; venter skin smooth. Arm slender, lower arm length 19.44% SVL; hand length 32.81% SVL; fingers long, without webbing, tip extended into discs, diamond-like shaped, with circummarginal groove; length of Finger I 96.63% Finger II, Finger III longest; flaps present on the outer phalanges of all fingers; subarticular tubercles distinctive; disc width of Finger III 94.42% disc width of Toe IV. Hindlimbs long, articulation of the heels reach far beyond the tip of snout when limb aligned with body, relative length of femur, foot, and tibia to SVL: 61.01%, 69.63%, and 59.24%, respectively; toe lengths: I < II < III < V < IV, Toe V only slightly longer than Toe III; toe tip extended into diamond-shaped discs; cirmummarginal groove present; webbing formula: I(0+―11/2)II(0+―2)III(0+―3+)IV(3-―0+)V; subarticular tubercle distinct; inner metatarsal tubercle distinct, oval, 152.09% T4DW; outer metatarsal tubercle absent; tarsal fold absent.
In life, dorsum and upper head brown with scattered light spots; dark dorsolateral line from eye to groin; flanks brown lighting up ventrad, with yellowish color in the posterior region, and many round dark spots; venter yellowish, dark markings on throat up to half of abdomen; golden brown color in at the upper quarter sector of iris, the remaining parts of iris with dense red stippling on black background; a series of dark spots encircled base of upper eye lid; dark brown line from eye to nostril (along canthus rostralis) towards snout tip, not connected to counterpart at tip of snout; dark brown area between eye and tympanum; tympanum pale brown with darker spot in the center; upper lip background brown, lighter posteriorly, with dark brown spots; lower lip brown with few light spots; arm with four dark cross-bars, from elbow to wrist; dorsal face of thigh and tibia brown, each with 6 dark bars; yellow spots on groin; rear of thigh mottled, whitish and yellow spots on brown background; ventral skin of thigh dusted brown on cream background, denser on both lateral side of posterior region; webbing color brown. Color in preservative similar to life coloration; dorsum brown and markings remain the same; yellowish color on flanks and venter changed into white; iris color became gray.
SVL 59.60, HL 23.35, HW 21.65, SL 9.14, SN 4.16, EN 5.55, IND 7.58, IOD 5.94, ED 7.95, UEW 6.00, TYv 3.92, TYh 3.57, ET 2.31, LAL 12.32, HAL 20.79, FE 38.66, TL 41.50, FL 37.54, IMTL 3.27, F1L 7.59, F2L 7.73, F3DW 2.03, T4DW 2.15.
(1) dorsum color background: light pale brown to dark brown; (2) lighter spots on dorsum, none to dense; variable size; (3) dorsolateral fold: continuous or interrupted, variable thickness; (4) yellowish posterior of flank; pale to brighter; (5) tubercles on flanks: none to many; (6) round dark spots on flanks, few to many; size: small to big; (7) dark marking on throat, chest, and ventrum: none to present and reaching the belly; (8) cross bars on limbs, 3–4 (arm, from elbow to wrist), 5–6 (thigh); variable thickness; (9) mottled pattern on rear of thigh: small, yellow and creamy spots to blotches, on brown background. (Metrics: Tables
Males smaller than females. Tympanum diameter 52.31–92.89% ED in males and 41.54–60.47% ED in females. Adult males with single, undivided nuptial pad covering base of the first finger to subarticular tubercle on dorsal and medial surface. Paired subgular vocal sacs visible, humeral glands absent.
The specific epithet is the Latin adjective montana in allusion to the distribution of this species at high elevations of the Bukit Barisan mountain range of Sumatra.
We propose Mountain Cascade Frogs as common English name and Katak Jeram Gunung in Bahasa Indonesia.
Only known from high elevations of northern (Provinsi Aceh and Provinsi Sumatera Utara) and mid (Provinsi Bengkulu) Sumatra (Fig.
Geographical distribution of Sumaterana dabulescens sp. n. (purple squares; type locality purple arrow [1]: Jamat, Taman Buru Linge Isaq), S. crassiovis comb. n. (brown circles; type locality brown arrow [2]: Kerinci), and S. montana sp. n. (red triangles; type locality red [3]: Gunung Baru, Taman Nasional Kerinci-Seblat). The map was prepared using GeoMapApp (
Unknown.
13 adults, one juvenile, and 8 tadpoles (Appendix 1).
(1) medium sized frog, SVL males (n = 27) 34.69–40.86 mm and females (n = 3) 48.03–66.60 mm; (2) dorsum finely granulated with scattered round, distinct tubercles; generally gray with dark gray spots on tubercles; (3) tympanum distinct and translucent (not transparent), supratympanic fold present, posttympanic fold absent; (4) dorsolateral fold absent; (5) venter smooth, granulated posteriorly, white; (6) tibia length 58.08–68.81% SVL; (7) Finger I 58.57–94.16 Finger II; (8) width of disc of Finger III 105.13–144.53% width of disc of Toe IV; (9) rear of thigh mottled; dark blotches on light background; (10) iris silver-gray with dark netting, slightly yellow to orange golden in the upper part; (11) all toes fully webbed to base of discs (I(1+/-―1+/-)II(1+/-―1+/-)III(1+/-―1+/-)IV(1+/-―1+/-)V); (12) outer metatarsal tubercle absent, inner metatarsal tubercle present; (13) males with paired vocal sacs, divided nuptial pad, humeral gland absent.
Sumaterana dabulescens sp. n. differs from S. crassiovis comb. n. and S. montana sp. n. (character in parentheses: S. crassiovis comb. n.; S. montana sp. n.) by gray dorsum with dark markings on tubercles, lighter area forming irregular network pattern (green background with dark markings on tubercles, lighter area forming irregular network pattern; brown background with lighter sports, Fig.
Male, vocal sacs distinct and paired; nuptial pad distinct, divided, covering dorso-medial face of proximal Finger I to level of subarticular tubercle; humeral gland absent; body relatively slender; head width 90.11% head length; in dorsal view, snout obtusely pointed, in lateral view acutely projecting; canthus rostralis sharp, constricted behind nostrils; loreal area deeply concave; vomerine teeth present, in oblique groups, between choanae; tongue lanceolate; rictal ridge present; eye-nostril distance 177.84% snout-nostril distance; interorbital distance 89.27% width of upper eyelid; tympanum distinct, translucent, diameter > 50% ED (TYv/ED = 64.85; TYh/ED = 69.36%); supratympanic fold distinct, posttympanic fold absent; pineal spot visible; dorsolateral fold absent; dorsum and flanks finely granulated with scattered rounded tubercles on the dorsal region up to the upper part of the flanks; venter skin smooth, finely granulated in the posterior region; hindlimb long, articulation of the heels reach far beyond the tip of snout when limb aligned with body; thigh length 94.90% tibia; tibia 64.02% SVL; fingers slender, without webbing; Finger I 94.16% Finger II, Finger III longest; skin flaps present on the outer phalanges of all fingers; subarticular tubercles on fingers and toes distinct; disc width of Finger III 105.13% disc width of Toe IV; discs of toes and fingers diamond-shaped, both with cirmummarginal grooves; toe lengths: I < II < III < V < IV, Toe V slightly longer than Toe III; toes fully webbed; inner metatarsal tubercle distinct, oval, 118.59% T4DW; outer metatarsal tubercle absent; tarsal fold absent.
In life, dorsum and flanks generally gray; scattered tubercles on the dorsum and the upper part of flanks usually embedded in dark color; lighter area of the dorsum form an irregular network; golden color with dark spot between eye and nostril; upper lip grayish-white with dark spots (right: 4; left: 4); lower lip whitish with dark spots (right: 3; left: 2); iris silver-gray with dark netting, golden orange in the upper part; tympanum gray with light spot in the center; venter, chest, and throat fully whitish; forearm with four distinct dark cross-bars; hind limbs with thick dark cross-bars dorsally (thigh: 5; tibia: 5); rear of thigh with dark mottling on light gray background; legs light brownish ventrally; webbing brown. Dorsal coloration turned from gray with dark spots into uniformly dark brown in preserved specimens; flanks remained gray, lighter ventrad; iris color changed to uniform gray; no color change in the dark markings or pattern.
SVL 36.13, HL 14.87, HW 13.40, SL 5.67, SN 1.94, EN 3.45, IND 3.88, IOD 3.66, ED 5.32, UEW 4.10, TYv 3.45, TYh 3.69, ETD 1.19, LAL 7.76, HAL 12.80, FE 21.95, TL 23.13, FL 19.19, IMTL 1.85, F1L 4.03, F2L 4.28, F3DW 1.64, T4DW 1.56.
(1) dorsum generally with round tubercles, lighter spots vary from few to dense; (2) number of dark-round tubercles on dorsum and flanks: few to many tubercles; (3) size of dark wound tubercles on dorsum and flanks: small to big tubercle; (4) life coloration of dorsum background: lighter grey or slightly grayish-green to dark gray; (5) iris upper sector: light yellow to orange; (6) dark netting of iris: loose to dense; (7) throat, chest, and venter with or without marking, ranging from none to marking reaching venter; (6) marking on upper and lower lip: variable in size; (9) number of cross bars on limbs: 2–4 (arm between wrist and elbow), 4–7 (thigh); (10) thickness of cross bars on limbs: variable; (11) composition of dark color on lighter background of mottling pattern on rear of thigh: dense to less dense dark pattern on lighter background. Metrics in Tables
Males smaller than females. Tympanum diameter 38.54–72.94% ED in males and 28.18–45.70% ED in females. Adult males with divided nuptial pads and vocal sacs, covering dorso-medial face of proximal Finger I to level of subarticular tubercle, humeral gland absent.
The species epithet dabulescens is an artificial construct of “dabul”, “gray” in Gayo language, combined with the Latin ending “-escense”, here in the sense of “tending to be”, in allusion to the gray appearance of this species. The Gayo are a local tribe in the Aceh region of Sumatra and after which the Gayo highlands have been named.
We propose Gayo Cascade Frogs as the English common name and Katak Jeram Gayo as name in Bahasa Indonesia.
Provinsi Aceh, particularly localities in the northern and middle part of Aceh: Kecamatan Mane, Kabupaten Pidie; Krung Meuriam, Kecamatan Tangse, Kabupaten Pidie; Kabupaten Bener Meriah; Road Takengon-Bierut, Enang-Enang Resort, Kabupaten Aceh Tengah, and Taman Buru Linge–Isaq, Kecamatan Takengon, Kabupaten Aceh Tengah (Fig.
(a–b) Typical cascading stream habitat of Sumaterana crassiovis comb. n. at Taman Nasional Gunung Leuser, Provinsi Aceh. Sumaterana dabulescens sp. n. inhabits similar stream habitats. (c) Specimen of S. dabulescens sp. n. on a rock near a small cascade in its natural habitat at Taman Buru Linge Isaq, Provinsi Aceh. Photos by U. Arifin.
We examined eight tadpoles of Sumaterana dabulescens sp. n.. Stage 25: UA20140336 (n = 5),
In life, dorsal coloration of body and tail densely mottled with brown and golden blotches on a grayish background with dense fine dark stippling; lower flanks with a conspicuous wedge-shaped white area; tail muscle dark with dense-dark stippling overlain by yellowish-golden to orange mottling; lateral tail vein visible in first third of tail, including dorsal branching along myosepta; upper and lower fin mostly transparent, stippled with melanophores, especially towards the fin margin; yellowish-golden stippling also present in the upper and lower fin; iris background color black, with dense golden to orange iridophore stippling; abdomen whitish laterally and densely stippled with golden iridophores medially; golden iridophores stippling also present in the anterior region of the snout and oral disc; abdominal sucker mostly transparent except for the central spot with golden iridocytes and scattered pigment along the rim. In preservative: color of dorsal region became gray with dense darker dots and dark brown mottling; darker region were obvious on the upper flanks and between eyes and naris; iris all black; lens grayish-white; ventrally uniformly transparent with dark pigments in the anterior region of snout, oral disc, and lateral.
Body proportions between Stage 25, Stage 28, and Stage 37 were variable, e.g., BW/BH in Stage 25 (165.01%) > in Stage 28 (160.72%) > in Stage 37 (144.97%); SUW/BW in Stage 25 (89.58%) > in Stage 28 (86.66%) > in Stage 37 (82.94%); TAL/BL in Stage 25 (153.74%) < Stage 37 (174.06%) < in Stage 28(183.00%); TMH/BH in Stage 25 (61.38%) < in Stage 37 (76.19%) < in Stage 28 (84.71%); TMH/MTH in Stage 25 (60.53%) < in Stage 37 (66.74%) < in Stage 28 (71.00%). Variation: Body shape in the Stage 25 and Stage 28 were oval; the posterior region gradually arched towards the end of the body (e.g. Stage 28; Fig.
1 | Highly stream-adapted, gastromyzophorous tadpoles abdominal sucker present | 2 |
– | Abdominal sucker absent | Abavorana, Amnirana, Chalcorana, Clinotarsus, Hylarana, Odorrana, Pulchrana, Staurois |
2 | Expanded, rounded finger and toe tips | Amolops |
– | Expanded finger and toe tips, pointed and diamond shaped | 3 |
3 | Posttympanic and dorsolateral folds well developed, thick dark ∏-shaped over tympanum | Huia |
– | Posttympanic and dorsolateral folds well developed, no thick dark ∏-shaped over tympanum, endemic to Borneo | Meristogenys |
– | Posttympanic fold absent, dorsolateral folds present or absent, no thick dark ∏-shaped over the tympanum, endemic to Sumatra | 4, Sumaterana |
4 | Poorly developed dorsolateral folds, F1 subequal to F2 in length, F3DW subequal to T4DW, dorsum shagreened, brown, sometimes slightly tuberculate | S. montana |
– | Dorsolateral folds absent, F1 shorter than F2, F3DW wider than T4DW, dorsum green or greyish with darker markings, finely granulated and tuberculate | 5 |
5 | Undivided nuptial pad in males, green dorsal background in life, rear of thighs with dark bars | S. crassiovis |
– | Divided nuptial pad in males, gray dorsal background in life, rear of thighs with dark mottling or blotches | S. dabulescens |
The taxonomic status of the taxon previously known as Chalcorana crassiovis has been problematic for a long time. The case was confounded by the description of a morphologically similar species (C. kampeni), the loss of the C. kampeni type specimen, insufficient sampling, and a lack of evidence beyond morphology (viz., molecular data). After the original description by
Samples from the type localities of Sumaterana crassiovis comb. n. and “Chalcorana kampeni” were nested in Clade A in the phylogenetic analysis (Fig.
In this study we included four known species of Huia (H. cavitympanum-type species, Borneo; H. sumatrana, Sumatra; H. masonii, Java; and H. melasma, the mainland Asia). Nevertheless, we were unable to solve the phylogenetic problem of Huia, which has previously been considered paraphyletic (
Another interesting subject arises from the optimized phylogenies in our analyses (Fig.
A third case of ranids with gastromyzophorous tadpoles has been reported in Rana sauteri (Boulenger, 1909). Its tadpoles are clearly more morphologically (
We are fully aware that phylogenetic and taxonomic problems persist in our studied taxa. These need to be addressed in the future. Broad thorough geographic sampling of adult and larval forms is a prerequisite to solve phylogenetic quandaries with any amphibian taxa, especially in the species rich tropical realm. Moreover, integrating independent sources of evidence (e.g. DNA, morphology, distribution) is an optimal strategy to accurately and convincingly validate the taxonomic position of doubtful amphibian taxa from hyperdiverse hotspots (
Our results are also further evidence that the taxonomic diversity of Sumatran frogs is still significantly underestimated (Iskandar and Colijn 2000,
This study was funded by the Deutsche Forschungsgemeinschaft (DFG Ha2323/12-1) and by a stipend for U. Arifin provided by the Deutscher Academischer Austauschdienst–Indonesian German Scholarship Program (DAAD–IGSP, 91548731). Some parts of the study were funded by the National Science Foundation (NSF) DEB-1146324 to E. N. Smith and M. B. Harvey, Volkswagen Foundation (I/79 405) to A. Haas, and Rufford Small Grants (RSG) 15779-1 to U. Smart. The Synthesis of Systematic Resources Access program (SYNTHESYS; NL-TAF-4882 and GB-TAF-4412) supported U. Arifin during examination of type specimens and other materials. The authors thank the School of Life Sciences-Institute of Technology Bandung, Indonesian Science Institute, RISTEK, Director General KKH–PHKA as well as Balai Besar Taman Nasional Gunung Leuser (BBTNGL), Balai Besar Taman Nasional Kerinci-Seblat (BBTNKS), Balai Taman Nasional Batang Gadis (BTNBG) and all Balai Konservasi Sumber Daya Alam (BKSDA) in Sumatra which made this research possible. Permits for research and collecting (SIP) in Sumatra and Java were kindly provided by RISTEK to E. N. Smith and team during the years 2013 to 2016: 149–150/SIP/FRP/SM/V/2013, 152/SIP/FRP/SM/V/2013, 149-A/SIP/FRP/SM/XII/2013, 151-A/SIP/FRP/SM/XII/2013, 153–154-A/SIP/FRP/SM/XII/2013, 193–197/SIP/FRP/SM/Vl/2015, and 209–210/SIP/FRP/SM/Vl/2015. For U. Arifin and team, research and collecting permit were kindly provided by Ministry of Forestry, Directorate General of Forest Protection and Nature Conservation: SI.10/Set-3/2014 and SI.298/Set-3/2014, S.49/KKH-2/2014, S.825/KKH-2/2014. We thank Ester Dondorp (Naturalis Biodiversity Center, Leiden) and Jeff Streicher (Natural History Museum, London) for their support during work of U. Arifin at both museums. We are grateful to Jamili Nais, Director of Research Sabah Parks, Economic Planning Unit, Prime Ministers department, Malaysia, for issuing collecting permit and providing essential help to A. Haas and team. We thank the Sarawak Forest Department and Sarawak Forestry Corporation, in particular Nur Afiza Binti Umar, Dayang Nuriza Binti Abang Abdillah, Mohamad bin Kohdi, Engkamat Anak Lading Datu Haji Ali Yusop and Mohd. Shabudin Sabki, for providing advice and issuing permits to S.T. Hertwig and A. Haas: NCCD.907.4.4(Jld.VI)-107, Park Permit 56/2011, export permit 09813. We thank Jimmy McGuire, David Bickford, and Jens Vindum for tissue samples, and Andri Irawan for specimen materials. We are very grateful to Ganjar Cahyadi, Novari Fajria, Amir Hamidy, Agus Yasin, Yoghi Budianto, Zainal, Kamarudin, Carmidi, Hajidin, Zamrin, Agusman, Aidil, Zainudin, Rikha, Sumarto, Darlizon, Muhardi, Samin, Hasbalah, Alfian, Adrinaldi, Abdullah, Mistar Kamsi, Dewi Roesma, Risky Dharma, Ari Arfama, David Gusman, Preddy Syahputra, Mantra Sanjaya, Dr. Nia Kurniawan and his group of herpetology students at Brawijaya University and many other people for all support during field work in Sumatra and Java. Annamarie Vogt, Dimitrij Trovinov, Katharina Gebauer, and Manuel Schweizer provided excellent support in the lab, and Lea Waser provided the illustration for morphological measurement. Ulrich Manthey kindly provided literature. David McLeod and two other anonymous reviewers for reviewing our manuscript.
Specimens examined
(* bold = measured, star (*) = sequenced)
Sumaterana crassiovis comb. n. (adults, n = 262)
Provinsi Aceh. – Kabupaten Pidie, Mountain above Geumpang, Transmigrasi community, old road to mining camp, 4.85824°N, 96.21348°E, 1090 m a.s.l.,
Provinsi Sumatera Utara. – Kabupaten Dili Serdang, Sungai DAM Bumi Perkemahan Sibolangit, 3.27347°N, 98.53586°E, 881–965 m a.s.l.,
Provinsi Sumatera Barat. – Kabupaten Pasaman, Kecamatan Panti, Stream 3 Cagar Alam Rimbo Panti, 0.35220°N, 100.04933°E, 425 m a.s.l.,
Provinsi Jambi. – Kabupaten Kerinci, trail to Danau Tujuh, 1.71076°S, 101.36986°E, 1506 m a.s.l.,
Provinsi Bengkulu. – Kabupaten Lebong, Stream at Camp 2 Desa Seblat Ulu, Taman Nasional Kerinci Seblat, 2.95330°S, 102.13955°E, 758-774 m a.s.l.,
Provinsi Sumatera Selatan. – Kabupaten Pagar Alam Selatan, road from Manna to Pagar Alam, 4.11296°S, 103.10007°E, 772 m a.s.l.,
Provinsi Lampung. – Kabupaten Lampung Barat, Curug Berdua, Gunung Abung, Desa Purajaya, 5.03730°S, 104.54828°E, 956–979 m a.s.l.,
Sumaterana crassiovis comb. n. (tadpoles, n = 21)
Provinsi Sumatera Barat. – Kabupaten Lima Puluh Koto, Desa Tanjuang Bungo, 0.15188°N, 100.47468°E, 388 m a.s.l.,
Provinsi Sumatera Selatan. – Kabupaten Muara Enim, Desa Batu Surau, 4.13725°S, 103.58640°E, 1048-1069 m a.s.l.,
Sumaterana montana sp. n. (adults, n = 28)
Provinsi Aceh. – Kabupaten Bener Meriah, foot of Berni Terlong, near Desa Rambune, pantan Pediangah, Tihmang gagah, 4.77054°N, 96.79341°E, 1377 m a.s.l.,
Provinsi Sumatera Utara. – Kabupaten Karo, Gunung Sibuatan, Above Kampung Naga Linga, 2.91076°N, 98.46313°E, 1625 m a.s.l.,
Provinsi Bengkulu. – Kabupaten Lebong, Desa Seblat Ulu, Taman Nasional Kerinci Seblat, 2.88525°S, 102.12993°E, 2000 m a.s.l.,
Sumaterana dabulescens sp. n. (adults, n = 38)
Provinsi Aceh. – Kabupaten Pidie, Krueng Meriam, Tangse, 4.938417°N, 95.98375°E, 314 m a.s.l.,
Sumaterana dabulescens sp. n. (juvenile, n = 1)
Provinsi Aceh. – Kabupaten Pidie, Kecamatan Mane, Desa Mane, 4.92334°N, 96.12215°E, 792 m a.s.l.,
Sumaterana dabulescens sp. n. (tadpoles, n = 8)
Provinsi Aceh. – Kabupaten Pidie, Kecamatan Mane, Stream 3 Mane, 4.91926°N, 96.12300°E, 747 m a.s.l.,
List of sequences and GenBank accession number
Data type: molecular data
Illustration of morphological characters
Data type: species data
Explanation note: Illustration of morphological characters measured in this study: A) for adults, B) for tadpoles. Explanation for each acronym available in Tables
Pairwise genetic distance
Data type: molecular data
Explanation note: Pairwise genetic distance (uncorrected p) within crassiovis-group and all taxa used in this study based on 16S sequence, calculated using MEGA 7.1.025. Values are in percentage (%).