Saturday, March 10, 2018

[Herpetology • 2018] Sumaterana gen. n. • Molecular Phylogenetic Analysis of A Taxonomically Unstable Ranid from Sumatra, Indonesia, reveals A New Genus with Gastromyzophorous Tadpoles and Two New Species


[a] Sumaterana crassiovis (Boulenger, 1920) 

[b] Sumaterana dabulescens  
 [c] S. montana
Arifin, Smart, Hertwig, Smith, Iskandar & Haas, 2018


Abstract

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.

Key Words: Clinotarsus, Huia, Meristogenys, Morphology, Molecular systematics, Ranidae, Species diversity, Taxonomy

Figure 2. 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). MZB.AMPH.29336 and ZMH.A14197 were collected from the type locality of C. kampeni and C. crassiovis, respectively.

Figure 3. 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 ZMH.A14197, male, Provinsi Sumatera Barat (a–c); ZMH.A14194, female, Provinsi Bengkulu (d–e); MZB.AMPH.23524, male, Provinsi Sumatera Utara (f); and MZB.AMPH.29396, male, Provinsi Aceh (g–i). Photos by U. Arifin.


Sumaterana gen. n.

Type species: Rana crassiovis Boulenger, 1920,
Syntypes: two adult females, BMNH1947.2.3.99 and BMNH1947.2.4.1.


Diagnosis: Sumaterana gen. n. belongs to a group of ranid torrent frogs, along with Huia and Meristogenys that possess gastromyzophorous larvae (Inger 1966, Inger and Gritis 1983, Inger 1986, Yang 1991). Sumaterana gen. n. species can be diagnosed by a combination of: (1) gastromyzophorous tadpole; (2) larval upper jaw sheaths thick, smooth, broadly arched, with thinner medial section; (3) lower jaw sheaths undivided, smooth, and V-shaped; (4) Labial Tooth Row Formula (LTRF): 8(5–9)/8(1) to 9(5–9)/9(1); (5) infraorbital and postorbital gland clusters present; (6) adult frogs medium sized (SVL males = 27.94–48.87 mm; females = 40.98–83.99 mm); (7) dorsum finely granulated, with or without scattered tubercles; (8) supratympanic fold present (skin fold above the tympanum, starting behind the eye); (9) posttympanic fold absent (vertical skin fold immediately posterior to tympanum); (10) dorsolateral fold absent or present; (11) tibia length 58.08–79.67% SVL; (12) outer metatarsal tubercle absent; (13) inner metatarsal tubercle present; (14) Finger I relatively shorter or subequal to Finger II; (15) width of finger discs larger or subequal to width of toe discs; (16) vocal sacs and nuptial pads present; (17) humeral gland absent.

Etymology: 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.

Common name: Sumatran Cascade Frogs (English) and
Katak Jeram Sumatra (Bahasa Indonesia).

Phylogenetic definition and content: Sumaterana gen. n. is a node-based genus that consists of three known species: Sumaterana crassiovis comb. n. (Fig. 2 Clade A, Fig. 5a), S. montana sp. n. (Fig. 2 Clade B, Fig. 5c), and S. dabulescens sp. n. (Fig. 2 Clade C, Fig. 5b), and their most recent common ancestor. Chalcorana kampeni is considered a junior synonym of S. crassiovis comb. n. based on Inger and Iskandar (2005) and the new molecular evidence. The monophyletic clade of Sumaterana gen. n. is restricted to the island of Sumatra, Indonesia. Our phylogenetic analyses and morphological examination supports these taxonomic recognitions (uncorrected p-distances in Suppl. materials 3).

Distribution and habitat: 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.



Figure 5. Sumaterana gen. n. species:
(a) Sumaterana crassiovis comb. n., ZMH.A14197, male, Provinsi Sumatera Barat; (b) S. dabulescens sp. n., MZB.AMPH.29396, male, holotype, Provinsi Aceh; (c) S. montana sp. n., ZMH.A14194, female, paratype, Provinsi Bengkulu. Photos by U. Arifin. 

Figure 8. Morphological variation within Sumaterana crassiovis comb. n.
(a) MZB.AMPH.29196, female, Provinsi Aceh, (b) Provinsi Sumatera Utara, (c) MZB.AMPH.29200, male, Provinsi Sumatera Barat, (d) ZMH.A14197, male, Provinsi Sumatera Barat. Photos by U. Arifin, except for (b) by A. Irawan.

Figure 8. Morphological variation within Sumaterana crassiovis comb. n.
 (e) MZB.AMPH.29320, male, Provinsi Sumatera Barat, (f) MZB.AMPH.29277, young male, Provinsi Bengkulu, (g) ZMH.A14151, male, Provinsi Sumatera Selatan, (h) ZMH.A14185 and MZB.AMPH.29296, male and female, Provinsi Lampung.

Photos by U. Arifin. 

Sumaterana crassiovis comb. n. 
Rana pantherina Van Kampen, 1910.
Rana crassiovis Boulenger, 1920.
Rana (Hyloranakampeni Boulenger, 1920.
Rana (Hyloranacrassiovis Boulenger, 1920.
Rana (Hylaranakampeni Van Kampen, 1923.
Rana (Hylaranacrassiovis Van Kampen, 1923.
Rana (Chalcoranakampeni Dubois, 1992.
Rana (Chalcoranacrassiovis Dubois, 1992.
Hydrophylax kampeni Frost et al., 2006.
Hydrophylax crassiovis Frost et al., 2006.
Hylarana kampeni Che et al., 2007.
Hylarana crassiovis Che et al., 2007.
Chalcorana kampeni Fei et al., 2010; Oliver et al., 2015.
Chalcorana crassiovis Fei eal., 2010; Oliver et al., 2015.

Common name: 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.

Figure 8. Morphological variation within Sumaterana crassiovis comb. n.
(a) MZB.AMPH.29196, female, Provinsi Aceh, (b) Provinsi Sumatera Utara, (c) MZB.AMPH.29200, male, Provinsi Sumatera Barat, (d) ZMH.A14197, male, Provinsi Sumatera Barat, (e) MZB.AMPH.29320, male, Provinsi Sumatera Barat, (f) MZB.AMPH.29277, young male, Provinsi Bengkulu, (g) ZMH.A14151, male, Provinsi Sumatera Selatan, (h) ZMH.A14185 and MZB.AMPH.29296, male and female, Provinsi Lampung. Photos by U. Arifin, except for (b) by A. Irawan.



Sumaterana montana sp. n.

Diagnosis: (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.

Etymology: 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.

Common name: We propose Mountain Cascade Frogs as common English name and Katak Jeram Gunung in Bahasa Indonesia.



Sumaterana dabulescens sp. n.

Diagnosis: (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.


Etymology: 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.

Common name: We propose Gayo Cascade Frogs as the English common name and Katak Jeram Gayo as name in Bahasa Indonesia.

Figure 10. (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.


 Umilaela Arifin, Utpal Smart, Stefan T. Hertwig, Eric N. Smith, Djoko T. Iskandar and Alexander Haas. 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. DOI:  10.3897/zse.94.22120

Abstrak: 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.

Kata Kunci: Clinotarsus, Huia, Meristogenys Morfologi, Molekular sistematik, Keanekaragaman spesies, Taksonomi

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