Article

Discovery of a deeply divergent and highly endemic frog lineage from Borneo: A taxonomic revision of Kalophrynus nubicola Dring, 1983 with descriptions of two new species (Amphibia: Anura: Microhylidae)

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  • Kitakyushu Museum of Natural History and Human History
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Abstract

The genus Kalophrynus is represented by tiny to medium terrestrial or subfossorial frogs and is widely distributed in Southeast Asia. The diversity centre of this genus is Borneo, where almost half of all nominal species are distributed and all of these are endemic to this and the peripheral islands. Kalophrynus nubicola is the smallest species within this genus; it is found only at high elevations in Gunung Mulu National Park, northeastern Sarawak, Malaysian Borneo. Three groups of populations were preliminary reported, but taxonomic decision on the groups was not yet given. In this study, we investigated the morphological, acoustic, and genetic differences among these three populations to reassess their taxonomic status. Morphological analyses confirmed differences in body size and colouration, molecular analyses indicated that each group was monophyletic, and differences in the acoustic characteristics of each group were also diagnostic. Therefore, herein, we describe them as distinct taxa. Phylogenetic analyses revealed that the K. nubicola group forms a highly divergent clade from other species within the genus. Our findings reveal that seven Kalophrynus species occur in Gunung Mulu National Park, with non-overlapping distributions according to elevation or forest type. We further discuss the biogeography and evolutionary history of this species group.

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Gives a description of the adult and tadpole stages of this microphylic frog discovered in the Pasoh Forest Reserve in 1981, with brief notes on ecology and behaviour and a comparison with closely related species.-R.Land
Article
We report a new microhylid frog of the genus Kalophrynus from Peninsular Malaysia and describe it as a new species Kalophrynus kiewi based on results of molecular and morphological analyses. The new species is a large-sized Kalophrynus (snout-vent length 34-47 mm) and is morphologically very similar to K. pleurostigma, in which it has long been unrecognized, and K. meizon, but is distinguished from them molecularly and by its body size, dorsal skin texture, and relative length of hindlimb. The new species is also clearly differentiated from all the other members of the genus by molecular and morphological differences. Taxonomic and distributional problems of the genus Kalophrynus in Peninsular Malaysia are briefly discussed.
Article
A new highland species of the dwarf litter frog, Leptobrachella itiokai, is described from Gunung Mulu National Park, northern Sarawak, East Malaysia. It occurs syntopically with another highland species, L. brevicrus, but differs from it by a unique call that may be described as a chirp, with dominant frequency of ca. 10 kHz. The new species is morphologically distinguishable from congeners by the combination of the following traits: rounded ventrolateral glands usually not in series; side of body with small black spots; ventrum entirely dark-coloured with tiny light spots; male with thread-like lineae masculinae.
Article
While the island of Borneo is considered a global biodiversity hotspot, the species richness in many groups remains unknown and appears underestimated. During herpetological surveys carried out in the interior of Sarawak, East Malaysia, several individuals of a small species of the genus Ansonia Stoliczka 1870 were collected on the Usun Apau plateau and in the Gunung Hose mountain range (Ansonia sp. Usun Apau). An integrative taxonomic approach comprising phylogenetic (2.4 kb mitochondrial rDNA fragment, Bayesian Inference and Maximum Likelihood, >5.1 % to its closest relative) and morphometric analyses (25 measurements, multivariate ratio analysis and linear discriminant analysis), as well as morphological comparisons support the status of this operational taxonomic unit as a separate taxon at species level. The obtained phylogenetic hypothesis corroborates the two major clades within Ansonia found in previous studies. Within Clade One Ansonia sp. Usun Apau and the enigmatic Ansonia torrentis are part of a monophyletic group of the Bornean species Ansonia hanitschi, Ansonia minuta, Ansonia platysoma, Ansonia spinulifer, Ansonia vidua, and two additional undescribed taxa. This subclade must be considered as the result of an on-island radiation in the complex evolution of Ansonia. The new species is formally described including the identification of diagnostic morphometric traits. Ansonia sp. Usun Apau is endemic to two isolated mountain ridges in central Sarawak and must be considered as a new element of the unique diversity of the Bornean amphibian fauna that is potentially threatened by habitat loss at least in parts of its range.
Article
An integrative taxonomic analysis is used to delimit and describe three new species of Pseudocalotoes from the sky island archipelago of the Banjaran (=mountain range) Titiwangsa of Peninsular Malaysia. Pseudocalotes drogon sp. nov., from Fraser’s Hill, Pahang is basal to the sister species P. larutensis from Bukit Larut, Perak in the Banjaran Bintang and the new species P. rhaegal sp. nov. from Cameron Highlands, Pahang. Pseudocalotes drogon sp. nov. is differentiated from all other species of Psuedocalotes by having the combination of a flat rostrum; seven postrostrals; an interparietal; 11 cir- cumorbitals; five canthals; 7–10 superciliaries; one scale between the rostral and nasal; nine supralabials; eight infralabi- als; 10 postnasal-suborbital scales; four postmentals; five or six sublabials; five or six chinshields; 47 smooth, wide, gular scales; weak transverse gular and antehumeral folds; two enlarged scales between the ear and eye; enlarged upper and low- er posttemporals; a single enlarged supratympanic; no enlarged postrictals; three large scales bordering the dorsal margin of the ear opening; large pretympanic scales; eight scales in the nuchal crest not separated by a gap; enlarged vertebral scales extending to the tip of the tail; keeled and non-plate-like scales on flanks; 51 midbody scales; midventrals smaller than dorsals; 19 subdigital lamellae on the fourth finger; 23 subdigital lamellae on the fourth toe; preaxial scales on third toe enlarged and spinose; subdigital lamellae not unicarinate; HW/HL 0.52; HL/SVL 0.31; no elbow or knee patches; and a male dewlap color of lime-green bearing a central yellow spot. Pseudocalotes rhaegal sp. nov. is differentiated from all other Psuedocalotes by having the combination of a convex rostrum; 6–8 postrostrals; an interparietal; nine or 10 circu- morbitals; five canthals; 7–10 superciliaries; one or two scales between the rostral and nasal scales; eight or nine suprala- bials; seven or eight infralabials; 11 or 12 postnasal-suborbital scales; four postmentals; four or five chinshields; 40–45 smooth, wide, gular scales; no transverse gular fold; a weak antehumeral fold; three or four enlarged scales between the ear and eye; an enlarged upper and lower posttemporal; an enlarged supratympanic; no enlarged postrictals; no large scales bordering the upper margin of the ear opening or in the pretympanic region; 6–8 enlarged nuchal crest scales not separated by a gap; enlarged vertebral scales extending to the base of the tail; weakly keeled, non-plate-like scales on the flanks; 52– 58 midbody scales; midventrals smaller than dorsals; 19–21 subdigital lamellae on the fourth finger; 22–26 subdigital la- mellae on the fourth toe; preaxial scales on the third enlarged and rounded; subdigital lamellae not unicarinate; HW/HL 0.50–0.54; HL/SVL 0.28–0.30; no elbow or knee patches; and female dewlap color yellow bearing a purple base. The analyses also indicated that the new species, P. viserion sp. nov. from Genting Highlands, Pahang in the southern section of the Banjaran Titiwangsa is the sister species of P. flavigula from Cameron Highlands 121 km to the north and can be separated from all other species of Psuedocalotes by having the combination of three postrostrals; 10 circumorbitals; four or five canthals; 5–7 superciliaries; rostral and nasals in contact; supralabials contacting the nasal; six or seven suprala- bials; six or seven infralabials; two or three postmentals; 47 or 48 smooth, flat, gular scales; three chinshields; weak trans- verse gular and antehumeral folds; two enlarged scales between the ear and eye; an enlarged upper and lower posttemporal; an enlarged supratympanic; no enlarged postrictals; 7–9 nuchal crest scales lacking gaps and not extending beyond midbody; weakly keeled and plate-like scales on the flanks; 35–38 midbody scales; ventrals smaller than dorsals; 22 or 23 subdigital lamellae on the fourth finger; 26 or 27 subdigital lamellae on the fourth toe; preaxial scales on the third toe not modified; subdigital scales not unicarinate; HW/HL 0.62; no white marking below the eye; dewlap in males yel- low; and no elbow or knee patches. Pseudocalotes rhaegal sp. nov. most likely occurs in syntopy with P. flavigula in Ta- nah Rata at Cameron Highlands and its discovery adds to a growing body of literature detailing the recent descriptions of several new, upland, closely related, sympatric species in Peninsular Malaysia. Another new population referred to here as Pseudocalotes sp. nov. from the Hala-Bala Wildlife Sanctuary, Betong District, Yala Province, Thailand is discussed. The discovery and description of these three new Pseudocalotes from the upland regions of Peninsular Malaysia continues to underscore the remarkably high herpetological diversity and ecological complexity in this sky island archipelago that is still underestimated, unappreciated, and unprotected.
Article
We present the latest version of the Molecular Evolutionary Genetics Analysis (MEGA) software, which contains many sophisticated methods and tools for phylogenomics and phylomedicine. In this major upgrade, MEGA has been optimized for use on 64-bit computing systems for analyzing bigger datasets. Researchers can now explore and analyze tens of thousands of sequences in MEGA. The new version also provides an advanced wizard for building timetrees and includes a new functionality to automatically predict gene duplication events in gene family trees. The 64-bit MEGA is made available in two interfaces: graphical and command line. The graphical user interface (GUI) is a native Microsoft Windows application that can also be used on Mac OSX. The command line MEGA is available as native applications for Windows, Linux, and Mac OSX. They are intended for use in high-throughput and scripted analysis. Both versions are available from www.megasoftware.net free of charge.
Article
The endangered frog, Odorrana ishikawae (Anura, Ranidae), is a species endemic to the mami and Okinawa Islands ofthe Ryukyu Archipelago, Japan. Segmentation of these islands has een considered to occur middle or upper Pleistocene. Our morphometric analyses revealed bvious differences between the Amami and Okinawa populations. Two distinct morphotypes were also recognized from the Amami Island (Amami common and Amami large types). Furthermore, the Amami and Okinawa populations could be distinguished clearly by coloration and dorsal uberculation. Based on 16SrRNA gene data, the Okinawa and Amami populations were phylogenetically separated but the genetic divergence (1.44-2.16%) was lower than the value suggested as species threshold in anurans (> 3% in 16S). Individuals of the Amami common and large types were nested within a single clade. Artificial hybridization experiments revealed normal hybrid viability between the two Amami types, with one exception. By contrast, between Okinawa females and two Amami type males, complete hybrid inviability was observed at early embryonic stages in the hybrids contrary to expectations from their low divergence in 16S. The reciprocal hybrids between two Amami type females and Okinawa males were viable, but spermatogenesis in the hybrid males showed some degree of abnormality. These results strongly indicate specific separation of the Amami population from the Okinawa population of O. ishikawae. Thus, we describe the Amami population as a new species, which is readily distinguishable from O. ishikawae by smaller ruggedly edged dorsal spots and an immaculate ventral surface.
Article
Extensive clearing of Indonesian primary forests results in increased greenhouse gas emissions and biodiversity loss. However, there is no consensus on the areal extent and temporal trends of primary forest clearing in Indonesia. Here we report a spatially and temporally explicit quantification of Indonesian primary forest loss, which totalled over 6.02 Mha from 2000 to 2012 and increased on average by 47,600 ha per year. By 2012, annual primary forest loss in Indonesia was estimated to be higher than in Brazil (0.84 Mha and 0.46 Mha, respectively). Proportional loss of primary forests in wetland landforms increased and almost all clearing of primary forests occurred within degraded types, meaning logging preceded conversion processes. Loss within official forest land uses that restrict or prohibit clearing totalled 40% of all loss within national forest land. The increasing loss of Indonesian primary forests has significant implications for climate change mitigation and biodiversity conservation efforts.
Article
Haplotype networks are an intuitive method for visualising relationships between individual genotypes at the population level. Here, we present popart, an integrated software package that provides a comprehensive implementation of haplotype network methods, phylogeographic visualisation tools and standard statistical tests, together with publication-ready figure production. popart also provides a platform for the implementation and distribution of new network-based methods – we describe one such new method, integer neighbour-joining. The software is open source and freely available for all major operating systems.
Article
Four species of endemic Leptobrachium are known from Borneo, two lowland species L. kanowitense and L. abbotti, a montane species L. montanum, and a highland species L. gunungense. Of these, both L. montanum and L. abotti were found to contain several cryptic species by recent molecular studies. The population from Bario, Kelabit Highland of Sarawak, is one such cryptic species and was once called Lineage 2 of L. abbotti. Our morphological survey on this population proved that it has characteristics distinct from all other congeners, and therefore, we describe the Bario population as a new species, Leptobrachium kantonishikawai sp. nov. The new species is distinguished from putative topotypes of L. montanum and L. abbotti, as well as from L. gunungense by having a grayish brown abdomen, usually vermiculated, although sometimes spotted or blotched with white, and some unique morphometric characteristics.
Article
The ubiquitous Mexican and Central American stream frogs allied to Eleutherodactylus rugulosus form a confusing spectrum of distinctive to subtly different populations. The condition of the male secondary sexual features: presence or absence of vocal slits and presence or absence of nuptial pads on the thumb, combined with the geographically consistent color (white, pale yellow, gold, orange, red or chestnut) of the venter of adults in life, provide the key to untangling the species problem in this group. For purposes of analysis the populations were grouped by the male secondary sexual features and compared in detail on the basis of 15 other characters of morphology and coloration. Twelve species are recognized within the rugulosus group, and may be placed in four series based on the presence (+) or absence (-) of vocal slits and nuptial pads in adult males. ++: Eleutherodactylus milesi of northern Honduras; E. merendonensis of northwestern Honduras; E. punctariolus of southern Costa Rica and western Panama; E. fleischmanni of Costa Rica; and E. escoces (sp. nov.) a bright red-bellied new species from the slopes (1100-2100 m) of Volcan Barba, Volcan Irazu and Volcan Turrialba of Costa Rica; +-: E. vocalis of northwestern Mexico; a new species, E. azueroensis (sp. nov.) from the Peninsula Azuero of western Panama; and E. taurus of the Golfo Dulce lowlands of southwestern Costa Rica and adjacent Panama; -+: E. matudai from the Pacific slopes of extreme southern Mexico and adjacent Guatemala; and a new species, E. angelicus, from the Cordillera de Tilaran and Volcan Poas in Costa Rica; --: E. brocchi of Alta and Baja Verapaz, Guatemala; and the wideranging lowland and slope species known from Mexico to western Panama, E. rugulosus. The Atlantic versant Mexican populations of this species are distinctive and have been variously recognized as a subspecies of E. rugulosus or as a separate species by previous authors. The earliest name for this population is Hylodes berkenbuschii Peters and E. natator Taylor and E. vulcani Shannon and Werler are strict synonyms. The seemingly allpatrically isolated southern populations of E. rugulosus in eastern and southwestern Nicaragua, Costa Rica and Panama are slightly distinct from the main population system of E. rugulosus. The earliest name for the southern stock is Lithodytes ranoides Cope with Liohyla pittieri Günther a strict synonym. Neither of these populations is recognized as separate from E. rugulosus. E. chiquito Lynch placed by its describer in the rugulosus group is a synonym of E. greggi of extreme southern Pacific slope Mexico and Guatemala, which is a member of the distantly related mexicanus group. Members of the rugulosus group fall into four geographic and ecologic distribution patterns: a) lowland and slope species, centered on the distribution of the wide-ranging E. rugulosus population system, with the allopatric E. vocalis on the northwest Mexican periphery, E. azueroensis on the southwest Panama periphery, the small population of E. merendonensis in northwestern Honduras and E. taurus occupying the Golfo Dulce lowlands of Costa Rica and western Panama, where E. rugulosus occurs only along the Pacific slope (600-1200 m) of the Talamanca-Chiriqui massif; b) E. brocchi and E. matudai in the highlands of southern Mexico and Guatemala; c) E. milesi in the uplands of northern Honduras; and d) E. angelicus, E. escoces, E. fleischmanni and E. punctariolus in the mountains of Costa Rica and western Panama. Verified cases of sympatry are known for E. rugulosus with E. matudai, with E. punctariolus and E. fleischmanni and E. punctariolus. An analysis of relationships and evolutionary trends indicates that the rugulosus group consists of four subgroups: the E. rugulosus subgroup in which males lack nuptial pads (E. azueroensis, E. taurus and E. vocalis, with vocal slits and E. brocchi and E. rugulosus, without vocal slits); the E. fleischmanni subgroup (E. angelicus, E. escoces, E. fleischmanni and E. punctariolus); the monotypic E. merendonensis subgroup; and the E. milesi subgroup (E. matudai and E. milesi). The latter three subgroups have nuptial pads in males. Within these lines vocal slits have been lost secondarily in E. matudai and E. angelicus. Of living forms E. vocalis most resembles the presumed ancestral stock of the group, that must have had a wide lowland range in Miocene. Evolution within the E. rugulosus subgroup involved fragmentation, modification and replacement in the lowlands during the remainder of Cenozoic, with E. brocchi evolving at a fairly late date in the Guatemala highland. Two other stocks seem to have diverged from the ancestral lineage by evolving nuptial pads in adult males, among other features: one in northern Central America to give rise to the specialized isolated E. merendonensis and the tuberculate highland E. milesi subgroup; a second in the mountains of Costa Rica and Panama to evolve into the E. fleischmanni group. Convergent evolution is found in each stock toward a highly specialized stream adapted form with increased webbing (E. merendonensis, E. punctariolus and E. taurus) and large toe disks in the former two, as modifications for life on boulders amid torrential racing water and splashing waterfalls. Three independent invasions of the uplands of Central America by members of the group, the E. milesi subgroup in northern Central America, the E. fleischmanni subgroup in Costa Rica and Panama and E. brocchi in Guatemala are responsible in large part for the species diversity within the rugulosus group.
Article
The Thai population of Kalophrynus pleurostigma interlineatus is distinct from the Bornean population of K. p. pleurostigma in advertisement call structure, i.e., notes pulsed in the former but unpulsed in the latter. This difference suggests that the Thai population is reproductively isolated from, or uses different recognition signals from, the nominal subspecies and should be regarded as a full species, K. interlineatus (Blyth, 1855). Taxonomic status of the population from Java requires further investigation.
Article
Advertisement call characteristics of Leptolalax heteropus from Peninsular Malaysia and L. gracilis, L. dringi, and two undescribed forms from Borneo are described. Leptolalax heteropus differs from the others in call characteristics, suggesting phylogenetic divergence; the call is short, lasting only 207-513 ms, and consists of a short series of 3-6 notes, the first note being longer in duration and higher in dominant frequency than subsequent ones. Calls of the remaining taxa are much longer, lasting 1.8-38 sec, and composed of a long series of 21-345 notes, each similar in duration and frequency within a call. However, dominant frequencies differ dramatically between species. Two new Bornean species, L. hamidi from Sarawak and L. arayai from Sabah, are described using acoustic and morphological characteristics.
Article
The original description of the Bornean megophryid Leptolalax dringi was not sufficient to differentiate the species from its Bornean congeners. The species was later re-described but the redescription included characters from both type specimens and Leptolalax from other sites, including undescribed species. Analyses of the advertisement call of specimens assigned to L. dringi have been published but call descriptions differ markedly from each other. Moreover, published pictures of L. dringi are dubious in identification. Thus, the identity of L. dringi is enigmatic, hindering taxonomic work on Bornean Leptolalax. We herein provide detailed descriptions of the type series as well as recently obtained topotypic specimens. We also present the results of an analysis of the advertisement call of a male paratype. These data will facilitate future taxonomic work on Bornean Leptolalax.