Genetic divergences of South and Southeast Asian frogs: a case study of several taxa based on 16S ribosomal RNA gene data with notes on the generic name Fejervarya

To elucidate the genetic divergences of several Asian frog taxa, the mitochondrial 16S rRNA gene (16S) sequences of 81 populations across 6 Asian countries were analyzed. In total, 109 haplotypes were found, and the concept of a 3% difference in 16S sequence corresponding to species threshold was applied to define candidate amphibian species, for which corroborating evidence, such as morphology, ecological characteristics, and/or nuclear gene data, is required. Polypedates leucomystax, Hylarana chalconota, and Hylarana sp. from Chantaburi, Maelippet Siberut, and Langkawi Island, respectively, correspond to 3 candidate species and H. erythraea from Malaysia/Thailand represents a possible candidate species. Hylarana cf. nicobariensis from Muara Siberut, Amolops larutensis from Gombak, and Microhyla okinavensis from Ishigaki Island showed divergences from the topotypic specimen, all suggesting a relevant candidate species. Microhyla heymonsi from Malaysia and M. ornata from 2 regions (Mudigere and Talapu) in India did not fit any congeneric species based on available 16S data, suggesting 3 possible candidate species in total. Two lineages of Duttaphrynus melanostictus from Malaysia denote 2 possible candidate species. Consequently, this study indicates the occurrence of 6 candidate and 6 possible candidate species, and argues that the generic allocation of the Fejervarya-Minervarya-Zakerana complex needs to be studied in detail.

Genetic divergences of South and Southeast Asian frogs: a case study of several taxa based on 16S ribosomal RNA gene data with notes on the generic name Fejervarya

To elucidate the genetic divergences of several Asian frog taxa, the mitochondrial 16S rRNA gene (16S) sequences of 81 populations across 6 Asian countries were analyzed. In total, 109 haplotypes were found, and the concept of a 3% difference in 16S sequence corresponding to species threshold was applied to define candidate amphibian species, for which corroborating evidence, such as morphology, ecological characteristics, and/or nuclear gene data, is required. Polypedates leucomystax, Hylarana chalconota, and Hylarana sp. from Chantaburi, Maelippet Siberut, and Langkawi Island, respectively, correspond to 3 candidate species and H. erythraea from Malaysia/Thailand represents a possible candidate species. Hylarana cf. nicobariensis from Muara Siberut, Amolops larutensis from Gombak, and Microhyla okinavensis from Ishigaki Island showed divergences from the topotypic specimen, all suggesting a relevant candidate species. Microhyla heymonsi from Malaysia and M. ornata from 2 regions (Mudigere and Talapu) in India did not fit any congeneric species based on available 16S data, suggesting 3 possible candidate species in total. Two lineages of Duttaphrynus melanostictus from Malaysia denote 2 possible candidate species. Consequently, this study indicates the occurrence of 6 candidate and 6 possible candidate species, and argues that the generic allocation of the Fejervarya-Minervarya-Zakerana complex needs to be studied in detail.

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  • Alam MS, Igawa T, Khan MMR, Islam MM, Kuramoto M, Matsui M, Kurabayashi A, Sumida M (2008). Genetic divergence and evolutionary relationships in six species of genera Hoplobatrachus and Euphlyctis (Amphibia: Anura) from Bangladesh and Other Asian countries revealed by mitochondrial gene sequences. Mole Phylogenet Evol 48: 515–527.
  • AmphibiaWeb: Information on amphibian biology and conservation. [web application] 2013. Berkeley, California: AmphibiaWeb.
  • Available: http://amphibiaweb.org/. (Accessed: August 19, 2013)
  • Bain RH, Lathrop A, Murphy RW, Orlov NL, Cuc HT (2003). Cryptic species of a cascade frog from Southeast Asia: taxonomic revisions and descriptions of six new species. Am Mus Novit 3417: 1–60.
  • Bansaln R, Karanth KP (2010). Molecular phylogeny of Hemidactylus geckos (Squamata: Gekkonidae) of the Indian subcontinent reveals a unique Indian radiation and an Indian origin of Asian house geckos. Mole Phylogenet Evol 57: 459–465.
  • Bickford D, Lohman DL, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2007). Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22: 148–155.
  • Biju SD, Bossuyt F (2003). New frog family from India reveals an ancient biogeographical link with the Seychelles. Nature 425: 711–714.
  • Biju SD, Van Bocxlaer I, Mahony S, Dinesh KP, Radhakrishnan C, Zachariah A, Giri V, Bossuyt F (2011). A taxonomic review of the Night Frog genus Nyctibatrachus Boulenger, 1882 in the Western Ghats, India (Anura: Nyctibatrachidae) with description of twelve new species. Zootaxa 3029: 1–96.
  • Bossuyt F, Brown RM, Hillis DM, Cannatella DC, Milinkovitch MC (2006). Phylogeny and biogeography of a cosmopolitan frog radiation: Late Cretaceous diversification resulted in continent- scale endemism in the family Ranidae. Syst Biol 55: 579–594.
  • Boulenger GA (1920). A monograph of the South Asian, Papuan,
  • Melanesian and Australian frogs of the genus Rana. Rec Ind Mus 20: 1–226. Brown RM, Guttman SI (2002). Phylogenetic systematic of the Rana signata complex of Philippine and Bornean stream frogs: reconsideration of Huxley’s modification of Wallace’s line at the Oriental-Australian faunal zone interface. Biol J Linn Soc 76: 393–461.
  • Brown RM, Linkem CW, Siler CD, Sukumaran J, Esselstyn JA, Diesmos AC, Iskandar DT, Bickford D, Evans BJ, McGuire JA et al. (2010). Phylogeography and historical demography of Polypedates leucomystax in the Islands of Indonesia and Philippines: Evidence for recent human-mediated range expansion? Mole Phylogenet Evol 57: 598–619.
  • Castresana J (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mole Biol Evol 17: 540–552.
  • Chan KO, Grismer LL (2010). Re-assessment of Reinwardt’s gliding frog, Rhacophorus reinwardtii (Schlegel 1840) (Anura: Rhacophoridae) in Southern Thailand and Peninsular Malaysia and its re-description as a new species. Zootaxa 2505: 40–50.
  • Chanda SK (2002). Hand Book-Indian Amphibians. Kolkata, India:
  • Zoological Survey of India. Claridge MF, Dawah HA, Wilson MR (1997). Species: The units of biodiversity. 1st ed. London, UK: Chapman and Hall.
  • Cracraft J (1989). Speciation and its ontology: the empirical consequences of alternative species concepts for understanding patterns and processes of differentiation. In: Otte D, Endler J, editors. Speciation and Its Consequences. Sunderland, MA,
  • USA: Sinauer Associates, pp. 28–59. Daniels RJR (2005). India-A Lifescape, Amphibians of Peninsular
  • India. Hyderabad, India: Indian Academy of Sciences, Universities Press (India) Private Limited. Das I (2002). An Introduction to the Amphibians and Reptiles of Tropical Asia. Kota Kinabalu, Borneo: Natural History
  • Publications (Borneo). Das I, Ravichandran MS (1998 [1997]). A new species of Polypedates
  • (Anura: Rhacophoridae) from the Western Ghats, India, allied to the Sri Lankan P. cruciger Blyth, 1852. Hamadryad 22: 88–94.
  • Dayrat B (2005). Towards integrative taxonomy. Biol J Linn Soc 85: 407–415. de Queiroz K (1998). The general lineage concept of species, species criteria, and the process of speciation: A conceptual unification and terminological recommendations. In: Howard DJ,
  • Berlocher SH, editors. Endless Forms: Species and Speciation. New York, NY, USA: Oxford University Press, pp. 57–75. de Queiroz K, Donoghue MJ (1990). Phylogenetic systematics or Nelson’s version of cladistics? Cladistics 6: 61–75.
  • Djong TH, Islam MM, Nishioka M, Matsui M, Ota H, Kuramoto M, Khan MMR, Alam MS, Anslem DS, Khonsue W et al. (2007).
  • Genetic relationships and reproductive-isolation mechanisms among the Fejervarya limnocharis complex from Indonesia (Java) and other Asian countries. Zool Sci 24: 360–375. Dobzhansky T (1950). Mendelian populations and their evolution. Am Nat 84: 401–418.
  • Dobzhansky T (1976). Organismic and molecular aspects of species formation. In: Ayala FJ, editor. Molecular evolution.
  • Sunderland, MA, USA: Sinauer Associates, pp. 95–105. Dubois A (1987). Miscellanea taxonomica batrachologica (ІІ). Alytes 6: 1–9.
  • Dubois A, Ohler A (1999). Asian and Oriental toads of the Bufo melanostictus, Bufo scaber and Bufo stejnegeri groups
  • (Amphibia, Anura): a list of available and valid names and redescription of some name-bearing types. J S Asian Nat Hist 4: 133–180. Dubois A, Ohler A, Biju SD (2001). A new genus and species of
  • Ranidae (Amphibia, Anura) from south-western India. Alytes 19: 53–79. Duméril AMC, Bibron G (1841). Erpétologie Genérale ou Histoire
  • Naturelle Complète des Reptiles Tome 8. Roret, Paris (in French). Dutta SK (1997). Amphibians of India and Sri Lanka (Checklist and Bibliography). Bhubaneswar, India: Odyssey Publication House.
  • Dutta SK, Manamendra-Arachchi K (1996). The Amphibian Fauna of Sri Lanka. Colombo, Sri Lanka: Wildlife Heritage Trust of Sri Lanka.
  • Emerson SB, Richards C, Drewes RC, Kjer KM (2000). On the relationships among ranoid frogs: a review of the evidence. Herpetologica 56: 209–230.
  • Ereshefsky M (1992). The units of evolution: Essays on the nature of species. Cambridge, MA, USA: MIT press.
  • Ferguson JWH (2002). On the use of genetic divergence for identifying species. Biol J Linn Soc 74: 509–516.
  • Fouquet A, Gilles A, Vences M, Marty C, Blanc M, Gemmell NJ (2007). Underestimation of species richness in neotropical frogs revealed by mtDNA analysis. PLoS ONE 2: e1109.
  • Frost DR (2013). Amphibian Species of the world: An online reference 5.6. Electronic Database accessible at http://research. amnh.org/vz/herpetology/amphibia/American Museum of
  • Natural History, New York, USA. Frost DR, Grant T, Faivovich J, Bain R, Haas A, Haddad CFB, de Sá RO, Donnellan SC, Raxworthy CJ, Wilkinson M et al. (2006).
  • The amphibian tree of life. Bull Am Mus Nat Hist 297: 1–370. Funk WC, Caminer M, Ron SR (2012). High levels of cryptic species diversity uncovered in Amazonian frogs. Proc R Soc B 279: 1806–1814.
  • Futuyma DJ (2005). Evolution. Sunderland, MA, USA: Sinauer
  • Associates. Gouy MAM, Guindon S, Gascuel O (2010).
  • SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27: 221–224. Gaston AJ, Zacharias VJ (1996). The recent distribution of endemic and disjunct birds in Kerala state: preliminary results of an ongoing survey. J Bombay Nat Hist Soc 93: 389–400.
  • Glaw F, Köhler J, de La Riva I, Vieites DR, Vences M (2010).
  • Integrative taxonomy of Malagasy tree frogs: combination of molecular genetics, bioacoustics and comparative morphology reveals twelve additional species of Boophis. Zootaxa 2383: 1–
  • Hanken J (1999). Why are there so many new amphibian species when amphibians are declining? Trends Ecol Evol 14: 7–8.
  • Hasan M, Islam MM, Khan MMR, Alam MS, Kurabayashi A, Igawa T, Kuaramoto M, Sumida M (2012a). Cryptic anuran biodiversity in Bangladesh revealed by mitochondrial 16S rRNA gene sequences. Zool Sci 29: 162–172.
  • Hasan M, Kuaramoto M, Islam MM, Alam MS, Khan MMR, Sumida M (2012b). A new species of genus Hoplobatrachus (Anura, Dicroglossidae) from the coastal belt of Bangladesh. Zootaxa 3312: 45–58.
  • Herbert PDN, Cywinska A, Ball SL, de Waard JR (2003). Biological identification through DNA barcodes. Proc R Soc Lond B Biol Sci 270: 313–321.
  • Herbert PDN, Stoekle MY, Zemlak TS, Francis CM (2004).
  • Identification of birds through DNA barcodes. PLoS Biol 2: e3 Howlader MS (2011). Cricket Frog (Amphibia: Anura: Dicroglossidae): Two regions of Asia are corresponding two groups. BNNOPRANI: Bd Wl Bull 5: 1–7.
  • Inger RF (1947). Preliminary survey of the amphibians of the Riukiu islands. Fieldiana Zool 32: 297–352.
  • Inger RF (1999). Distribution of amphibians in Southern Asia and adjacent islands. In: Duellman WE, editor. Patterns of
  • Distribution of Amphibians: A Global Perspective. Baltimore, MD, USA: Johns Hopkins University Press, pp. 445–482. Inger RF, Stuart BL, Iskandar DT (2009). Systematics of a widespread
  • Southeast Asian frog, Rana Chalconota (Amphibia: Anura: Ranidae). Zool J Linn Soc 155: 123–147. Inger RF, Stuebing RB (2005). A Field Guide to the Frogs of Borneo.
  • Borneo: Natural History Publication. Iskandar DT (1998). The Amphibians of Java and Bali. Bogor,
  • Indonesia: Research and Development Centre for Biology- LIPI. Islam MM, Khan MMR, Djong HT, Alam MS, Sumida M (2008a).
  • Genetic differentiation of the Fejervarya limnocharis complex from Bangladesh and other Asian countries elucidated by allozyme analyses. Zool Sci 25: 261–272. Islam MM, Kurose N, Khan MMR, Nishizawa T, Kuramoto M, Alam MS, Hasan M, Kurniwan N, Nishioka M, Sumida M (2008b).
  • Genetic divergence and reproductive isolation in the genus Fejervarya (Amphibia: Anura) from Bangladesh inferred from morphological observations, crossing experiments, and molecular analyses. Zool Sci 25: 1084–1105.
  • Jansen M, Bloch R, Schulze A, Pfenninger M (2011). Integrative inventory of Bolivia’s lowland reveals hidden diversity. Zool Scr 40: 567–583.
  • Jayaram KC (1974). Ecology and distribution of freshwater fishes, amphibians and reptiles. In: Mani MS, Editor. In Ecology and Biogeography in India. The Hague, Netherlands: Dr. W. Junk B.V. Publishers, pp. 517–580.
  • Jobb G, von Haeseler A, Strimmer K (2004). TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 4: 18.
  • Karanth KP (2003). Evolution of disjunct distributions among wet-zone species of the Indian subcontinent: Testing various hypotheses using a phylogenetic approach. Curr Sci India 85: 1276–1283.
  • Kosuch J, Vences M, Dubois A, Ohler A, Böhme W (2001). Out of
  • Asia: mitochondrial DNA evidence for an Oriental origin of tiger frogs, genus Hoplobatrachus. Mole Phylogenet Evol 21: 398–407. Kotaki M, Kurabayashi A, Matsui M, Kuramoto M, Djong HT, Sumida M (2010). Molecular phylogeny of the diversified frogs of genus Fejervarya (Anura: Dicroglossidae). Zool Sci 27: 386–395.
  • Kurabayashi A, Kuramoto M, Joshy H, Sumida M (2005) Molecular phylogeny of the Ranid frogs from Southwest India based on the mitochondrial ribosomal RNA gene sequences. Zool Sci 22: 525–534.
  • Kuraishi N, Matsui M, Ota H (2009). Estimation of the origin of
  • Polypedates leucomystax (Amphibia: Anura: Rhacophoridae) introduced to the Ryukyu Archipelago, Japan. Pac Sci 63: 317– 3 Kuramoto M, Joshy SH, Kurabayashi A, Sumida M (2007). The genus
  • Kurup GU (1974). Mammals of Assam and the mammal-geography of India. In: Mani MS, Editor. In Ecology and Biogeography in
  • India. The Hague, Netherlands: Dr. W. Junk B.V. Publishers, pp. 585–613. Lannoo M (2005). Amphibian Declines: The Conservation Status of United States Species. Berkeley and Los Angeles, CA, USA:
  • University of California Press. Matsui M, Hamidy A, Belabut DM, Ahmad N, Panha S, Sudin A, Khonsue W, Oh HS, Yong HS, Jiang JP et al. (2011). Systematic relationships of Oriental tiny frogs of the family Microhylidae
  • (Amphibia, Anura) as revealed by mtDNA geneology. Mole Phylogenet Evol 61: 167–176. Matsui M, Hamidy A, Murphy RW, Khonsue W, Yambun P, Shimada T, Ahmad N, Belabut DM, Jiang JP (2010). Phylogenetic relationships of megophryid frogs of the genus Leptobrachium
  • (Amphibia, Anura) as revealed by mtDNA gene sequences. Mole Phylogenet Evol 56: 259–272. Matsui M, Ito H, Shimada T, Ota H, Saidapur SK, Khonsue W, Tomoko TU, Wu GF (2005). Taxonomic relationships within the Pan-Oriental narrow-mouth toad Microhyla ornata as revealed by mtDNA analysis (Amphibia, Anura, Microhylidae). Zool Sci 22: 489–495.
  • Mayden RL (1997). A hierarchy of species concepts: the denouement in the saga of the species problem. In: Claridge MF, Dawah
  • HA, Wilson MR, editors. Species: The Units of Biodiversity. London, UK: Chapman and Hall, pp. 381–424. Mayden RL (1999). Consilience and a hierarchy of species concepts: advances toward closure on the species puzzle. J Nematol 31: 95–116.
  • Mayr E (1942). Systematics and the Origin of Species. New York, NY,
  • USA: Columbia University Press. Mayr E (1982). The Growth of Biological Thought: Diversity,
  • Evolution, and Inheritance. Cambridge, MA, USA, and London, UK: Belknap Press of Harvard University Press. Meenakshi K, Sujith VG, Sanil G (2009). DNA barcoding of some amphibians of Western Ghats. Third International Barcode of
  • Life Conference (in press). Milá B, Tavares ES, Saldaña AM, Karubian J, Smith TB, Baker AJ (2012). A trans-Amazonian Screening of mtDNA reveals deep intraspecific divergence in forest birds and suggests a vast underestimation of species diversity. PLoS ONE 7: e40541.
  • Moyle RG, Schilthuizen M, Rahman MA, Sheldon FH (2005).
  • Molecular phyogenetic analysis of the white-crowned forktail Enicurus leschenaulti in Borneo. J Avian Biol 36: 96–101. Ohler A, Deuti K, Grosjean S, Paul S, Ayyaswamy AK, Ahmed MF, Dutta SK (2009). Small-sized dicroglossids from India, with the description of a new species from West Bengal, India. Zootaxa 2209: 43–56.
  • Padil JM, Miralles A, de la Riva I, Vences M (2010). The integrative future of taxonomy. Front Zool 7: 16.
  • Pyron RA, Wiens JJ (2011). A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mole Phylogenet Evol 61: 543–583.
  • Rambaut A, Drummond AJ (2007). Tracer v. 1.5. http://beast.bio. ed.ac.uk/Tracer.
  • Roe BA, Ma DP, Wilson RK, Wong JFH (1985). The complete nucleotide sequences of Xenopus laevis mitochondrial genome. J Biol Chem 260: 9759–9774.
  • Ronquist F, Huelsenbeck JP (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.
  • Stuart BL, Inger RF, Voris HK (2006). High level of cryptic species diversity revealed by sympatric lineages of Southeast Asian forest frogs. Biol Lett 2: 470–474.
  • Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004). Status and trends of amphibian declines and extinctions worldwide. Science 306: 1783–1786.
  • Sumida M, Kondo Y, Kanamori Y, Nishioka M (2002). Inter- and intraspecific evolutionary relationships of the rice frog Rana limnocharis and the allied species R. cancrivora inferred from crossing experiments and mitochondrial DNA sequences of the 12S and 16S rRNA genes. Mol Phylogenet Evol 25: 293–305.
  • Sumida M, Kotaki M, Islam MM, Djong HT, Igawa T, Kondo Y, Matsui M, Anslem, Khonsue DSW, Nishioka M (2007). Evolutionary relationships and reproductive isolating mechanisms in the rice frog (Fejervarya limnocharis) species complex from Sri
  • Lanka, Thailand, Taiwan and Japan, inferred from mtDNA gene sequences, allozymes, and crossing experiments. Zool Sci 24: 547–562. Tamura K, Dudley J, Nei M, Kumar S (2007). MEGA 4.0: Molecular
  • Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596–1599.
  • Tanabe AS (2007). Kakusan: a computer program to automate the selection of a nucleotide substitution model and the configuration of a mixed model on multilocus data. Mole Ecol Notes 7: 962–964.
  • Tautz D, Arctander P, Minelli A, Thomas RH, Vogler AP (2003). A plea for DNA taxonomy. Trends Ecol Evol 18: 70–74.
  • Thompson JD, Higgins DG, Gibson TJ (1994). ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680.
  • Turner H, Hovenkamp P, Welzen PCV (2001). Biogeography of
  • Southeast Asia and the West Pacific. J Biogeogr 28: 217–230. Vences M, Thomas M, Bonett RM, Vieites DR (2005a). Deciphering amphibian diversity through DNA barcoding: chances and challenges. Phil Trans R Soc B 360: 1859–1868.
  • Vences M, Thomas M, Meijden AVD, Chiari Y, Vieites DR (2005b).
  • Comparative performance of the 16S rRNA gene in DNA barcoding of amphibians. Front Zool 2: 5. Vieites DR, Wollenberg KC, Andreone F, Köhler J, Glaw F, Vences M (2009). Vast underestimation of Madagascar’s biodiversity evidenced by an integrative amphibian inventory. Proc Natl
  • Acad Sci USA (PNAS), 106: 8267–8272.
  • Vogt T (1911). Beitrag zur Amphibien-fauna der Insel Formosa.
  • Sitzungsberichte der Gesellschaft Naturforschender Freunde zu Berlin 1911: 179-184 (in German).
  • Wright S (1940). The statistical consequences of Mendelian Heredity in relation to speciation. In: Huxley J, editor. The New
  • Bossuyt and Milinkovitch, 2000
  • Meegaskumbura et al., 2009
  • Meegaskumbura et al., 2009 FJ788167 FJ788168 AY141833 GQ285674 Lie et al., 2009 Lie et al., 2009 Biju and Bossuyt, 2009 Gururaja et al., 2007 India: Western Ghats AY753560 Ra. travancoricus Ra. nerostagona Ra. anili Ra. dubois Ra. beddomii Ra. graminirupes Ra. glandulosus Ra. glandulosus Ra. bobingeri
  • Indonesia: Sulawesi Island AY326060
  • Meegaskumbura et al., 2010
  • Meegaskumbura et al., 2010
  • Meegaskumbura et al., 2010 Meenakshi et al., 2009 Brown et al., 2010
  • Meegaskumbura et al., 2010
  • Meegaskumbura et al., 2010
  • Meegaskumbura et al., 2010
  • Meegaskumbura et al., 2010
  • Darst and Cannatella, 2004 Lie et al., 2008 Lie et al., 2008 Lie et al., 2008 Lie et al., 2008 Sano et al., 2005 Lie et al., 2008
  • Meegaskumbura et al., 2010
  • Meegaskumbura et al., 2010 FMNH 235047 FMNH 231366 FMNH 235741 M 3003 AMNHA 161405 EU215533 EU215537 EU215535 AB202078 EU215544 GQ204712 GQ204714 GQ204711 GQ204715 GU136112 DQ283049 GQ204719 GQ204718 EU215529 SN 030035 FMNH 253114 ZRC 5273 SCUM 37941C FMNH 253934
  • Meegaskumbura et al., 2010
  • Meegaskumbura et al., 2010 Lie et al., 2008
  • Thailand: Krabi Province Malaysia: Selangor Malaysia: Sabah Papua New Guinea: nr. Haia DQ283203
  • Bangladesh: Mymensingh Vietnam: Tram Lap Cambodia: Siem Reap Province Vietnam: Tram Lap Indonesia: Java Vietnam: Ha Tinh Vietnam: Vinh Phu Vietnam: Tram Lap Japan: Isehara China: Hong Kong China: Fujian Vietnam: Cao Bang Province DQ204486 Thailand: Narathiwat Malaysia: Perak
  • China: Sichuann province DQ283394 EF453748 DQ650566 EF453751 DQ650596 EF453752 EF453754 AB511287 EF453747 EF453750 EF453746 EF453749 EF453745 EF487449 DQ650428 EF487483 EF487520 EF487456 Inger et al., 2009 Frost et al., 2006 Hasan et al., 2012 Chen et al., 2005 Frost et al., 2006 Chen et al., 2005
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