Abstract
A new species of tree frog of the genus Rhacophorus is described from two different localities on Sulawesi Island, Indonesia. The new species is divergent morphologically and genetically, and is deeply nested within the monophyletic group of endemic Sulawesian Rhacophorus comprising R. edentulus, R. georgii, and R. monticola. The new species has a combination of distinctive morphological characteristics that distinguishes it from other Rhacophorus species, including from other Sulawesian Rhacophorus: medium size SVL 40.4–44.6 mm in males; 48.1–54.2 mm in females, males have sloped snout in lateral view, presence of vomerine teeth, absence of a bony crest in the occipital region of the skull, dorsal skin coarsely granular with white-tipped keratinized asperities, flank with white blotched pattern, dermal flaps absent on limbs, heel without dermal appendage, and tuberculate cloaca. The discovery of the new species enhances knowledge of the diversity of endemic Sulawesian amphibians and requires future conservation efforts, especially in light of ongoing threats such as agricultural expansion.
References
- Alhadi, F., Kaprawi, F., Hamidy, A. & Kirschey, T. (2021) Amfibi Pulau Jawa: Panduan Bergambar dan Identifikasi. Perkumpulan Amfibi Reptil Sumatra, Jakarta and NABU, Berlin, 214 pp.
- Biju, S.D., Kamei, R.G., Mahony, S., Thomas, A., Garg, S., Sircar, G. & Suyesh, R. (2013) Taxonomic review of the tree frog genus Rhacophorus from the Western Ghats, India (Anura: Rhacophoridae), with description of ontogenetic colour changes and reproductive behaviour. Zootaxa, 3636 (2), 257–289. https://doi.org/10.11646/zootaxa.3636.2.3
- Boulenger, G.A. (1896) Descriptions of new reptiles and batrachians collected in Celebes by Drs. P. and F. Sarasin. Annals and Magazine of Natural History, Series 6, 17 (101), 393–395. https://doi.org/10.1080/00222939608680385
- Brown, W.C. & Alcala, A.C. (1994) Philippine frogs of family Rhacophoridae. Proceeding of the Californian Academy of Sciences, 48, 185–220.
- Chan, K.O. & Gismer, L.L. (2010) Reassessment of the Reinwardt`s Gliding Frog, Rhacophorus reindwardtii (Schlegel 1840) (Anura: Rhacophoridae) in Southern Thailand and Peninsular Malaysia and its re-description as a new species. Zootaxa, 2505 (1), 40–50. https://doi.org/10.11646/zootaxa.2505.1.2
- Chan, K.O., Grismer, L.L. & Brown, R.M. (2018) Comprehensive multi-locus phylogeny of Old World tree frogs (Anura: Rhacophoridae) reveals taxonomic uncertainties and potential cases of over-and underestimation of species diversity. Molecular Phylogenetics and Evolution, 127, 1010–1019. https://doi.org/10.1016/j.ympev.2018.07.005
- Che, J., Jiang, K., Yan, F. & Zhang, Y. (2020) Amphibians and reptiles in Tibet. Science Press, Beijing, 803 pp.
- Clement, M., Snell, Q., Walker, P., Posada, D. & Crandall, K. (2002) TCS: Estimating gene genealogies. Parallel and Distributed Processing Symposium, International Proceedings, 2, 184. https://doi.org/10.1109/IPDPS.2002.1016585
- Darst, C.R. & Cannatella, D.C. (2004) Novel relationships among hyloid frogs inferred from 12S and 16S mitochondrial DNA sequences. Molecular Phylogenetics and Evolution, 32, 462–475. https://doi.org/10.1016/j.ympev.2003.09.003
- Das, I. & Haas, A. (2005) A new species of Rhacophorus (Anura: Rhacophoridae) from Gunung Gading, Sarawak. The Raffles Bulletin of Zoology, 53 (2), 257–263.
- Duellman, W.E. & Trueb, L. (1986) Biology of Amphibians. The John Hopkins University Press, Baltimore, Maryland, and London, 670 pp. https://doi.org/10.2307/1445022
- Evans, B.J., Brown, R.M. McGuire, J.A., Supriatna, J., Andayani, N., Diesmos, A., Melnick, D.J. & Cannatella, D.C. (2003) Phylogenetics of fanged frogs: testing biogeographical hypotheses at the interface of the Asian and Australian faunal zones. Systematic Biology, 52 (6), 794–819. https://doi.org/10.1093/sysbio/52.6.794
- Evans, B.J., Morales, J.C., Supriatna, J. & Melnick, D.J. (1999) Origin of the Sulawesi macaques (Cercopithecidae, Macaca) as inferred from a mitochondrial DNA phylogeny. Biological Journal of Linnaean Society, 66 (4), 539–560. https://doi.org/10.1111/j.1095-8312.1999.tb01925.x
- Frederick, J.H., Iskandar, D.T., Riyanto, A., Hamidy, A., Reilly, S.B., Stubbs, A.L., Bloch, L.M., Bach, B & McGuire, J.A. (2023) A new species of terrestrially-nesting fanged frog (Anura: Dicroglossidae) from Sulawesi Island, Indonesia. PLoS ONE, 18 (12), e0292598. https://doi.org/10.1371/journal.pone.0292598
- Frost, D.R. (1985) Amphibian Species of the World. A Taxonomic and Geographical Reference. Association of Systematics Collections and Allen Press. Lawrence, Kansas, 732 pp.
- Frost, D.R. (2024) Amphibian Species of the World: an Online Reference. Version 6.1. American Museum of Natural History, New York. Electronic Database accessible. Available from: https://amphibiansoftheworld.amnh.org/index.php (accessed 2 March 2024).
- Gillespie, G.R., Anstis, M., Howard, S.D, Lockie, D. (2007) Description of the Tadpole of the Rhacophorid Frog Rhacophorus georgii Roux (Rhacophoridae) from Sulawesi, Indonesia. Journal of Herpetology, 41 (1), 150–153. https://doi.org/10.1670/0022-1511(2007)41[150:DOTTOT]2.0.CO;2
- Gillespie, G.R., Lockie, D., Scroggie, M.P. & Iskandar, D.T. (2004) Habitat use by stream breeding frogs in southeast Sulawesi, with some preliminary observations on community organization. Journal of Tropical Ecology, 20, 439–448. https://doi.org/10.1017/S0266467404001361
- Gosner, K.L. (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica, 16 (3), 183–190.
- Haas, A. & Das, I. (2011) Describing east Malaysian tadpole diversity: status and recommendations for standards and procedures associated with larval amphibian description and documentation. Bonner Zoologische Monographien, 57, 29–46.
- Haas, A., Hertwig, S.T., Krings, W., Braskamp, E., Dehling, J.M., Min, P.Y., Jankowsi, A., Schweizer, M. & Das, I. (2012) Description of three Rhacophorus tadpoles (Lissamphibia: Anura: Rhacophoridae) from Sarawak, Malaysia (Borneo). Zootaxa, 3328 (1), 1–19. https://doi.org/10.11646/zootaxa.3328.1.1
- Hamidy, A. & Kurniati, H. (2015) A new species of tree frog genus Rhacophorus from Sumatra, Indonesia (Amphibia, Anura). Zootaxa, 3947 (1), 49–66. https://doi.org/10.11646/zootaxa.3947.1.3
- Hamidy, A., Munir, M., Mumpuni, M., Rahmania, M. & Kholik, A.A. (2018) Detection of cryptic taxa in the genus Leptophryne (Fitzinger, 1843) (Amphibia; Bufonidae) and the description of a new species from Java, Indonesia. Zootaxa, 4450 (4), 427–444. https://doi.org/10.11646/zootaxa.4450.4.2
- Harvey, M.B., Pemberton, A.J. & Smith, E.N. (2002) New and poorly known parachuting frogs (Rhacophoridae: Rhacophorus) from Sumatra and Java. Herpetological Monographs, 16 (1), 46–92. https://doi.org/10.1655/0733-1347(2002)016[0046:NAPKPF]2.0.CO;2
- Hertwig, S.T., Schweizer, M., Das, I. & Haas, A. (2013) Diversification in a biodiversity hotspot-the evolution of Southeast Asian rhacophorid tree frogs on Borneo (Amphibia: Anura: Rhacophoridae). Molecular Phylogenetics and Evolution, 68, 567–581. https://doi.org/10.1016/j.ympev.2013.04.001
- Hoang, D.T., Chernomor, O., Haeseler, A.V., Minh, B.Q. & Vinh, L.S. (2017) UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology Evolution, 35, 518–522. https://doi.org/10.1093/molbev/msx281
- Huelsenbeck, J.P.P. & Hillis, D.M. (1993) Success of phylogenetic methods in the four-taxon case. Systematic Biology, 42, 247–264. https://doi.org/10.1093/sysbio/42.3.247
- in Den Bosch, H.A.J. (1994) On the juvenile forms of Oligodon waandersi (Bleeker, 1860). Mitteilungen aus dem Museum für Naturkunde in Berlin, 70 (2), 301–309. https://doi.org/10.1002/mmnz.19940700209
- Inger, R.F. & Stuebing, R.B. (2005) A Field Guide to the Frogs of Borneo. The Natural History Publications, Kota Kinabalu, Sabah, 201 pp.
- Iskandar, D.T. (1998) The amphibians of Java and Bali. Research and Development Centre for Biology, Lipi, xix + 117 pp., 26 (unnumbered pages of plates) pp.
- Iskandar, D.T., Arifin, U. & Rachmanasah, A. (2011) A new frog (Anura, Dicroglossidae), related to Occidozyga semipalmata Smith, 1927, from the eastern peninsula of Sulawesi, Indonesia. Raffles Bulletin of Zoology, 59 (2), 219–228.
- Iskandar, D.T., Evans, B.J. & McGuire, J.A. (2014) A novel reproductive mode in frogs: A new species of Fanged Frog with internal fertilization and birth of tadpoles. PLoS ONE, 9 (12), e115884, 1–14. https://doi.org/10.1371/journal.pone.0115884
- Jiang, D., Jiang, K., Ren, J., Wu, J. & Li, J. (2019) Resurrection of the genus Leptomantis, with description of a new genus to the family Rhacophoridae (Amphibia: Anura). Asian Herpetological Research, 10 (1), 1–12. https://doi.org/10.16373/j.cnki.ahr.180058
- Katoh, K. & Standley, D.M. (2013) MAFFT Multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30 (4), 772–780. https://doi.org/10.1093/molbev/mst010
- Kuraishi, N., Matsui, M., Hamidy, A., Belabut, D.M., Ahmad, N., Panha, S., Sudin, A., Yong, H.S., Jiang, J.P., Ota, H., Thong, H.T. & Nishikawa, K. (2012) Phylogenetic and taxonomic relationships of the Polypedates leucomystax complex (Amphibia). Zoologica Scripta, 42 (1), 54–70. https://doi.org/10.1111/j.1463-6409.2012.00562.x
- Kurniati, H. (2014) Karakteristik suara Rhacophorus edentulus Mueller, 1984 asal Pegunungan Mekongga, Sulawesi Tenggara (Anura: Rhacophoridae). Jurnal Biologi Indonesia, 11 (1), 21–29
- Kusrini, M.D., Rowley, J.J.L., Khairunnisa, R., Shea, G.M. & Altig, R.I. (2015) The reproductive biology and larvae of the first tadpole-bearing frog, Limnonectes larvaepartus. PLoS ONE, 10 (1), e116154, 1–9. https://doi.org/10.1371/journal.pone.0116154
- Leaché, A.D. & Reeder, T.W. (2002) Molecular systematics of the eastern fence lizard (Sceloporus undulatus): a comparison of parsimony, likelihood, and Bayesian approaches. Systematic Biology, 51 (1), 44–68. https://doi.org/10.1080/106351502753475871
- Leigh, J.W., Bryant, D. (2015) popart: full‐feature software for haplotype network construction. Methods in Ecology and Evolution, 6 (9), 1110–1116. https://doi.org/10.1111/2041-210X.12410
- Li, J.T., Li, Y., Murphy, R.W., Rao, D.Q. & Zhang, Y.P. (2012) Phylogenetic resolution and systematics of the Asian tree frogs, Rhacophorus (Rhacophoridae, Amphibia). Zoological Scripta, 41 (6), 557–570. https://doi.org/10.1111/j.1463-6409.2012.00557.x
- Liem, S.S. (1970) The morphology, systematics and evolution of the old world tree frogs (Rhacophoridae and Hyperoliidae). Fieldiana Zoology, 57, 1–145. https://doi.org/10.5962/bhl.title.2939
- Lleonart, J., Salat, J. & Torres, G.J. (2000) Removing allometric effects of body size in morphological analysis. Journal of Theoretical Biology, 205, 85–93. https://doi.org/10.1006/jtbi.2000.2043
- Malkmus, R., Manthey, U., Vogel, G., Hoffmann, P. & Kosuch, J. (2002) Amphibians & Reptile of Mount Kinabalu (North Borneo). Koeltz Scientific Books, Königstein, 424 pp.
- Matsui, M. (1984) Morphometric variation analyses and revision of the Japanese toads (genus Bufo, Bufonidae). Contributions from the Biological Laboratory, Kyoto University, 26, 209–428.
- Matsui, M., Kawahara, Y., Nishikawa, K., Ikeda, S., Eto, K. & Mizuno, Y. (2019) Molecular phylogeny and evolution of two Rhacophorus species endemic to mainland Japan. Asian Herpetological Research, 10 (2), 86–104. https://doi.org/10.16373/j.cnki.ahr.190015
- Matsui, M., Shimada, T. & Sudin, A. (2013) A new gliding frog of the genus Rhacophorus from Borneo. Current Herpetology, 32 (2), 112–124. https://doi.org/10.5358/hsj.32.112
- Matsui, M., Shimada, T. & Sudin, A. (2014) First record of the tree frog genus Chiromantis from Borneo with the description of a new species (Amphibia: Rhacophoridae). Zoological Science, 31 (1), 45–51. https://doi.org/10.2108/zsj.31.45
- McDiarmid, R.W. & Altig, R. (1999) Tadpoles, the biology of anuran larvae. The University of Chicago Press, Chicago, Illinois, xiv + 444 pp.
- McGuire, J.A., Huang, X., Reilly, S.B., Iskandar, D.T., Wang-Claypool, C.Y., Werning, S., Chong, A.C., Lawata, S.Z.S., Stubbs, A.L., Frederick, J.H., Brown, R.M., Evans, B.J., Arifin, U., Riyanto, A., Hamidy, A., Arida, E., Koo, M.S., Supriatna, J., Andayani, N. & Hall, R. (2023). Species delimitation, phylogenomics, and biogeography of Sulawesi flying lizards: a diversification history complicated by ancient hybridization, cryptic species, and arrested speciation. Systematic Biology, 72, 885–911.
- Meegaskumbura, M., Meegaskumbura, S., Bowatte, G., Manamendra-Arachchi, K., Pethiyagoda, R., Hanken, J. & Schneider, C.J. (2010) Taruga (Anura: Rhacophoridae), a new genus of foam-nesting tree frogs endemic to Sri Lanka. Ceylon Journal of Science (Biological Science), 39 (2), 75–94. https://doi.org/10.4038/cjsbs.v39i2.2995
- Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: IEEE (Ed.), Proceedings of the Gateway Computing Environments Workshop (GCE), New Orleans, Louisiana, 14 November 2010, pp. 1–8. https://doi.org/10.1109/GCE.2010.5676129
- Müller, F. (1894) Reptilien und Amphibien aus Celebes. Verhandlungen der Naturforschenden Gesellschaft in Basel, 10, 825–843.
- Munir, M., Hamidy, A., Farajallah, A. & Smith, E.N. (2018) A new Megophrys Kuhl and van Hasselt (Amphibia: Megophryidae) from southwestern Sumatra, Indonesia. Zootaxa, 4442 (3), 389–412. https://doi.org/10.11646/zootaxa.4442.3.3
- Pettitt, B.A., Bourne, G.R. & Bee, M.A. (2012) Quantitative Acoustic analysis of the Vocal Repertoire of the Golden Rocket Frog (Anomaloglossus beebei). Journal Acoustical Society of America, 131 (6), 4811–4820. https://doi.org/10.1121/1.4714769
- Putri, A.A., Fahri, F. & Annawaty & A.(2018) Deskripsi Katak Terbang Sulawesi, Rhacophorus edentulus (Mueller, 1894) dari Danau Kalimpa’a, Taman Nasional Lore Lindu, Sulawesi, Indonesia : Catatan Habitat dan Distribusi. Natural Science: Journal of Science and Technology, 7 (1), 50–56.
- Putri, A.A., Trilaksono, W., Kurniati, H., Hitch, A. T., Engilis, A.J., Widayati, K.A., Farajallah, A & Hamidy, A. (2023) A new high elevation species of Oreophryne Boettger (Anura: Microhylidae) from Sulawesi, Indonesia. Zootaxa, 5353 (5), 455–467. https://doi.org/10.11646/zootaxa.5353.5.4
- Riyanto, A., Mumpuni, & McGuire, J.A. (2011) Morphometry of striped tree frogs, Polypedates leucomystax (Gravenhorst, 1829) from Indonesia with description of a new species. Russian Journal of Herpetology, 18 (1), 29–35. https://doi.org/10.30906/1026-2296-2011-18-1-29%E2%80%9335
- R Core Team (2020) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. Available from: https://www.R-project.org (accessed 14 October 2024)
- Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M.A. & Hulsenbeck, J.P. (2012) MRBAYES 3.2: Efficient Bayesian phylogenetic inference and model selection across a large model space. Systematic Biology, 61, 539–542. https://doi.org/10.1093/sysbio/sys029
- Roux, J. (1904) Reptilien und Amphibien aus Celebes. Verhandlungen der Naturforschenden Gesellschaft in Basel, 15, 425–433.
- Rueden, C.T., Schindelin, J., Hiner, M.C., DeZonia, B.E., Walter, A.E., Arena, E.T. & Eliceiri, K.W. (2017) ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinformatics, 18 (1), 529. https://doi.org/10.1186/s12859-017-1934-z
- Sano, N., Kurabayashi, A., Fujii, T., Yonekawa, H. & Sumida, M. (2005) Complete nucleotide sequence of the mitochondrial genome of Schlegel’s tree frog Rhacophorus schlegelii (family Rhacophoridae): duplicated control regions and gene rearrangements. Genes & genetic systems, 80 (3), 213–224. https://doi.org/10.1266/ggs.80.213
- Savage, J.M. & Hyer, W.R. (1967) Variation and distribution of the tree frog genus Pyllomedusa in Costa Rica, Central America. Beiträge zur Neotropischen Fauna, 5 (2), 111–131. https://doi.org/10.1080/01650526709360400
- Savage, J.M. & Heyer, W.R. (1997) Digital webbing formulae for anurans: a refinement. Herpetological Review, 28, 131.
- Setiadi. M.I., McGuire, J.A., Brown, R.M., Zubairi, M., Iskandar, D.T., Andayani, N., Supriatna, J. & Evans, B.J. (2011) Adaptive radiation and ecological opportunity in Sulawesi and Philippine fanged frog (Limnonectes) communities. The American Naturalist, 178, 221–240. https://doi.org/10.1086/660830
- Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30 (9), 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
- Streicher, J.W., Hamidy, A., Harvey, M.B., Andres, B., Shaney, K.J., Kurniawan, N. & Smith, E.N. (2014) Mitochondrial DNA reveals a new species of parachuting frog (Rhacophoridae: Rhacophorus) from Sumatra. Zootaxa, 3878 (4), 351–356. https://doi.org/10.11646/zootaxa.3878.4.2
- Streicher, J.W., Harvey, M.B., Sheehy, C.M., Anders, B. & Smith, E.N. (2012) Identification and description of the tadpole of the parachuting frog Rhacophorus catamitus from southern Sumatra, Indonesia. Journal of Herpetology, 46 (4), 503–506. https://doi.org/10.1670/11-086
- Tamura, K., Stecher, G. & Kumar, S. (2021) MEGA11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 38 (7), 3022–3027. https://doi.org/10.1093/molbev/msab120
- Tanabe, A.S. (2011) Kakusan4 and Aminosan: Two programs for comparing nonpartitioned, proportional and separate models for combined molecular phylogenetic analyses of multilocus sequence data. Molecular Ecollogy Resource, 11, 914–921. https://doi.org/10.1111/j.1755-0998.2011.03021.x
- Tao, N.T., Matsui, M., Eto, K. & Orlov, N.L. (2014) A preliminary study of phylogenetic relationships and taxonomic problems of Vietnamese Rhacophorus (Anura: Rhacophoridae). Russian Journal of Herpetology, 21 (4), 274–280. https://doi.org/10.30906/1026-2296-2014-21-4-274-280
- Thorpe, R.S. (1983) A review of the numerical methods for recognizing and analyzing racial differentiation. In: Felsenstein, J. (Ed.), Numerical Taxonomy: NATO Advanced Studies Institute Series. Series G. Ecological sciences. No. 1. Springer Verlag, Berlin and Heidelberg, pp. 404–423. https://doi.org/10.1007/978-3-642-69024-2_43
- Trifinopoulos, J., Nguyen, L., Haeseler, A.V. & Minh, B.Q. (2016) W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research, 14, W222–W234. https://doi.org/10.1093/nar/gkw256
- van Kampen, P.N. (1923) The Amphibia of the Indo-Australian Archipelago. E. J. Brill, Leiden, 304 pp. https://doi.org/10.1163/9789004590182
- Wolf, S. (1936) Revision der Untergattung Rhacophorus (ausschliesslich der Madagaskar-Formen). Bulletin of the Raffles Museum, 12, 137–217.
- Yu, G., Rao, D., Yang, J. & Zhang, M. (2008) Phylogenetic relationships among Rhacophorinae (Rhacophoridae, Anura, Amphibia), with an emphasis on the Chinese species. Zoological Journal of the Linnean Society, 153 (4), 733–749. https://doi.org/10.1111/j.1096-3642.2008.00404.x