Natural History and Reproductive Data of Kurixalus yangi (Anura: Rhacophoridae) in Nagaland, India

L. Nzano Humtsoe, Sabitry Bordoloi, Annemarie Ohler, Stéphane Grosjean

Abstract


The genus Kurixalus Ye, Fei et Dubois, 1999 (Rhacophoridae Hoffman, 1932) is a small and taxonomically difficult group of treefrogs for which biological and reproductive data are missing for most of the species. A recent study of the K. odontotarsus species group (Yu et al., 2017a) revealed numerous undescribed lineages. Among them a lineage comprising specimens from Myanmar and western Yunnan, China was described as K. yangi. We report here the presence of a population of this species from Nagaland, North East India, identified by DNA barcoding of the 16S rRNA gene and morphology. A pair of adults found in amplexus is described morphologically. Data on reproduction and developmental mode were until now unknown for the continental species of this genus. Observation of reproduction in the field of K. yangi from Nagaland provided us data on its reproductive activity including spawning behavior and reproductive mode, and details on the larval developmental timing. The tadpole of this species is described for the first time including buccal anatomy. Adults are commonly found in the stumps of bamboo internodes. They breed in forest ponds, temporary rain pools or rain water tanks. Breeding activity starts from mid-April till late part of July. Unpigmented eggs measure 2.4 – 2.7 mm and are laid underwater. Under natural conditions (air temperature 18 – 30°C, water temperature 12 – 24°C), the frog complete its larval life cycle in 47 days. The tadpole shows a «classical» pond-dwelling morphology and reproductive mode. These reproductive data are compared to the Taiwanese species for which the developmental mode is well known and the evolution of the reproductive modes within the genus is discussed.

Keywords


development; morphology; North East India; spawning; tadpole

Full Text:

PDF

References


Altig R. and Johnston G. F. (1989), «Guilds of anuran larvae: Relationships among developmental modes, morphologies, and habitats», Herpetol. Monogr., 3, 81 – 109.

Altig R. and McDiarmid R. W. (1999), «Body plan. Development and morphology», in: R. W. McDiarmid and R. Altig (eds.), Tadpoles. The Biology of Anuran Larvae, The University of Chicago Press, Chicago – London, pp. 24 – 51.

Annandale N. (1912), «Zoological results of the Abor Expedition, 1911 – 1912. I. Batrachia», Rec. Indian Mus., 8, 7 – 36, pl. II – IV.

Ao J. M., Bordoloi S., and Ohler A. (2003), «Amphibian fauna of Nagaland with nineteen new records from the state including five new records for India», Zoo’s Print J., 18(6), 1117 – 1125.

Bahir M. M., Meegaskumbura M., Manamendra-Arachchi K., Schneider C. J., and Pethiyagoda R. (2005), «Reproduction and terrestrial direct development in Sri Lankan shrub frogs (Ranidae: Rhacophorinae: Philautus)», Raffles Bull. Zool., 12(Suppl.), 339 – 350.

Biju S. D., Mahony S., and Kamei R. G. (2010), «Description of two new species of torrent frog, Amolops Cope (Anura: Ranidae) from a degrading forest in the northeast Indian state of Nagaland», Zootaxa, 2408, 31 – 46.

Boettger O. (1895), «Neue Frosche und Schlangen von den Liu-Kiu Inseln», Zool. Anz., 18(479), 266 – 270.

Bortamuli T., Bordoloi S., Ohler A., and Grosjean S. (2010), «External morphology, buccopharyngeal anatomy, growth rate and larval period of the tadpoles of two Asian Ranidae (Amphibia: Anura), Humerana humeralis (Boulenger, 1887) and Sylvirana leptoglossa (Cope, 1868)», J. Nat. Hist., 44(7 – 8), 421 – 445.

Boulenger G. A. (1882), Catalogue of the Batrachia Salientia s. Ecaudata in the collection of the British Museum. Second edition, Taylor and Francis, London.

Boulenger G. A. (1893), «Concluding report on the reptiles and batrachians obtained in Burma by Signor L. Fea, dealing with the collection made in Pegu and Karin Hills in 1887 – 88», Ann. Mus. Civ. Stor. Nat. Genova. Ser. 2, 13, 304 – 347, pl. VII – XII.

Bourret R. (1942), Les batraciens de l’Indochine, Institut Océanographique de l’Indochine.

Brown W. C and Alcala A. C. (1983), «Modes of reproduction of Philippine anurans», in: A. G. J. Rhodin and K. Miyata (eds.), Advances in Herpetology and Evolutionary Biology, Museum of Comparative Zoology, Cambridge, pp. 416 – 428.

Chanda S. K. (1994), «Anuran (Amphibia) fauna of Northeast India», Mem. Zool. Surv. India, 18, i – vi + 1 – 143 + 21 maps.

Chanda S. K. (2006), «Amphibian», Zoological Survey of India. Fauna of Nagaland, State Fauna Series, 12, 427 – 432.

Chou W.-h. and Lin J.-y. (1997), «Tadpoles of Taiwan», Nat. Mus. Nat. Sci. Spec. Publ., 7, 1 – 98.

Das A., Chetia M., Dutta S. K., and Sengupta S. (2013), «A new species of Duttaphrynus (Anura: Bufonidae) from Northeast India», Zootaxa, 3646, 336 – 348.

Das I. and Chanda S. (2000), «A new species of Scutiger (Anura: Megophryidae) from Nagaland, north-eastern India», Herpetol. J., 10(2), 69 – 72.

Das I. and Dutta S. K. (1998), «Checklist of the amphibians of India, with English common names», Hamadryad, 23(1), 63 – 68.

Delorme M., Dubois A., Grosjean S., and Ohler A. (2005), «Une nouvelle classification générique et subgénérique de la tribu des Philautini (Amphibia, Anura, Ranidae, Rhacophorinae)», Bull. Mens. Soc. Linn. Lyon, 74(5), 165 – 171.

Dubois A. (1995), «Keratodont formula in anuran tadpoles: proposals for standardization», J. Zool. Syst. Evol. Res., 33(2), I – XV.

Dubois A. (2004), «Development pathway, speciation and supraspecific taxonomy in amphibians. 2. Developmental pathway, hybridizability and generic taxonomy», Alytes, 22(1 – 2), 38 – 52.

Duellman W. E. and Treub L. (1986), Biology of Amphibians, McGraw-Hill, New York.

Fei L. (1999), Atlas of Amphibians of China, Henan Publishing House of Science and Technology, Zhengzhou.

Frost D. R., Grant T., Faivovich J., Bain R. H., Haas A., Haddad C. F. B., De Sa R. O., Channing A., Wilkinson M., Donnellan S. C., Raxworthy C. J., Campbell J. A., Blotto B. L., Moler P., Drewes R. C., Nussbaum R. A., Lynch J. D., Green D. M., and Wheeler W. C. (2006), «The amphibian tree of life», Bull. Am. Mus. Nat. Hist., 297, 1 – 370.

Frost D. R. (2019), Amphibian Species of the World: an Online Reference. Version 6.0, American Museum of Natural History, New York, USA, http://research.amnh.org/herpetology/amphibia/index.html (accessed on January 30, 2019).

Gosner K. L. (1960), «A simplified table for staging anuran embryos and larvae with notes on identification», Herpetologica, 16(3), 183 – 190.

Grosjean S. (2004), Apport des caractиres larvaires à la phylogénie des Amphibiens Anoures. Cas de deux familles: les Megophryidae et les Ranidae. PhD Thesis, Muséum national d’Histoire naturelle, Paris, France.

Grosjean S. (2006 «2005»), «The choice of external morphological characters and developmental stages for tadpole-based anuran taxonomy: a case study in Rana (Sylvirana) nigrovittata (Blyth, 1855) (Amphibia, Anura, Ranidae)», Contrib. Zool., 74(1 – 2), 61 – 76.

Grosjean S., Delorme M., Dubois A., and Ohler A. (2008), «Evolution of reproduction in the Rhacophoridae (Amphibia, Anura)», J. Zool. Syst. Evol. Res., 46(2), 169 – 176.

Hall T. A. (1999), «BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT», Nucl. Acids Symp. Ser., 41, 95 – 98.

Humtsoe L. N., Bordoloi S., Ohler A., and Dubois A. (2008), «Rediscovery of a long known species, Ixalus lateralis Anderson, 1871», Zootaxa, 1921, 24 – 34.

Inger R. F. (1999), «Distribution of amphibians in Southern Asia and adjacent islands», in: W. E. Duellman (ed.), Patterns of distribution of Amphibians: A global perspective, The Johns Hopkins University Press, Baltimore and London, pp. 445 – 482.

Inger R. F., Orlov N. L., and Darevsky I. (1999), «Frogs of Vietnam: A report on new collections», Fieldiana Zool. N. S., 92, 1 – 46.

Kamei R. G., Wikinson M., Gower D. J., and Biju S. D. (2009), «Three new species of striped Ichthyophis (Amphibia: Gymnophiona: Ichthyophiidae) from the northeast India states of Manipur and Nagaland», Zootaxa, 2267, 26 – 42.

Kamei R. G., Gower D. J., Wikinson M., and Biju S. D. (2013), «Systematics of the caecilian family Chikilidae (Amphibia: Gymnophiona) with the description of three new species of Chikila from northeast India», Zootaxa, 3666, 401 – 435.

Kiyasetuo and Khare M. K. (1987), «A new record of Rhacophorus bisacculus Taylor, from North Eastern hills of India», J. Assam Sci. Soc., 29(1), 16 – 19.

Kumar S., Stecher G., and Tamura K. (2016), «MEGA7: Molecular Evolutionary Genetics Analysis. Ver. 7.0 for bigger datasets», Mol. Biol. Evol., 33(7), 1870 – 1874.

Kuramoto M. and Wang C.-S. (1987), «A new rhacophorid treefrog from Taiwan, with comparisons to Chirixalus eiffingeri (Anura, Rhacophoridae)», Copeia, 1987(4), 931 – 942.

Lehtinen R. M. and Nussbaum R. A. (2003), «Parental care: a phylogenetic perspective», in: B. G. M. Jamieson (ed.), Reproductive Biology and Phylogeny of Anura, Science Publishers, Inc., Plymouth, pp. 343 – 386.

Li J.-T., Che J., Bain R. H., Zhao E.-M., and Zhang Y.-P. (2008), «Molecular phylogeny of Rhacophoridae (Anura): A framework of taxonomic reassignment of species within the genera Aquixalus, Chiromantis, Rhacophorus, and Philautus», Mol. Phylogen. Evol., 48(1), 302 – 312.

Li J.-T., Che J., Murphy R. W., Zhao H., Zhao E.-M., Rao D.-Q., and Zhang Y.-P. (2009), «New insights to the molecular phylogenetics and generic assessment in the Rhacophoridae (Amphibia: Anura) based on five nuclear and three mitochondrial genes, with comments on the evolution of reproduction», Mol. Phylogen. Evol., 53(2), 509 – 522.

Lv Y.-Y., He K., Klaus S., Brown R. M., and Li J.-T. (2018), «A comprehensive phylogeny of the genus Kurixalus (Rhacophoridae, Anura) sheds light on the geographical range evolution of frilled swamp treefrogs», Mol. Phylogen. Evol., 121, 224 – 232.

Liem S. S. (1970), «The morphology, systematics, and evolution of the Old World treefrogs (Rhacophoridae and Hyperoliidae)», Fieldiana Zool., 57, i – vii + 1 – 145.

Maeda M. and Matsui M. (1989), Frogs and Toads of Japan, Bun-Ichi Sogo Shuppan Co., Ltd., Tokyo.

Mathew R. and Sen N. (2007), «Description of two new species of Xenophrys (Amphibia: Anura: Megophryidae) from north-east India», Cobra, 1, 18 – 28.

Mathew R. and Sen N. (2009), «Studies on little known Amphibian species of North East India», Rec. Zool. Surv. India Occ. Pap., 293, 1 – 64, 23 pl.

Matsui M., Kawahara Y., Eto K., Hamidy A., Ahmad N., and Hossman M. Y. B. (2018), «Distinct species status of Kurixalus chaseni (Rhacophoridae, Anura) as revealed by mitochondrial phylogeny», Alytes, 36, 170 – 177.

Meegaskumbura M., Bossuyt F., Pethiyagoda R., Manamendra-Arachchi K., Bahir M. M., and Schneider C. J. (2002), «Sri Lanka: an amphibian hotspot», Science, 298(5592), 379.

Myers N., Mittermeier R. A., Mittermeier C. G., da Fonseca G. A. B., and Kent J. (2000), «Biodiversity hotspots for conservation priorities», Nature, 403, 853 – 858.

Nguyen V. S., Ho T. C., and Nguyen Q. T. (2005), Danh luc ech nhai va bo sat Viet Nam [A Checklist of Amphibians and Reptiles of Vietnam], Nha Xuat Ban Hong Nghiep, Hanoi.

Ohler A. (1996), «Systematics, morphometrics and biogeography of the genus Aubria (Ranidae, Pyxicephalinae)», Alytes, 13(4), 141 – 166.

Ohler A., Swan S. R., and Daltry J. C. (2002), «A recent survey on the amphibian fauna of the Cardamom Mountains, Southwest Cambodia with descriptions of three new species», Raffles Bull. Zool., 50(2), 465 – 481.

Orlov N. L., Dutta S. K., Ghate H. V., and Kent Y. (2006), «New species of Theloderma from Kon Tum Province (Vietnam) and Nagaland state (India) [Anura: Rhacophoridae]», Russ. J. Herpetol., 13(2), 135 – 154.

Orlow N. L. and Ho T. C. (2000), «Die Ruder-bzw. Flugfrösche der Gattungen Polypedates Tschudi, 1838 and Rhacophorus Kuhl & Van Hasselt, 1822 der Bergwälder Vietnams. Teil 2», Herpetofauna, 22(126), 5 – 15.

Orton G. L. (1953), «The systematic of vertebrate larvae», Syst. Zool., 2(2), 63 – 75.

Palumbi S. R. (1996), «Nucleic acids II: the polymerase chain reaction», in: D. M. Hillis, C. Moritz & B. K. Mable (eds.), Molecular Systematics. Second edition, Sinauer Associates, Inc., Sunderland, Massachusetts, pp. 205 – 247.

Pawar S. and Birand A. (2001), A survey of amphibians, reptiles, and birds in Northeast India. CERC Technical Report 6, Centre for Ecological Research and Conservation, Mysore.

Rowley J. J. L., Tran D. T. A., Le D. T. T., Hoang H. D., and Altig R. (2012), «The strangest tadpole: the oophagous, tree-hole dwelling tadpole of Rhacophorus vampyrus (Anura: Rhacophoridae) from Vietnam», J. Nat. Hist., 46(47 – 48), 2969 – 2978.

Salthe S. N. and Duellman W. E. (1973), «Quantitative constraints associated with reproductive mode in anurans», in: J. L. Vial (ed.), Evolutionary Biology of the Anurans: Contemporary Research on Major Problems, University Missouri Press, Columbia, pp. 229 – 249.

Sen N. (2004), «Further notes on statewise distribution of the amphibian fauna of North East India», Rec. Zool. Surv. India, 102(1 – 2), 105 – 112.

Sengupta S., Choudhury N. K., and Das I. (2001), «Leptobrachium smithi Matsui, Nabhitabhata & Panha, 1999 (Anura: Megophryidae), a new record for India», J. Bombay Nat. Hist. Soc., 98(2), 289 – 291.

Swofford D. L. (2001), PAUP*: phylogenetic analysis using parcimony (*and other methods). Ver. 4.0b10 for 32-bit Microsoft Windows, Sinauer Associates, Sunderland, MA.

Ueda H. (1986), «Reproduction of Chirixalus eiffingeri (Boettger)», Sci. Report Lab. Amph. Biol. Hiroshima Univ., 8, 109 – 116.

van Dijk P. P., Ashton P., and Jinshuang M. (1999), «Indo-Burma», in: R. A. Mittermeier (ed.), Hotspots: Earth’s Biologically Richest and Most Endangered Terrestrial Ecoregions, Cemex, S. A. & Conservation International, Mexico City, pp. 319 – 337.

Vences M., Thomas M., Bonett R. M., and Vieites D. R. (2005a), «Deciphering amphibian diversity through DNA barcoding: chances and challenges», Phil. Trans. Roy. Soc. B, 360(1462), 1859 – 1868.

Vences M., Thomas M., van der Meijden A., Chiari Y., and Vieites D. R. (2005b), «Comparative performance of the 16S rRNA gene in DNA barcoding of amphibians», Front. Zool., 2, 5.

Wassersug R. J. (1976), «Oral morphology of anuran larvae: terminology and general description», Occas. Pap Mus. Nat. Hist. Univ. Kansas, 48, 1 – 23.

Wells K. D. (2007), The Ecology and Behavior of Amphibians, The Univ. of Chicago Press, Chicago.

Wilkinson J. A., Drewes R. C., and Tatum O. L. (2002), «A molecular phylogenetic analysis of the family Rhacophoridae with an emphasis on the Asian and African genera», Mol. Phylogen. Evol., 24(2), 265 – 273.

Wolf S. (1936), «Revision der Untergattung Rhacophorus (ausschliesslich der Madagaskar-Formen)», Bull. Raffles Mus., 12, 137 – 217.

Wu S.-P., Huang C.-C., Tsai C.-L., Lin T.-E., Jhang J.-J., and Wu S.-H. (2016), «Systematic revision of the Taiwanese genus Kurixalus members with a description of two new endemic species (Anura, Rhacophoridae)», ZooKeys, 557, 121 – 153.

Yu G., Hui H., Rao D., and Yang J. (2018), «A new species of Kurixalus from western Yunnan, China (Anura, Rhacophoridae)», ZooKeys, 770, 211 – 226.

Yu G., Rao D., Matsui M., and Yang J. (2017a), «Coalescent-based delimitation outperforms distance-based methods for delineating less divergent species: the case of Kurixalus odontotarsus species group», Sci. Reports, 7, 16124.

Yu G., Rao D., Yang J., and Zhang M. (2008), «Phylogenetic relationships among Rhacophorinae (Rhacophoridae, Anura, Amphibia), with an emphasis on the Chinese species», Zool. J. Linn. Soc., 153(4), 733 – 749.

Yu G., Rao D., Zhang M., and Yang J. (2009), «Re-examination of the phylogeny of Rhacophoridae (Anura) based on mitochondrial and nuclear DNA», Mol. Phylogen. Evol., 50(3), 571 – 579.

Yu G., Wang J., Hou M., Rao D., and Yang J. (2017b), «A new species of the genus Kurixalus from Yunnan, China (Anura, Rhacophoridae)», ZooKeys, 694, 71 – 93.

Yu G., Zhang M., and Yang J. (2010), «A species boundary within the Chinese Kurixalus odontotarsus species group (Anura: Rhacophoridae): new insights from molecular evidence», Mol. Phylogen. Evol., 56, 942 – 950.

Yu G., Zhang M., and Yang J. (2013), «Molecular evidence for taxonomy of Rhacophorus appendiculatus and Kurixalus species from northern Vietnam, with comments on systematics of Kurixalus and Gracixalus (Anura: Rhacophoridae)», Biochem. Syst. Ecol., 47, 31 – 37.

Ziegler T. and Vences M. (2002), «The tadpole of Rhacophorus verrucosus Boulenger, 1893 from Vietnam (Amphibia: Anura: Rhacophoridae)», Faun. Abhandl. Staat. Mus. Tierk. Dresden, 22, 319 – 327.




DOI: https://doi.org/10.30906/1026-2296-2020-27-5-257-274

Refbacks

  • There are currently no refbacks.


You can subscribe to the print or electronic version of the journal on the site of EastView Company. If you have any questions, please write to the email sales@ivis.ru