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Seven New Species of Night Frogs (Anura, Nyctibatrachidae) from the Western Ghats Biodiversity Hotspot of India, with Remarkably High Diversity of Diminutive Forms

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Seven New Species of Night Frogs (Anura, Nyctibatrachidae) from the Western Ghats Biodiversity Hotspot of India, with Remarkably High Diversity of Diminutive Forms Seven new species of Night Frogs (Anura, Nyctibatrachidae) from the Western Ghats Biodiversity Hotspot of India, with remarkably high diversity of diminutive forms Sonali Garg1, Robin Suyesh1, Sandeep Sukesan2 and SD Biju1 1 Systematics Lab, Department of Environmental Studies, University of Delhi, Delhi, India 2 Kerala Forest Department, Periyar Tiger Reserve, Kerala, India ABSTRACT The Night Frog genus Nyctibatrachus (Family Nyctibatrachidae) represents an endemic anuran lineage of the Western Ghats Biodiversity Hotspot, India. Until now, it included 28 recognised species, of which more than half were described recently over the last five years. Our amphibian explorations have further revealed the presence of undescribed species of Nights Frogs in the southern Western Ghats. Based on integrated molecular, morphological and bioacoustic evidence, seven new species are formally described here as Nyctibatrachus athirappillyensis sp. nov., Nyctibatrachus manalari sp. nov., Nyctibatrachus pulivijayani sp. nov., Nyctibatrachus radcliffei sp. nov., Nyctibatrachus robinmoorei sp. nov., Nyctibatrachus sabarimalai sp. nov. and Nyctibatrachus webilla sp. nov., thereby bringing the total number of valid Nyctibatrachus species to 35 and increasing the former diversity estimates by a quarter. Detailed morphological descriptions, comparisons with other members of the genus, natural history notes, and genetic relationships inferred from phylogenetic analyses of a mitochondrial dataset are presented for all the new species. Additionally, characteristics of male advertisement calls are described for four new and three previously known species. Among the new species, six are currently known to be geographically restricted to low and mid elevation Submitted 6 October 2016 regions south of Palghat gap in the states of Kerala and Tamil Nadu, and one is Accepted 20 January 2017 probably endemic to high-elevation mountain streams slightly northward of the gap in Published 21 February 2017 Tamil Nadu. Interestingly, four new species are also among the smallest known Indian Corresponding author frogs. Hence, our discovery of several new species, particularly of easily overlooked SD Biju, [email protected] miniaturized forms, reiterates that the known amphibian diversity of the Western Ghats Academic editor of India still remains underestimated. Marcio Pie Additional Information and Declarations can be found on Subjects Biodiversity, Taxonomy, Zoology page 44 Keywords Amphibians, Ancient lineage, Bioacoustics, DNA barcoding, Endemism, Integrative DOI 10.7717/peerj.3007 systematics, Miniature frogs, Nyctibatrachus, Species diversity, Western Ghats Copyright 2017 Garg et al. INTRODUCTION Distributed under The mountains of the Western Ghats in Peninsular India are a global biodiversity Creative Commons CC-BY 4.0 hotspot (Myers et al., 2000; Mittermeier et al., 2004). Over 92% of the presently known OPEN ACCESS 225 amphibian species (Frost, 2016) of the Western Ghats are endemic to this region. How to cite this article Garg et al. (2017), Seven new species of Night Frogs (Anura, Nyctibatrachidae) from the Western Ghats Biodiver- sity Hotspot of India, with remarkably high diversity of diminutive forms. PeerJ 5:e3007; DOI 10.7717/peerj.3007 An exponential two-fold increase in the number of species over the last decade and a half (2001–2015) has evidenced that a vast majority of amphibians of this region had remained undiscovered until recently (Biju, 2001), and the trends also suggest that the actual diversity may still be higher than currently estimated (Biju et al., 2014a). The present rate of species description from the Western Ghats is also comparable to the eight ‘hottest’ biodiversity hotspots of the world (Myers et al., 2000). Between 2006–2015, 1,581 new species of amphibians were described globally (AmphibiaWeb, 2016). Of these maximum are from the Brazilian Atlantic Forest (approximately 182) and the second highest from the Western Ghats-Sri Lanka (approximately 159), as per estimates based on AmphibiaWeb (2016), Frost (2016) and Conservation International (2016). The Western Ghats alone also stands at a close fourth position (with 103 new species) after Indo-Burma (approximately 117). Therefore, the Western Ghats can be considered among the leading biodiversity hotspot regions in terms of the number of new amphibian species described over the past decade. Such rapid rates of species discoveries can be attributed to intensified explorations as well as the increased use of molecular tools and integrated systematic approaches (e.g., Glaw & Köhler, 1998; Hanken, 1999; Hebert et al., 2003; Köhler et al., 2005; Vieites et al., 2009). These have also aided comprehensive taxonomic revisions of various amphibian groups in the Western Ghats (e.g., Biju & Bossuyt, 2009; Biju et al., 2011; Gower et al., 2011; Biju et al., 2014a; Biju et al., 2014b) thereby providing stable and reliable data for further identification of new taxa. The anuran family Nyctibatrachidae is considered to be an ancient lineage of frogs that originated on the Indian landmass between the Cretaceous (Middle to Upper) and Palaeocene periods, synchronous with the long period of its isolation from the Gondwana (Roelants, Jiang & Bossuyt, 2004). This relic family comprises of two genera—Lankanectes Dubois & Ohler, 2001 and Nyctibatrachus Boulenger, 1882—which are restricted to Sri Lanka and the Western Ghats of India, respectively. Since the former is a monotypic genus with a single known species (Lankanectes corrugatus) and the latter includes 28 species recognised as valid (Frost, 2016), family Nyctibatrachidae can largely be considered as a radiation of the Western Ghats. Members of the genus Nyctibatrachus, commonly known as Night Frogs (Frank & Ramus, 1995) are known to occur in five states in southern India, with their distribution extending from the southern tip of Indian Peninsula in Tamil Nadu to Kerala, Karnataka, Goa and ending in northern Maharashtra. These frogs can be found in close association with mountain streams or marshes in forests of the Western Ghats (Biju et al., 2011). Their sizes vary from 10–77 mm (Snout-vent length) (Biju et al., 2011), including the 10 mm long Nyctibatrachus minimus, which is the smallest Indian tetrapod described so far (Biju et al., 2007). The Night Frog genus Nyctibatrachus is among the relatively well-studied amphibian groups of the Western Ghats. The first Nyctibatrachus species was described in 1882 along with the recognition of the genus (Boulenger, 1882). Over the next century, another nine species were described (Bhaduri & Kripalani, 1955; Dubois, 1984; Inger et al., 1984; Myers, 1942; Rao, 1920; Rao, 1937; Ravichandran, 1997), and this number was more than doubled by new descriptions during the past decade (Biju et al., 2007; Biju et al., 2011; Das & Kunte, 2005; Dinesh, Radhakrishnan & Bhatta, 2008; Gururaja et al., 2014). A comprehensive Garg et al. (2017), PeerJ, DOI 10.7717/peerj.3007 2/50 systematic revision by Biju et al. (2011) provided taxonomic stability for various previously available names in this genus. The latest studies on Nyctibatrachus frogs have particularly drawn attention towards their natural history, including reproductive behaviour and ecology (e.g., Kunte, 2004; Biju et al., 2011; Gramapurohit, Gosavi & Phuge, 2011; Gururaja et al., 2014; Willaert et al., 2016) and tadpole development (Annandale, 1918; Annandale, 1919; Rao, 1923; Bhaduri & Kripalani, 1955; Pillai, 1978; Priti, Gururaja & Ravikanth, 2015), as well as patterns of distribution and endemism in the Western Ghats (Van Bocxlaer et al., 2012). Male advertisement calls have so far been described for N. major (Kuramoto & Joshy, 2001), N. jog, N. kempholeyensis, N. kumbara (Gururaja et al., 2014) and N. humayuni (Willaert et al., 2016). In the case of N. humayuni, the rare occurrence of female calls has also been documented (Willaert et al., 2016). During our routine amphibian surveys in the Western Ghats (in 2002 and between 2013–2016), we sampled various populations of Nyctibatrachus from the southern Western Ghats states of Kerala and Tamil Nadu, which reveal undescribed diversity of Night Frogs. Based on newly collected material, molecular, morphological and bioacoustic data, here we describe seven new species of Nyctibatrachus from the Western Ghats of India. MATERIALS AND METHODS Field surveys and specimen collection Field surveys and collection of specimens were carried out in 2002 and between 2013– 2016 in forests of Kerala and Tamil Nadu, in southern Western Ghats, India. Adult specimens were collected during both day and night, mostly by locating calling males and sometimes through opportunistic surveys. Geographical coordinates of the sampling localities were recorded on a Garmin 76CSx GPS using the WGS-84 datum. Live animals were photographed, euthanised in MS-222 (Tricaine methane sulphonate), fixed in 4% formalin and preserved in 70% ethanol. Prior to fixation, a portion of the thigh muscle was preserved in absolute ethanol for subsequent molecular analyses. Tissue samples were stored at −20 ◦C in the Systematics Lab, University of Delhi. Type specimens are deposited in the Zoological Survey of India–Western Ghats Regional Centre (ZSI-WGRC), Calicut, and referred specimens are available at the Systematics Lab, University of Delhi (SDBDU), India. The study was conducted with permissions and following guidelines from the responsible authorities in the State Forest Departments of Kerala and Tamil Nadu (Study permits: No.WL12-1830/2009,
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