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Research Article
The curious case of Charles Darwin’s frog, Rana charlesdarwini Das, 1998: Phylogenetic position and generic placement, with taxonomic insights on other minervaryan frogs (Dicroglossidae: Minervarya) in the Andaman and Nicobar Archipelago
expand article infoSonali Garg, Sivaperuman Chandrakasan§, G. Gokulakrishnan§, C. Gopika, Indraneil Das|, S. D. Biju
‡ University of Delhi, Delhi, India
§ Andaman and Nicobar Regional Centre, Zoological Survey of India, Port Blair, India
| Universiti Malaysia, Sarawak, Malaysia
Open Access

Abstract

Since the description of Charles Darwin’s frog as Rana charlesdarwini in 1998, its generic placement has been a taxonomic enigma. Subsequent studies first transferred this species to the dicroglossid genus Limnonectes, and then considered it as a ceratobatrachid of the genus Ingerana, which has since been moved to the family Dicroglossidae. However, recent works have doubted this generic placement and also suggested the possibility of its sister relationship with the genus Liurana, within Ceratobatrachidae. Nonetheless, there have been no detailed investigations to ascertain the generic placement of this taxon by confirming its phylogenetic position or using integrative taxonomic approaches. Here, we provide the first molecular assessment of Ingerana charlesdarwini based on mitochondrial and nuclear DNA and reveal that it is nested in the dicroglossid genus Minervarya. A member of the Minervarya andamanensis species group, Minervarya charlesdarwini comb. nov. is sister taxon to M. andamanensis and shows relatively shallow genetic distances (2.8–3.6%) in the 16S gene. Both species are widely distributed, occur sympatrically, and exhibit high morphological variations, leading to long-standing confusions with other dicroglossid frogs reported from the region. Our combined morphological and molecular studies on dicroglossid frogs sampled across the known ranges of these species suggest that reports of Limnonectes doriae (Boulenger, 1887) and L. hascheanus (Stoliczka, 1870) from the Andamans are misidentifications of the former two, pointing to the absence of genus Limnonectes from the Andaman Islands. Our study also reveals the novel record of Minervarya agricola from the Andamans, a species that appears to have been confused with Fejervarya limnocharis and Minervarya keralensis in the literature and misidentified museum specimens, and is found to be widely distributed across these islands. We further find another congener from the Nicobar group of Islands, M. nicobariensis, to be closely related to M. charlesdarwini. Similar to the case of Andaman dicroglossids, our work emphasises on the need for further studies to ascertain the taxonomic identities and generic placement of Minervarya and Limnonectes species reported from the Nicobars.

Key words

Amphibia, Ingerana, integrative taxonomy, island biogeography, Limnonectes, sympatric species

Introduction

The Andaman and Nicobar Archipelago are home to about 21 species of amphibians, although knowledge on the fauna of these islands remains incomplete (Harikrishnan and Vasudevan 2018; Garg et al. 2022). In particular, the species-level delimitation and identities, or their higher-level taxonomic placements remain doubtful and often uninvestigated for several known taxa (e.g., Das 1998; Harikrishnan and Vasudevan 2018; Chandramouli et al. 2020a, 2020b; Chandramouli and Prasad 2020; Biju et al. 2020; Garg et al. 2022). Frogs of the family Dicroglossidae represent a large proportion of this region’s known diversity, with nine species representing five genera, namely Fejervarya, Hoplobatrachus, Ingerana, Limnonectes, and Minervarya (Stoliczka 1870; Sclater 1892; Sarkar 1990; Pillai 1991; Das 1996, 1998, 1999; Dutta 1997; Harikrishnan and Vasudevan 2018; Rangasamy et al. 2018; Chandramouli et al. 2020b; Chandramouli and Prasad 2020). Dicroglossid members occur commonly and inhabit a wide range of habitats, from saline water bodies near the seashores to forested mountain tops up to the highest elevations of over 700 m asl within the archipelago. Yet, the taxonomy of several members of this group remains uncertain (Harikrishnan and Vasudevan 2018). Although dicroglossid frogs, in general, are considered taxonomically challenging for lack of sufficient morphological traits to distinguish closely related species and genera (Dubois et al. 2001; Kuramoto et al. 2008 “2007”; Kotaki et al. 2010; Howlader 2011; Dinesh et al. 2015; Garg and Biju 2017; Sanchez et al. 2018; Köhler et al. 2019), the absence of detailed taxonomic studies has additionally contributed towards the existing long-standing uncertainties on this group of frogs in the Andaman and Nicobar Archipelago.

A classic case is that of Charles Darwin’s frog, originally described in the family Ranidae as Rana charlesdarwini. Ever since its description, this species has had an uncertain genus as well as family level placement (Das 1998; Dubois et al. 2005; Das and Dutta 2007; Chandramouli 2017). While describing this endemic species of the Andaman Islands, Das (1998) discussed the tentative nature of his generic assignment due to the confusing morphological affinities of the species and the lack of clear diagnoses or definitions for several of the potentially related South-east Asian ranid genera at the time. Nonetheless, this new species was suggested as being more closely allied to the subgenera Ingerana Dubois, 1987 or Liurana Dubois, 1987 (Das 1998). Dubois et al. (2005) removed this taxon from the subfamily “Raninae” due to the presence of a forked omosternum and regarded it as a member of “Limnonectini” without generic allocation. Das and Dutta (2007) later treated it as a member of the dicroglossid genus Limnonectes Fitzinger, 1843, based on the previous allocation of this taxon to Limnonectini. Subsequently, due to reclassification of Rana Linnaeus, 1758 sensu lato, Frost (2006) considered this species to be a member of the genus Ingerana (Frost 2021), which was at that time in family Ceratobatrachidae, on the basis of affinities discussed in the original description. Ever since, the taxon has been treated as Ingerana charlesdarwini in the literature and regional checklists (e.g., Dinesh 2009; Chandramouli 2017; Harikrishnan and Vasudevan 2018; Rangasamy et al. 2018). The genus Ingerana was also since then shown to be more closely related to dicroglossids than ceratobatrachids, leading to its transfer to the subfamily Occidozyginae within the family Dicroglossidae (Roelants et al. 2004; Bossuyt et al. 2006; Frost et al. 2006; Pyron and Wiens 2011; Brown et al. 2015). However, more recently, Yuan et al. (2016) speculated that Ingerana charlesdarwini might represent a distinct lineage in the family Ceratobatrachidae possibly having a sister-group relationship with members of the genus Liurana. Chandramouli (2017), meanwhile, reported high colour variations among individuals of this species. Even though the recent studies have remarked that the generic placement of Ingerana charlesdarwini should be considered provisional (Chandramouli 2017; Harikrishnan and Vasudevan 2018), any new supporting or conclusive evidence based on genetic data or detailed morphological studies remains unavailable. Hence, the current knowledge showcases the highly confusing taxonomy of I. charlesdarwini and its unresolved systematic relationships with other related taxa. Taking into account the long-standing confusions, intertwined taxonomic histories, and complex genus-level definitions, a resolution to the puzzling case of I. charlesdarwini appears to have been long deterred in anticipation of a need to study multiple dicroglossid taxa from the Andaman Islands, as well as other biogeographically allied South and South-east Asian regions.

The genus Ingerana, with currently four recognised species, is reported primarily from mainland regions of South and South-east Asia spanning across north-east India, southern China, Bhutan, Bangladesh, Myanmar, Thailand and the adjoining Peninsular Malaysia (Frost 2021), except for I. charlesdarwini that is the only known insular member. However, the presence of genus Ingerana in the Andamans cannot be easily ruled out. The trouble being the intriguing geographical position of the Andaman and Nicobar Islands, which are located near the contact zone of two biogeographically distinct regions in the Bay of Bengal. The Andamanese biota is known to have closer affinities with the Indo-Burmese components, whereas the Nicobarese biota is related to those of Sundaland (Mani 1974; Das 1999). Another two poorly known dicroglossid genera reported from the Andaman and Nicobar, Limnonectes and Minervarya, have confounding morphological and biogeographical affinities. Within the Andamans, Ingerana charlesdarwini shares diagnostic characters with three species—Limnonectes doriae, L. hascheanus, and Minervarya andamanensis. These four species can be confused due to their overlapping size range, comparable body plan, and highly variable dorsal skin texture and colouration. At the same time, however, the absence of prominent chevron mark and longitudinal skin folds (commonly shagreened to sparsely granular) on the dorsum, and stout appearance makes the systematic position of Ingerana charlesdarwini enigmatic. It is noteworthy that the identities of these closely related species have also been questioned in the past (Inger and Stuart 2010; Harikrishnan and Vasudevan 2018). The reports of Limnonectes doriae and L. hascheanus are solely based on a few specimens originally contained in the type series of Minervarya andamanensis (Stoliczka 1870) that were identified as belonging to the two Limnonectes species (Sclater 1892; Annandale 1917; Dutta 1997). Despite subsequently being included in the regional fauna for over two decades (Das 1999; Harikrishnan et al. 2010, 2012; Chandramouli et al. 2015; Rangasamy et al. 2018), these species have surprisingly not been sampled from the Andamans ever since. On the other hand, the identity of another widely reported species, Minervarya andamanensis, also remains confusing, after seemingly being restricted to a sub-adult lectotype specimen (Annandale 1917). This apart, even though widely reported, M. andamanensis is largely known from confusing literature records and museum specimens (Harikrishnan and Vasudevan 2018) and apparently unconfirmed DNA sequences based on which its systematic relationships have been discussed (Kotaki et al. 2010; Sanchez et al. 2018; Garg and Biju 2021). Recently, Chandramouli (2017) identified some museum specimens, likely referred to either Limnonectes doriae or Minervarya andamanensis, as belonging to Ingerana charlesdarwini, further suggesting that these species have long been confused and misidentified, both historically and contemporarily.

The genus Minervarya is recognised as a predominantly South Asian radiation, whereas Limnonectes members are largely restricted to South-east and East Asia (Sanchez et al. 2018). The taxonomy of both these genera has undergone considerable changes in the recent years with active research and growing evidence on systematic relationships using integrative approaches. This has led to taxonomic stability of several species that had variously been placed in dicroglossid genera such as Rana, Fejervarya, Limnonectes, Minervarya, and Sphaerotheca due to lack of sufficient morphological traits to distinguish closely related taxa (Dubois 1987; Iskandar 1998; Inger and Stuart 2010; Howlader 2011; Dinesh et al. 2015; Sanchez et al. 2018; Köhler et al. 2019; Garg and Biju 2021; Khatiwada et al. 2021). However, members of these genera from the Andaman and Nicobar Islands have rarely been subjected to detailed taxonomic studies or included in comprehensive works due to the absence of data from this region. This has propagated uncertainties concerning not just the diagnoses and systematic relationships at various taxonomic levels, but also the diversity and distribution patterns of related dicroglossid genera.

Hence, in an attempt to resolve the curious case of Ingerana charlesdarwini, we studied multiple closely related and possibly confused Andaman species (Ingerana charlesdarwini, Limnonectes doriae, L. hascheanus, and Minervarya andamanensis) to address some persisting questions due to their complex taxonomic identities and unresolved systematic relationships. We extensively sampled these taxa, based on their apparent identities as understood in the literature, and provide the first integrative molecular and morphological assessment for these species from the Andaman Islands. Our study further investigates the identity of Fejervaryalimnocharis’ reported from Andamans and also looks into the systematic relationships of another closely related minervaryan frog, Minervarya nicobariensis, from the Nicobar group of islands.

Materials and Methods

Field sampling

Sampling of various species of dicroglossid frogs was carried out across the Andaman and Nicobar Archipelago (Tables 1 and 2). Opportunistic searches were carried out in a wide range of habitats such as primary and secondary forests, agricultural fields, parks, beaches and wayside areas with permanent or temporary water bodies, from sea level up to elevations of nearly 700 m asl. During the breeding season, individuals were often located by calls. Live specimens were photographed in the wild or captive conditions and euthanised in Tricaine methanesulfonate (MS-222) solution. Tissue samples were obtained from thigh (adult) or tail muscle (tadpoles) and preserved in absolute ethanol. Specimens were fixed in 4% formalin and rinsed in water before preservation in 70% ethanol. The sampled specimens are available in the amphibian collection of Zoological Survey of India, Andaman and Nicobar Regional Centre, Port Blair (ZSI/ANRC) or the Systematics Lab at University of Delhi (SDBDU). Geographical coordinates and elevation at the sampling localities were recorded using the WGS84 datum system. Maps were prepared using QGIS (http://www.qgis.org).

Molecular study

Genomic DNA was extracted from 15 samples using the Qiagen DNeasy blood and tissue kit (Qiagen, Valencia, CA, USA). From all the extracted samples, a ~540 bp fragment of the mitochondrial 16S rRNA gene was PCR-amplified using primers from Simon et al. (1994). Three additional gene fragments were sequenced for selected samples, using previously published primers: 385 bp of the mitochondrial 12S rRNA (Richards and Moore 1996), 564 bp of the nuclear recombination activating gene 1 (Biju and Bossuyt 2003), and 603 bp of the nuclear tyrosinase (Bossuyt and Milinkovitch 2000). Sequencing was performed on both strands using a BigDye Terminator v3.1 Cycle Sequencing kit on an ABI 3730 automated DNA sequencer (Applied Biosystems). Raw sequences were assembled and checked in ChromasPro v1.4 (Technelysium Pty Ltd.). Sequences from this study are deposited in the National Center for Biotechnology Information (NCBI) GenBank under accession numbers ON009953ON009969 and ON010541-ON010544. Additional homologous sequences were retrieved from the GenBank for all known members of the Minervarya andamanensis species group and representatives of other Minervarya species. Ten species from other closely related dicroglossid genera were used as the outgroup taxa for phylogenetic analyses. Datasets for each gene were assembled and aligned using MUSCLE (Edgar 2004) in MEGA 7.0 (Kumar et al. 2016). The alignments for coding DNA were checked by comparison with amino acid sequences, whereas those for the non-coding fragments were manually optimised.

Bayesian inference (BI) and Maximum Likelihood (ML) analyses were performed with a concatenated character matrix of 2,101 nucleotides for 69 taxa (Table 1). The data was partitioned by genes for 16S and 12S, and by codons for Rag1 and Tyr, with a total of eight partitions. The following best-fitting models of sequence evolution for each partition were selected through a greedy search in PartitionFinder 2 (Lanfear et al. 2017) using the corrected Akaike information criterion (AICc): GTR+I+G for 16S and 12S, TVM+I+G for the first codon positions of Rag1 and Tyr, K81UF+I for the second codon positions of Rag1 and Tyr, TRN+G for Rag1 third codon position, and TVM+G for Tyr third codon position. Using this partitioning scheme, the Bayesian phylogenetic inference was performed in MrBayes (Ronquist and Huelsenbeck 2003) with four independent Bayesian runs, each running with four Metropolis-Coupled Markov chain Monte Carlo (MCMCMC) chains for 20,000,000 generations using default priors, chain temperature of 0.1, and tree sampling at every 4,000 generations. The convergence of the runs was determined by the nearing of standard deviation of split frequencies < 0.01 and potential scale reduction factors ~1.0. Stationarity of the likelihood scores and effective sample sizes (ESS) for all parameters were viewed in Tracer v. 1.7 (Rambaut et al. 2018). The Bayesian posterior probabilities (BPP) were summarised after discarding the first 25% trees as burn-in (Huelsenbeck et al. 2001). A partitioned maximum likelihood analysis was also performed for 10,000 ultrafast bootstrap (UBS) replicates, executed with the ‘auto’ model selection option, using IQ-TREE (Minh et al. 2013) on the IQ-TREE webserver (Trifinopoulos et al. 2016). Nodes with BPP≥95% and UBS≥90% were considered well supported.

Table 1.

List of DNA sequences included in the phylogenetic study.

S.N Taxa Collection Locality Voucher No. Accession Number Reference
Minervarya andamanensis group 16S 12S TYR RAG1
1 M. andamanensis India: Andaman Island n.a. AB488899 AB488876 AB489015 AB488951 Kotaki et al. 2010
2 M. andamanensis India: South Andaman: Mt. Harriet National Park SDBDU 2019.3951 ON009955 n.a. n.a. n.a. Present study
3 M. andamanensis India: South Andaman: Mt. Harriet National Park SDBDU 2019.3956 ON009956 n.a. n.a. n.a. Present study
4 M. andamanensis India: South Andaman: Chidiya Taapu SDBDU 2019.3964 ON009957 n.a. n.a. n.a. Present study
5 M. andamanensis India: South Andaman: Chidiya Taapu SDBDU 2019.3978 ON009958 n.a. n.a. n.a. Present study
6 M. andamanensis India: South Andaman: Munda Pahad SDBDU 2019.3992 ON009959 n.a. n.a. n.a. Present study
7 M. andamanensis India: South Andaman: Chidiya Taapu SDBDU 2019.3996 ON009960 n.a. n.a. n.a. Present study
8 M. andamanensis India: Little Andaman SDBDU 2019.4011 ON009961 n.a. n.a. n.a. Present study
9 M. andamanensis India: South Andaman: Sippi Ghat SDBDU 2019.4028 ON009962 n.a. n.a. n.a. Present study
10 M. charlesdarwini India: South Andaman: Mt. Harriet National Park SDBDU 2019.3945 ON009963 ON009953 ON010541 ON010543 Present study
11 M. charlesdarwini India: South Andaman: Mt. Harriet National Park SDBDU 2019.3947 ON009964 ON009954 ON010542 ON010544 Present study
12 M. charlesdarwini India: South Andaman: Mt. Harriet National Park SDBDU 2019.3952 ON009965 n.a. n.a. n.a. Present study
13 M. charlesdarwini India: South Andaman: Mt. Harriet National Park SDBDU 2019.3954 ON009966 n.a. n.a. n.a. Present study
14 M. muangkanensis Thailand: Pilok IABHU 18145/18156/18157 AB277300 n.a. AB277352 AB488956 Kotaki et al. 2008, 2010
15 M. muangkanensis Thailand: Kanchanaburi, Thong Pha Phum KIZ 024627 MF166918 n.a. n.a. n.a. Suwannapoom et al. 2017
16 M. muangkanensis Myanmar: Bago, Dawei USNM:Herp:587076 MG935778 n.a. n.a. n.a. Mulcahy et al. 2018
17 M. muangkanensis Myanmar: Bago, Dawei USNM:Herp:587073 MG935779 n.a. n.a. n.a. Mulcahy et al. 2018
18 M. muangkanensis Myanmar: Tanintharyi, Yeybu village USNM:Herp:586873 MG935780 n.a. n.a. n.a. Mulcahy et al. 2018
19 M. muangkanensis Myanmar: Tanintharyi, Yeybu village USNM:Herp:586874 MG935781 n.a. n.a. n.a. Mulcahy et al. 2018
20 M. muangkanensis Myanmar: Tanintharyi, Yeybu village USNM:Herp:586875 MG935782 n.a. n.a. n.a. Mulcahy et al. 2018
21 M. muangkanensis Myanmar: Tanintharyi, Yeybu village USNM:Herp:586876 MG935783 n.a. n.a. n.a. Mulcahy et al. 2018
22 M. muangkanensis Myanmar: Tanintharyi, Yeybu village USNM:Herp:586878 MG935784 n.a. n.a. n.a. Mulcahy et al. 2018
23 M. muangkanensis Myanmar: Tanintharyi, Yeybu village USNM:Herp:586879 MG935785 n.a. n.a. n.a. Mulcahy et al. 2018
24 M. muangkanensis Myanmar: Ayeyarwady, near Mwe Hauk village CAS 208016 MK621439 n.a. n.a. n.a. Köhler et al. 2019
25 M. muangkanensis Myanmar: Ayeyarwady, near Mwe Hauk village CAS 208033 MK621440 n.a. n.a. n.a. Köhler et al. 2019
26 M. muangkanensis Myanmar: Ayeyarwady, near Kyanigan SMF 103782 MK621441 n.a. n.a. n.a. Köhler et al. 2019
27 M. muangkanensis Myanmar: Ayeyarwady, Kan Ywa to Negwesaung SMF 103787 MK621442 n.a. n.a. n.a. Köhler et al. 2019
28 M. muangkanensis Myanmar: Ayeyarwady, Kan Ywa to Negwesaung SMF 103788 MK621443 n.a. n.a. n.a. Köhler et al. 2019
29 M. muangkanensis Myanmar: Ayeyarwady, Kan Ywa to Negwesaung SMF 103790 MK621444 n.a. n.a. n.a. Köhler et al. 2019
30 M. muangkanensis Myanmar: Rakhaing, Ngapali, Dam Lake SMF 104873 MK621445 n.a. n.a. n.a. Köhler et al. 2019
31 M. muangkanensis Myanmar: Ayeyarwady, Kan Ywa to Negwesaung SMF 105012 MK621446 n.a. n.a. n.a. Köhler et al. 2019
32 M. muangkanensis Myanmar: Ayeyarwady, Kan Ywa to Negwesaung SMF 105013 MK621447 n.a. n.a. n.a. Köhler et al. 2019
Minervarya agricola group
33 M. agricola India: Karnataka: Mudigere BNHS 4651 AB488895 AB488872 AB489011 AB488947 Kotaki et al. 2010
34 M. agricola India: South Andaman: Chidiya Taapu SDBDU 2019.3986 ON009967 n.a. n.a. n.a. Present study
35 M. agricola India: South Andaman: Sippi Ghat SDBDU 2019.4027 ON009968 n.a. n.a. n.a. Present study
36 M. agricola India: Middle Andaman: Rangat SDBDU 2019.4054 ON009969 n.a. n.a. n.a. Present study
37 M. asmati India: Assam n.a. AB488900 AB488877 AB489016 AB488952 Kotaki et al. 2010
38 M. chiangmaiensis Thailand: Chiang Mai: Omkoi KIZ024057 KX834135 n.a. n.a. n.a. Suwannapoom et al. 2016
39 M. teraiensis Nepal: Britamod: Jhapa CDZMTU356 MT983106 n.a. n.a. n.a. Khatiwada et al. 2021
Minervarya greenii group
40 M. greenii Sri Lanka: Hakgala MNHN 2000.617 AB488891 AB488868 AB489008 AB488944 Kotaki et al. 2010
41 M. kirtisinghei Sri Lanka: Hakgala MNHN 2000.620 AB488890 AB488867 AB489007 AB488943 Kotaki et al. 2010
Minervarya mysorensis group
42 M. brevipalmata India: Kerala: Kadalar SDBDU 2011.1048 MZ156230 n.a. n.a. n.a. Garg and Biju 2021
43 M. goemchi India: Goa: Surla ZSI/WRC/A/2017 MG800343 n.a. n.a. n.a. Dinesh et al. 2018
44 M. mysorensis India: Karnataka: Kudremukh BNHS 4653 / 4654 AB488898 AB488875 AB489014 AB488950 Kotaki et al. 2010
Minervarya nilagirica group
45 M. keralensis India WII: 3263 JX573181 JX573190 n.a. n.a. Raj et al. 2018
46 M. nilagirica India: Madikeri BNHS 4646 AB488896 AB488873 AB489012 AB488948 Kotaki et al. 2010
47 M. kalinga India: Odisha: Barbara Reserve Forest SDBDU 2015.3108 MZ156316 n.a. n.a. n.a. Garg and Biju 2021
Minervarya rufescens group
48 M. cepfi India: Maharashtra: Amboli ZSI/WGRC/V/A/938 KY447308 n.a. n.a. KY820753 Garg and Biju 2017
49 M. kadar India: Kerala: Thavalakuzhipara ZSI/WGRC/V/A/940 KY447312 n.a. n.a. KY820754 Garg and Biju 2017
50 M. manoharani India: Kerala: Chathankod-Bonnacad ZSI/WGRC/V/A/945 KY447313 n.a. n.a. KY820757 Garg and Biju 2017
51 M. neilcoxi India: Kerala: Parambikulam ZSI/WGRC/V/A/951 KY447318 n.a. n.a. KY820759 Garg and Biju 2017
52 M. rufescens India: Padil: Mangalore RBRL 040716-1 or 39-16-Jul-2004 AB530602 AB488874 AB489013 AB488949 Hasan et al. 2014;
Kotaki et al. 2010
53 M. marathi India: Maharashtra: Pune, Bhamburde n.a. MH370483 n.a. MH370484 n.a. Phuge et al. 2019
Minervarya sahyadris group
54 M. sahyadris India: Karnataka: Mangalore SDBDU 2015.3046 MZ156082 n.a. n.a. n.a. Garg and Biju 2021
55 M. gomantaki India: Codal village ZSI/WGRC/V/A/867 KR781085 n.a. KT004440 n.a. Dinesh et al. 2015
56 M. krishnan India: Karnataka: Jog Falls SDBDU 2003.40156 MZ156093 n.a. n.a. n.a. Garg and Biju 2021
Minervarya syhadrensis group
57 M. pentali India: Kerala: Nedumbaserry BNHS 6116 MZ156229 n.a. n.a. n.a. Garg and Biju 2021
58 M. nepalensis Nepal: Chitwan n.a. AB488889 AB488866 AB500268 AB500225 Kotaki et al. 2010
59 M. syhadrensis India: Karnataka: Mudigere BNHS 5060 AB488894 AB488871 AB489010 AB488946 Kotaki et al. 2010
Outgroups
60 F. limnocharis Indonesia: Bogor IABHU 18002 AB277302 AB277286 AB277354 AB488953 Kotaki et al. 2008, 2010
61 F. orissaensis India: Odisha KU 197186 AB277304 AB277288 AB277356 AB500222 Kotaki et al. 2008, 2010
62 S. dobsonii India: Bajipe n.a. AB277305 AB277290 AB277357 AB488959 Kotaki et al. 2008, 2010
63 S. pluvialis Sri Lanka VUB0182 AF249042 AF249014 AF249173 DQ347214 Bossuyt and Milinkovitch 2000
64 E. cyanophlyctis India VUB0039 AF249053 AF249015 AF249174 DQ347205 Bossuyt and Milinkovitch 2000
65 E. hexadactylus India: Mudigere n.a. AB272608 AB273176 n.a. n.a. Alam et al. 2008
66 H. crassus Sri Lanka VUB0107 AF249044 AF249013 AF249172 DQ347211 Bossuyt and Milinkovitch 2000
67 H. tigerinus India: Mangalore n.a. AB488902 n.a. AB277358 AB488958 Kotaki et al. 2008, 2010
68 N. ceylonensis Sri Lanka VUB0172 AF249047 AF249016 AF249175 AY948917 Bossuyt and Milinkovitch 2000
69 L. laticeps Malaysia: Kuala Lumpur n.a. AB277306 n.a. AB277359 AB488960 Kotaki et al. 2008, 2010

A species delimitation analysis was performed using the multi-gene ML phylogram as input by Bayesian implementation of the Poisson Tree Processor (PTP) method (Zhang et al. 2013) on the bPTP webserver (https://species.h-its.org). To further assess the population structure in the Minervarya andamanensis species group, a haplotype network was constructed using the available 16S rRNA sequences. A dataset of 32 sequences comprising 513 characters, excluding sites with missing data but including the alignment gaps, was used to reconstruct haplotypes using the PHASE algorithm (Stephens et al. 2001) in DnaSP version 5 (Librado and Rozas 2009). A median-joining network was then constructed with 64 recovered haplotype sequences using the software Network 4.6.1.0 (www.fluxus-engineering.com). Intra- and interspecific uncorrected pairwise genetic distances for 16S sequences of the M. andamanensis species group were computed in PAUP* 4.0b10 (Swofford 2002).

Morphological study

We morphologically examined our new collections and compared them with the available type specimens, original descriptions, other topotypic specimens or general collections of all the dicroglossid frogs known to occur in the Andaman and Nicobar Archipelago. Sex and maturity were determined by the presence of secondary sexual characters (such as nuptial pads and vocal sacs in males) or examination of gonads through a small lateral or ventral incision. Only adult (sexually mature) individuals were used for morphometric studies. The following measurements were taken to the nearest 0.1 mm using digital slide-calipers with the aid of a stereomicroscope, following measurements and associated terminologies of Garg and Biju (2017, 2021): snout-vent length (SVL), head width (HW, at the angle of the jaws), head length (HL, from rear of mandible to tip of snout), MN (distance from the rear of the mandible to the nostril), MFE (distance from the rear of the mandible to the anterior orbital border), MBE (distance from the rear of the mandible to the posterior orbital border), snout length (SL, from tip of snout to anterior orbital border), eye length (EL, horizontal distance between bony orbital borders), inter upper eyelid width (IUE, the shortest distance between the upper eyelids), maximum upper eyelid width (UEW), internarial distance (IN), internal front of the eyes (IFE, shortest distance between the anterior orbital borders), internal back of the eyes (IBE, shortest distance between the posterior orbital borders), NS (distance from the nostril to the tip of the snout), EN (distance from the front of the eye to the nostril), TYD (greatest tympanum diameter), TYE (distance from the tympanum to the back of the eye), forearm length (FAL, from flexed elbow to base of outer palmar tubercle), hand length (HAL, from base of outer palmar tubercle to tip of third finger), FLI–IV (finger length), thigh length (TL, from vent to knee), shank length (SHL, from knee to heel), foot length (FOL, from base of inner metatarsal tubercle to tip of fourth toe), total foot length (TFOL, from heel to tip of fourth toe), FD (maximum disc width of finger), width of finger (FW, measured at the base of the disc), TD (maximum disc width of toe), width of toe (TW, measured at the base of the disc). Digit number is represented by Roman numerals I–V in subscript. Measurements and photographs are mostly for the right side of the specimen, unless a character was damaged, in which case the left side was taken. All measurements provided in the taxonomy section are in millimetres. The body size categories discussed in the text for the purpose of convenience and morphological comparisons follow Garg and Biju (2021). The webbing formulae follow Savage and Heyer (1967), as modified by Myers and Duellman (1982). The amount of webbing relative to subarticular tubercles is described by numbering the tubercles 1–3, starting from the base of the digits.

Abbreviations. Museum acronyms and other frequently used abbreviations are as follows: ZSI (Zoological Survey of India); ZSIC (Zoological Survey of India, Kolkata); ZSI/ANRC (Zoological Survey of India, Andaman and Nicobar Regional Centre, Port Blair); ZSI/SRS (Zoological Survey of India, South Regional Station, Chennai); NHM (Natural History Museum, London), formerly BMNH (British Museum [Natural History], London); Systematics Lab, University of Delhi (SDBDU).

ZooBank registration. This published work and the nomenclatural acts it contains have been registered in ZooBank, the online registration system for the International Commission on Zoological Nomenclature (ICZN). The ZooBank LSID (Life Science Identifier) for this publication is urn:lsid:zoobank.org:pub:2780E8F9-1ABF-4708-898A-B14447591063. The LSID and associated information can be resolved through any standard web browser by appending the LSID to the prefix http://zoobank.org.

Results

Phylogenetic relationships and genetic structure

Our phylogenetic study found Ingeranacharlesdarwini to be deeply nested within the genus Minervarya (Fig. 1), based on 16S rRNA sequences from four exemplars, as well as additional mitochondrial (12S rRNA) and nuclear markers (Rag1 and Tyr) from two selected samples. Both the BI and ML analyses of a concatenated dataset of 2,101 characters recovered the species as a distinct well-supported (BPP 100, UFB 99) lineage in the M. andamanensis species group (Garg and Biju 2021). It also formed a highly supported (BPP 100, UFB 98) sister-group relationship with M. andamanensis, showing relatively shallow divergence of 2.8–3.6% for the 16S rRNA sequences. In comparison, the two previously recognised members of the group, M. andamanensis and M. muangkanensis, showed a higher divergence of 3.8–4.6%. Further, Ingeranacharlesdarwini was divergent from M. muangkanensis by 4.4–4.7% for the 16S locus. These interspecific divergences fall well within the range of genetic distances usually observed at the species-level in the genus Minervarya and closely related dicroglossid genera (e.g., Kotaki et al. 2010; Köhler et al. 2019; Garg and Biju 2021). Our results, thus, clearly indicate that Ingeranacharlesdarwini is a member of the genus Minervarya and should therefore be treated as Minervarya charlesdarwini comb. nov. Within the M. andamanensis species group, both the insular Andaman species, M. charlesdarwini and M. andamanensis, are more closely related to each other than to M. muangkanensis of mainland Thailand and Myanmar region, which formed the basal lineage (Fig. 1).

Figure 1. 

Phylogenetic position and genetic structure of species in the Minervarya andamanensis species group. A. Maximum likelihood phylogram based on a multi-gene dataset (2,101 bp of mitochondrial and nuclear DNA), depicting the phylogenetic position of Minervarya charlesdarwini comb. nov. in the genus Minervarya and relationships among three members of the M. andamanensis species group. Voucher numbers at terminal nodes are referenced in Table 1. Values above and below the branches represent Ultrafast Bootstrap Support (UFB, >50%) and Bayesian Posterior Probabilities (BPP, >0.50), respectively. Vertical bars indicate the recovery of three M. andamanensis group members as distinct species in multi-gene bPTP species delimitation analysis. B. Median-Joining network based on 513 bp of the mitochondrial 16S gene depicting the genetic structure among three species. Circle colours indicate different species; circle size is proportional to the frequency of haplotypes; black circles indicate median vectors; values on circles indicate frequency of haplotypes; values on connecting branches indicate number of mutation steps.

Within the focal Minervarya andamanensis species group, the multi-loci species delimitation analysis recovered all the three recognised species as distinct (Fig. 1). At the same time, the mitochondrial 16S median-joining network did not find sharing of haplotypes among the three species. A total of 12 haplotypes were recovered with an overall haplotype diversity of 0.8834 within the species group. In line with the results obtained in the phylogenetic analyses, the mainland member of the group, M. muangkanensis, was the most distinct species showing separation from M. andamanensis by minimum 24 mutation steps and from M. charlesdarwini by 26 steps. Eight haplotypes were detected among individuals of M. muangkanensis. Although the populations from Thailand and Myanmar did not share any haplotypes, the absence of clear genetic structuring indicates ongoing gene flow and admixture between these geographically continuous regions. The populations of M. andamanensis from South Andamans and Little Andamans formed two distinct haplotype clusters without sharing of haplotypes, separated by minimum six mutation steps and considerable genetic differentiation (1.1–1.3%), suggestive of limited gene flow, longer geographical isolation, and hence a potential area of population differentiation between these islands. On the other hand, the two widely co-occurring sister species within the Andaman Islands that do not exhibit similar habitat associations—M. charlesdarwini (largely forest dwelling, phytotelm breeding, and possibly a habitat specialist) and M. andamanensis (occupies a broader range of habitats, breeds in open water bodies, and is possibly a habitat generalist)—formed clearly distinct clusters separated from each other by minimum 18 mutation steps, suggesting that sympatric speciation potentially occurred within this radiation (Fig. 1). These species appear to present an insightful case for future investigations on the patterns of gene flow, speciation and diversification processes, ecological niche segregation, and phylogeography within the islands of Andaman and Nicobar.

Taxonomy

Minervarya andamanensis species group

Members included

Minervarya charlesdarwini, M. andamanensis, M. muangkanensis, and M. nicobariensis.

Morphological definition

This group can be distinguished from other minervaryan groups by the following suite of characters (revised after Garg and Biju 2021): small to large-sized adults (male SVL 24–50 mm, female SVL 30–72 mm); elongate to robust body; dorsal skin shagreened to sparsely granular, or with prominent glandular warts; dorsum with or without weakly developed short discontinuous skin folds or chevron mark at the centre of dorsum; upper ⅔rd of tympanum and inner margin of tympanic fold dark brown; groin without prominent reticulations; thighs with or without reticulations; foot webbing moderate, below the third subarticular tubercle on either side of toe IV; long and cylindrical inner metatarsal tubercles.

Furthermore, Minervarya charlesdarwini, M. andamanensis and M. nicobariensis are placed in the genus due to the following suite of characters: omosternum unforked; vomerine ridge with weakly developed teeth; absence of lingual papilla; presence of fejervaryan lines; finger and toe tips rounded with slightly swollen discs, without circum-marginal grooves; and foot webbing not extending up to the toe tips.

Distribution

Andaman and Nicobar Archipelago of India (Fig. 2), Myanmar (Köhler et al. 2019), and Thailand (Suwannapoom et al. 2017).

Figure 2. 

Distribution of Minervarya species in the Andaman and Nicobar Archipelago. A Location of the Archipelago in the Bay of Bengal. B Expanded view of the Andaman and Nicobar groups of islands. C Minervarya nicobariensis in the Nicobar Islands. D Minervarya charlesdarwini in the Andaman Islands. E Minervarya andamanensis in the Andaman Islands. F Minervarya agricola in the Andaman Islands.

Note

Garg and Biju (2021) provisionally placed Minervarya marathi in this group. Based on the results of our present study, M. marathi is phylogenetically more closely related to members of the M. rufescens group, rather than M. andamanensis group. Hence, we exclude M. marathi from the M. andamanensis group, and recommend further detailed studies to ascertain the systematic affinities of the taxon.

Minervarya charlesdarwini (Das, 1998), comb. nov.

Charles Darwin’s minervaryan frog Figs 1, 2, 3, 4; Tables 1, 2

Note

Das (1998) described Rana charlesdarwini based on three adult and five larval specimens from Mount Harriet National Park in the South Andaman Island. Until recently, new vouchered reports of this species were lacking and the species was known only from its type series. Chandramouli (2017) reported rediscovery of this species along with a redescription based on new collections and some old museum specimens reidentified as Ingerana charlesdarwini, while also discussing morphological variations among the studied individuals. However, owing to the confounding taxonomic history and generic placement of this taxon (see Introduction), clarity on the systematics relationships of Rana charlesdarwini remained lacking. Our first ever molecular assessment of this taxon combined with morphological studies based on topotypic collections has confirmed its placement in the dicroglossid genus Minervarya. We further confirmed the prevalence of high morphological variation among individuals of this species, particularly with regard to dorsal colouration, markings, and body size (Figs 3, 4). However, due to the uncertainty of its systematic position, a morphological comparison with relevant taxa has been lacking. Below, we provide a revised morphological diagnosis for the species as well as comparisons with the closely related members of the M. andamanensis species group. We also elaborate on and provide detailed illustrations of the morphological variations observed in our study, considering that this species is likely to have been confused with other dicroglossids found in the regions for several years, before and after its formal description (see taxonomic remarks for M. andamanensis, Limnonectes doriae and L. hascheanus).

Figure 3. 

Morphological variation in skin colouration and markings observed among individuals of Minervarya charlesdarwini in the Andaman Islands. A–N Dorsolateral views. A SDBDU 2021.4212 (♂). B–C SDBDU 2019.4059 (♀). D Not preserved. E SDBDU 2019.4006 (♂). F SDBDU 2019.3975 (♂). G SDBDU 2021.4212 (♂). H SDBDU 2019.4005 (♀). I SDBDU 2019.3968 (♀). J SDBDU 2019.4004 (♂). K SDBDU 2021.4213 (♀). L SDBDU 2020.4165 (♀). M SDBDU 2019.3946 (♀). N SDBDU 2021.4214 (♀). Photographs: S. D. Biju, G. Gokulakrishnan & Sonali Garg.

Figure 4. 

Morphological variation in skin texture, colouration, and markings observed among individuals of Minervarya charlesdarwini in the Andaman Islands. A–H Dorsal views. A–D Variation in skin texture and enlarged view of dorsal skin (demarcated with white square) above. A SDBDU 2019.4059 (♀). B SDBDU 2020.4162 (♂). C SDBDU 2021.4212 (♂). D SDBDU 2019.3977 (♂). E–G Not preserved (♂). H SDBDU 2019.4004 (♂). I SDBDU 2019.4005 (♀). J Ventral view, SDBDU 2021.4212 (♂). K Lateral view, SDBDU 2021.4218 (♂). L Dorsal view of thigh, SDBDU 2021.4212 (♂). M Posterior view of thigh, SDBDU 2021.4212 (♂). N Ventral view of hand, SDBDU 2021.4212 (♂). O Ventral view of foot, SDBDU 2021.4212 (♂). P Schematic illustration of foot webbing, SDBDU 2021.4212 (♂). Photographs: S. D. Biju.

Morphological diagnosis

Minervarya charlesdarwini can be morphologically diagnosed by the following suite of characters: small to medium-sized adults (male SVL 24.8–30.1 mm, female SVL 30.8–36.6 mm); rather elongate body; dorsal skin shagreened to granular, or with prominently glandular warts; presence or absence of a weakly to well developed interrupted inverse V-shaped ridge (chevron mark) at the centre of dorsum; upper ⅔rd of tympanum and inner margin of tympanic fold dark brown; groin and thighs without prominent reticulations; finger and toe tips rounded with slightly swollen discs, without circum-marginal grooves; foot webbing relatively reduced, up to or just above the second subarticular tubercle but not beyond on either side of toe IV; elongate inner metatarsal tubercles; small and rounded outer metatarsal tubercle; presence of fejervaryan lines on abdomen; vomerine ridge with weakly developed teeth; absence of lingual papilla; omosternum unforked.

Redescription (all measurements in mm)

A small to medium-sized species (males: SVL 24.8–30.1, 26.6±1.8, N=6; females: SVL 30.8–36.6, 33.5±1.9, N=7), body rather elongate; head longer (males: HL 10.0–12.0, 10.6±0.7; females: HL 11.1–13.8, 12.7±1.0, N=7) than wide (males: HW 9.0–10.9, 9.6±0.7; females: HW 10.4–12.4, 11.6±0.7, N=7); snout rounded in dorsal and lateral view; snout length (males: SL 4.2–4.4, 4.3±0.1, N=6; females: SL 4.7–5.7, 5.2±0.4, N=7) longer than horizontal diameter of eye (males: EL 3.1–3.9, 3.4±0.3, N=6; females: EL 3.6–4.5, 4.0±0.3, N=7); loreal region obtuse; canthus rostralis rounded; interorbital space flat; tympanum diameter (males: TYD 1.9–2.3, 2.1± 0.2, N=6; females: TYD 2.1–2.8, 2.5±0.3, N=7) nearly ⅗th of the eye diameter (males: EL 3.1–3.9, 3.4±0.3, N=6; females: EL 3.6–4.5, 4.0±0.3, N=7); pineal ocellus present; supratympanic fold well developed, extends from posterior corner of the eye up to nearly the shoulder; vomerine ridge present, bearing small teeth; tongue moderately long, emarginated; 1–4 glands present at labial commissure (Figs 3, 4).

Forearm length (males: FAL 4.8–6.0, 5.3±0.5, N=6; females: FAL 6.0–6.9, 6.6±0.3, N=7) shorter than hand length (males: HAL 6.1–7.8, 6.7±0.6, N=6; females: HAL 7.4–8.7, 8.1±0.6, N=7); subarticular tubercles prominent, single, circular, all present; prepollex oval, prominent; two rounded palmar tubercles; supernumerary tubercles absent; relative length of fingers II < I=IV < III; tip of fingers rounded, not enlarged into discs. Hind limbs short in comparison to the body length with tibiotarsal articulation reaching up to the anterior end of eye when hind limb is stretched along the body; thigh (males: TL 13.1–15.4, 13.6±0.9, N=6; females: TL 16.2–17.0, 16.6±0.4, N=7) shorter than shank (males: SHL 14.1–15.8, 14.5±0.6, N=6; females: SHL 17.5–18.9, 18.0±0.7, N=7) and nearly equal to foot (males: FOL 12.8–15.3, 13.4±1.0, N=6; females: FOL 15.9–17.7, 16.8±0.7, N=7); total foot length (males: TFOL 19.1–22.7, 19.7±1.6, N=6; females: TFOL 23.0–26.1, 24.7±1.2, N=7); toe tips rounded, slightly swollen without discs, toes without dermal fringes, foot webbing moderate: I2––2II1½–3–III2––3+IV3––2–V; subarticular tubercles prominent, all present; inner metatarsal tubercle prominent, elongate; outer metatarsal tubercle small, rounded; supernumerary tubercles absent.

Skin of dorsum highly variable from shagreened to prominently granular or with glandular warts; an interrupted inverse V-shaped ridge (chevron mark) at the centre of dorsum weakly to well developed or absent. Ventral surfaces of throat, chest, belly, and limbs smooth; and posterior parts of thigh and region surrounding the vent sparsely granular (Fig. 4). Dorsal and ventral skin colouration is extremely variable. Dorsal surface: uniform grey, brownish-grey, yellowish-brown, light to dark brown, blackish-brown, reddish-brown, and occasionally (but not rarely) with a broad median band extending from the upper eyelids or anterior border of eyes to vent, and a thin or broad middorsal line extending from the tip of the snout to vent (Figs 3, 4); presence or absence of reddish-brown or orange colouration on snout, lateral surfaces of dorsum, and fore and hind limbs (Figs 3, 4); presence or absence of dark blackish-brown lining on dorsal tubercles; faint or prominent crossbands on lips; upper ⅔rd of tympanum and inner margin of tympanic fold dark brown; anterior and posterior parts of thighs without prominent reticulations. Ventral surface: throat and chest light to dark brown or dark grey, with light or dark patches; belly yellowish-white, with or without orange tinge; margins of limbs usually with blackish-brown colouration; hand and foot light or dark brown.

Comparison (only with males, N=6)

Minervarya charlesdarwini cannot be confused with other known species of the genus Minervarya, except three members of the M. andamanensis group (M. andamanensis, M. nicobariensis, and M. muangkanensis). Minervarya charlesdarwini can be distinguished from M. andamanensis and M. nicobariensis by its relatively smaller adult size, male SVL 24.8–30.1 mm (vs. larger, SVL 36.2–42.2 mm and SVL 40.0–49.8 mm, respectively); and elongate body (vs. stout and robust in both the species). It specifically also differs from M. andamanensis by the absence of forearm tubercles (vs. present); canthus rostralis rounded (vs. indistinct); posterior half of thigh without reticulations, usually brown or orangish-brown (vs. light to dark brown with yellowish reticulations); upper eyelid width nearly equal to inter upper eyelid width, UEW 2.4±0.2 vs. IUE 2.4±0.2 (vs. wider, UEW 3.6±0.3 vs. IUE 2.8±0.1); and thigh nearly equal to foot length, TL 13.6±0.9 vs. FOL 13.4±1.0 (vs. shorter, TL 19.9±1.3 vs. FOL 21.7±1.5). Minervarya charlesdarwini also differs from M. nicobariensis by its head being longer than wide, HL 10.6±0.7 vs. HW 9.6±0.7 (vs. wider, HW 17.5±1.0 vs. HL 16.5±1.1); upper eyelid width nearly equal to inter upper eyelid width, UEW 2.4±0.2 vs. IUE 2.4±0.2 (vs. wider, UEW 4.5±0.4 vs IUE 3.2±0.4); thigh nearly equal to foot length, TL 13.6±0.9 vs. FOL 13.4±1.0 (vs. shorter, TL 20.7±1.4 vs. FOL 22.1±1.5); presence of outer metatarsal (vs. absent); and posterior part of thighs without prominent reticulations, usually brown or orangish-brown (vs. light to dark red with thin black reticulations). Further, M. charlesdarwini differs from M. muangkanensis, a species endemic to Thailand and Myanmar, in possessing a distinct supratympanic fold that extends from posterior corner of upper eyelid, along the upper margin of tympanum, up to the shoulder (vs. indistinct supratympanic fold, and not extending up to posterior corner of upper eyelid and down to the shoulder); webbing between toes relatively reduced, up to the second subarticular tubercle on either side of toe IV (vs. above); and posterior part of thighs without reticulations, usually brown or orangish-brown (vs. light to dark brown with yellowish reticulations).

Distribution

Minervarya charlesdarwini is endemic to the Andaman Archipelago of India, where we find it to be widely distributed in all the major groups of islands: North and Middle Andamans (North Andaman Is., Interview Is., Middle Andaman Is., Baratang Is., and Long Is.), South Andamans (South Andaman Is., Neil Is., Havelock Is., Boat Is., Red Skin Is., Alexandra Is., Rutland Is., and Tarmugli Is.), up to the Little Andaman Island. This species has been observed between elevations of nearly sea level up to 600 m asl (Fig. 2; Table 2).

Table 2.

Distribution of Minervarya species reported in the present study from the Andaman and Nicobar Islands, India.

District / Group Island / Locality Coordinates Elevation
Latitude (°N) Longitude (°E) (meters)
Minervarya andamanensis
1 North Andaman Landfall Island 13.6680 93.0190 2
2 North Andaman Landfall Island 13.6630 93.0217 33
3 North Andaman Landfall Island 13.6406 93.0304 0.4
4 North Andaman East Island 13.6333 93.0450 9
5 North Andaman Landfall Island – South East 13.6299 93.0298 14
6 North Andaman East Island 13.6285 93.0481 30
7 North Andaman Paget Island 13.4321 92.8438 25
8 North Andaman Hathi Level 13.4068 92.9094 8
9 North Andaman Badur Tikrey 13.3685 92.9632 13
10 North Andaman Smith Island 13.3494 93.0570 4
11 North Andaman Smith Island 13.3465 93.0527 8
12 North Andaman Aerial Bay 13.2728 93.0319 18
13 North Andaman Durgapur 13.2711 93.0376 4
14 North Andaman Kishori Nagar 13.2711 92.9596 63
15 North Andaman Durgapur 13.2672 93.0382 24
16 North Andaman Durgapur 13.2644 93.0407 18
17 North Andaman Madhupur 13.2589 92.9805 13
18 North Andaman Madhupur 13.2585 92.9772 13
19 North Andaman Khudirampur 13.2361 92.9768 11
20 North Andaman Shibpur 13.2339 93.0490 8
21 North Andaman Kalipur 13.2240 93.0454 5
22 North Andaman Lamiya Bay 13.2037 93.0408 10
23 North Andaman Khudirampur 13.2033 92.9691 36
24 North Andaman Kishori Nagar 13.2025 92.9690 31
25 North Andaman Lamiya Bay 13.2010 93.0380 36
26 North Andaman Khudirampur 13.1994 92.9731 41
27 North Andaman Saddle Peak 13.1967 93.0314 34
28 North Andaman Lamiya Bay 13.1930 93.0340 53
29 North Andaman Sita Nagar 13.1881 92.9290 43
30 North Andaman Saddle Peak 13.1860 93.0260 57
31 North Andaman Sita Nagar 13.1853 92.9246 92
32 North Andaman Saddle Peak 13.1850 93.0190 224
33 North Andaman Kalara 13.1752 92.9341 47
34 North Andaman Kalpong Dam 13.1140 92.9971 60
35 North Andaman Kalighat 13.1013 92.9912 40
36 North Andaman Ram Nagar 13.0800 93.0151 22
37 North Andaman Ram Nagar 13.0724 93.0145 28
38 North Andaman Patti Level 13.0596 92.9907 123
39 North Andaman Interview Island 12.8999 92.7200 20
40 Middle Andaman Mayabunder, Austin Strait 12.8934 92.8574 28
41 Middle Andaman Mayabunder, Tugapur 12.8395 92.8568 13
42 Middle Andaman Mayabunder, Hanspuri 12.7581 92.8059 74
43 Middle Andaman Mayabunder, Chainpur 12.7396 92.8068 28
44 Middle Andaman Rangat, Cuthbert Bay 12.7090 92.9680 7
45 Middle Andaman Rangat, Mount Diavalo 12.6800 92.9400 156
46 Middle Andaman Rangat, Mount Diavalo 12.6800 92.9420 98
47 Middle Andaman Rangat, Dhanni Nallah 12.6160 92.9550 11
48 Middle Andaman Rangat, Moricedera 12.5535 92.9712 17
49 Middle Andaman Rangat, Parnashala 12.5265 92.9053 26
50 Middle Andaman Rangat, Yeratta 12.5038 92.9028 40
51 Middle Andaman Rangat, Bakultala 12.5015 92.8857 119
52 Middle Andaman Rangat, Shyamkund 12.4910 92.8480 38
53 Middle Andaman Rangat, Sabari 12.4861 92.9002 13
54 Middle Andaman Rangat, Vishnupur 12.4840 92.8734 17
55 Middle Andaman Rangat, Vishnupur 12.4756 92.8766 7
56 Middle Andaman Rangat, Ullidera 12.4718 92.8613 9
57 Middle Andaman Rangat, Ullidera 12.4715 92.8634 10
58 Middle Andaman Rangat, Bharatpur 12.4680 92.8930 16
59 Middle Andaman Rangat, Bronil 12.4631 92.8312 5
60 Middle Andaman Rangat, Panchawati 12.4078 92.8877 9
61 Middle Andaman Long Island, Sigman Dera 12.3820 92.9290 37
62 Middle Andaman Long Island, Lalaji Bay Forest 12.3790 92.9350 60
63 Middle Andaman Long Island 12.3710 92.9220 60
64 Middle Andaman North Passage Island 12.2880 92.9334 12
65 Middle Andaman Baratang Island, Shankar Nallah 12.2543 92.8041 64
66 Middle Andaman Baratang Island, Shankar Nallah 12.2543 92.8041 67
67 Middle Andaman Baratang Island, Loroijg 12.2389 92.7957 37
68 Middle Andaman Baratang Island, Roglachang 12.1603 92.7936 26
69 Middle Andaman Baratang Island, Baludera 12.1363 92.8069 8
70 Middle Andaman Baratang Island, Baludera 12.1357 92.8032 4
71 Middle Andaman Baratang Island, Jarawa Creek 12.1250 92.7881 18
72 Middle Andaman Baratang Island, Wrafters Creek 12.1127 92.7680 45
73 Middle Andaman Baratang Island, Wrafters Creek 12.1105 92.7725 21
74 Middle Andaman Baratang Island, Wrafters Creek 12.1066 92.7722 12
75 Middle Andaman Baratang Island, Naya Dera 12.0974 92.7535 54
76 South Andaman Jirkatang – 21km 12.0930 92.7070 73
77 South Andaman Jarawa Reserve 12.0581 92.7128 59
78 South Andaman Jarawa Reserve, Jirkatang – 16km 12.0560 92.7020 89
79 South Andaman Havelock Island, Govind Nagar 12.0418 92.9831 6
80 South Andaman Havelock Island, Shyam Nagar 12.0087 92.9635 58
81 South Andaman Havelock Island, Krishna Nagar 12.0076 92.9612 61
82 South Andaman Jarawa Reserve, Jirkatang – 6km 11.9650 92.6770 105
83 South Andaman Jirkatang 11.9453 92.6812 127
84 South Andaman Jirkatang 11.9060 92.6660 132
85 South Andaman Shoal Bay – 19 11.8967 92.7662 33
86 South Andaman Shoal Bay – 19 11.8950 92.7650 16
87 South Andaman Shoal Bay – 1 11.8820 92.7470 56
88 South Andaman Shoal Bay 11.8770 92.7410 31
89 South Andaman Shoal Bay 11.8747 92.7402 23
90 South Andaman Shoal Bay 11.8746 92.7406 32
91 South Andaman Shoal Bay 11.8710 92.7420 87
92 South Andaman Jirkatang 11.8680 92.6550 82
93 South Andaman Shoal Bay 11.8570 92.7350 21
94 South Andaman Shoal Bay 10 11.8438 92.7293 6
95 South Andaman Shoal Bay 10 11.8410 92.7290 35
96 South Andaman Neil Island 11.8354 93.0362 6
97 South Andaman Shoal Bay – 8 11.8270 92.7220 9
98 South Andaman Kalatang 11.8050 92.7140 27
99 South Andaman Wrightmayo Creek 11.8010 92.7080 16
100 South Andaman Kalatang 11.7958 92.7118 18
101 South Andaman Mount Harriet 11.7570 92.7320 308
102 South Andaman Mount Harriet 11.7440 92.7390 285
103 South Andaman Wimberlygunj 11.7375 92.7132 42
104 South Andaman Kadakachang, Stewartgunj 1 11.7330 92.7150 61
105 South Andaman Tirur 11.7312 92.6146 10
106 South Andaman Mount Harriet 11.7290 92.7420 87
107 South Andaman Mount Harriet 11.7250 92.7370 211
108 South Andaman Kadakachang, Mathura 11.7230 92.6810 16
109 South Andaman Mount Harriet 11.7202 92.7339 351
110 South Andaman Katagachang 11.7160 92.6940 18
111 South Andaman Tirur–Jhau kona Hotspot 11.7123 92.5727 49
112 South Andaman Mazar Pahad 11.7030 92.6370 12
113 South Andaman Gandhi Park 11.6617 92.7408 45
114 South Andaman Ograbraj 11.6577 92.6631 4
115 South Andaman Rachibasthi 11.6469 92.7280 61
116 South Andaman Corbyns Cove 11.6434 92.7442 12
117 South Andaman BSI Garden 11.6390 92.7367 16
118 South Andaman Garacharma 11.6238 92.7041 17
119 South Andaman Chouldhari 11.6225 92.6685 3
120 South Andaman Garacharma 11.6180 92.7062 2
121 South Andaman Wandoor 11.6177 92.6167 15
122 South Andaman Wandoor 11.6149 92.6190 15
123 South Andaman Sippighat 11.6125 92.6931 11
124 South Andaman Bathu Basti 11.6120 92.7183 58
125 South Andaman Tarmugli Island, Mummy Dera 11.6028 92.5413 12
126 South Andaman Tarmugli Island 11.5935 92.5437 19
127 South Andaman Alexandra Island 11.5851 92.6031 15
128 South Andaman Alexandra Island 11.5850 92.6060 40
129 South Andaman Alexandra Island 11.5770 92.6030 39
130 South Andaman Tarmugli Island 11.5650 92.5523 24
131 South Andaman Boat Island 11.5329 92.5579 24
132 South Andaman Boat Island 11.5268 92.5652 18
133 South Andaman Boat Island 11.5240 92.5600 33
134 South Andaman Burmanallah 11.5225 92.7209 40
135 South Andaman Chidiyatapu 11.5162 92.6992 13
136 South Andaman Chidyatapu 11.5081 92.6915 10
137 South Andaman Rutland Island 11.5080 92.6439 40
138 South Andaman Rutland Island 11.5078 92.6436 36
139 South Andaman Rutland Island 11.5066 92.6426 39
140 Little Andaman V. K. Pur 10.7590 92.5530 23
141 Little Andaman V. K. Pur 10.7460 92.5410 26
142 Little Andaman Donghighat 10.7379 92.5703 12
143 Little Andaman Rabinder Nagar Dam 10.7150 92.5360 71
144 Little Andaman Rabinder Nagar Dam 10.7080 92.5350 63
145 Little Andaman Rabinder Nagar Dam 10.7050 92.5430 68
146 Little Andaman RK Pur Dam 10.7020 92.5490 44
147 Little Andaman Krishna Nala 10.6783 92.5396 72
148 Little Andaman Krishna Nala 10.6710 92.5130 114
149 Little Andaman Netaji Nagar 10.6630 92.5440 29
150 Little Andaman Kalapather 10.6597 92.5765 5
151 Little Andaman Netaji Nagar 10.6493 92.5409 57
152 Little Andaman White Surf Water Fall 10.6290 92.5280 87
153 Little Andaman Rabinder Nagar Dam 10.5945 92.5326 -1
154 Little Andaman Farm Tikery 10.5890 92.5241 73
155 Little Andaman Herimidhar Bay 10.5870 92.5330 4
156 Little Andaman Ongi Tikery 10.5710 92.5540 34
Minervarya charlesdarwini
157 North Andaman Hathi Level 13.4068 92.9094 6
158 North Andaman Badur Tikrey 13.3685 92.9632 13
159 North Andaman Kishori Nagar 13.2711 92.95955 62
160 North Andaman Durgapur 13.2672 93.0382 23
161 North Andaman Lamiya Bay 13.2037 93.0408 10
162 North Andaman Khudirampur 13.2033 92.9691 36
163 North Andaman Khudirampur 13.2026 93.0375 72
164 North Andaman Kishori Nagar 13.2025 92.9690 31
165 North Andaman Lamiya Bay 13.2010 93.0380 36
166 North Andaman Saddle Peak 13.1967 93.0314 72
167 North Andaman Lamiya Bay 13.1930 93.0340 54
168 North Andaman Saddle Peak 13.1860 93.0260 54
169 North Andaman Saddle Peak 13.1850 93.0190 219
170 North Andaman Kalara 13.1752 92.9341 47
171 North Andaman Kalpong Dam 13.1140 92.9971 59
172 North Andaman Ram Nagar 13.0800 93.0151 8
173 North Andaman Patti Level 13.0596 92.9907 122
174 North Andaman Interview Island 12.8999 92.7200 22
175 North Andaman Interview Island 12.8953 92.6884 78
176 Middle Andaman Mayabunder, Austin Strait 12.8934 92.8574 28
177 Middle Andaman Mayabunder, Tugapur 12.8395 92.8568 13
178 Middle Andaman Mayabunder, Hanspuri 12.7581 92.8059 73
179 Middle Andaman Mayabunder, Chainpur 12.7396 92.8068 28
180 Middle Andaman Rangat, Mount Diavalo 12.6800 92.9420 99
181 Middle Andaman Rangat, Moricedera 12.5535 92.9712 15
182 Middle Andaman Rangat, Parnashala 12.5265 92.9053 24
183 Middle Andaman Rangat, Yeratta 12.5038 92.9028 36
184 Middle Andaman Rangat, Bakultala 12.5015 92.8857 119
185 Middle Andaman Rangat, Shyamkund 12.4910 92.8480 36
186 Middle Andaman Rangat, Sabari 12.4861 92.9002 12
187 Middle Andaman Rangat, Vishnupur 12.4840 92.8734 63
188 Middle Andaman Rangat, Ullidera 12.4715 92.8634 15
189 Middle Andaman Rangat, Bharatpur 12.4680 92.8930 16
190 Middle Andaman Rangat, Bronil 12.4631 92.8312 5
191 Middle Andaman Rangat, Panchawati 12.4078 92.8877 8
192 Middle Andaman Long Island, Sigman Dera 12.3820 92.9290 38
193 Middle Andaman Long Island, Lalaji Bay Forest 12.3790 92.9350 60
194 Middle Andaman Long Island, Long Island 12.3710 92.9220 60
195 Middle Andaman Baratang Island, Shankar Nallah 12.2543 92.8041 68
196 Middle Andaman Baratang Island, Shankar Nallah 12.2543 92.8041 68
197 Middle Andaman Baratang Island, Loroijg 12.2389 92.7957 37
198 Middle Andaman Baratang Island, Roglachang 12.1603 92.7936 21
199 Middle Andaman Baratang Island, Baludera 12.1357 92.8032 5
200 Middle Andaman Baratang Island, Jarawa Creek 12.1250 92.7881 17
201 Middle Andaman Baratang Island, Wrafters Creek 12.1127 92.7680 46
202 Middle Andaman Baratang Island, Wrafters Creek 12.1105 92.7725 21
203 Middle Andaman Baratang Island, Naya Dera 12.0974 92.7535 54
204 South Andaman Jirkatang – 21km 12.0930 92.7070 73
205 South Andaman Jirkatang – 16km 12.0560 92.7020 85
206 South Andaman Jirkatang – 6km 11.9650 92.6770 106
207 South Andaman Jirkatang 11.9453 92.6812 126
208 South Andaman Jirkatang 11.9060 92.6660 133
209 South Andaman Shoal Bay – 19 11.8950 92.7650 16
210 South Andaman Shoal Bay – 19 11.8910 92.7790 13
211 South Andaman Shoal Bay – 1 11.8820 92.7470 57
212 South Andaman Shoal Bay 11.8770 92.7410 29
213 South Andaman Shoal Bay 11.8747 92.7402 25
214 South Andaman Shoal Bay 11.8746 92.7406 55
215 South Andaman Shoal Bay 11.8746 92.7406 55
216 South Andaman Shoal Bay 11.8710 92.7420 87
217 South Andaman Jirkatang 11.8680 92.6550 83
218 South Andaman Shoal Bay 11.8570 92.7350 21
219 South Andaman Shoal Bay – 10 11.8410 92.7290 37
220 South Andaman Neil Island 11.8354 93.0362 6
221 South Andaman Shoal Bay – 8 11.8270 92.7220 9
222 South Andaman Kalatang 11.8050 92.7140 23
223 South Andaman Wrightmayo Creek 11.8010 92.7080 15
224 South Andaman Boat Island, Kalatang 11.7958 92.7118 19
225 South Andaman Mount Harriet 11.7570 92.7320 310
226 South Andaman Tirur–Jhau Kona Hotspot 11.7510 92.6120 12
227 South Andaman Mount Harriet 11.7440 92.7390 387
228 South Andaman Mount Harriet 11.7290 92.7420 87
229 South Andaman Mount Harriet 11.7250 92.7370 197
230 South Andaman Mount Harriet 11.7202 92.7339 351
231 South Andaman Tirur–Jhau Kona Hotspot 11.7190 92.5850 17
232 South Andaman Mazar Pahad 11.7030 92.6370 12
233 South Andaman Gandhi Park 11.6617 92.7408 46
234 South Andaman BSI Garden 11.6390 92.7367 18
235 South Andaman Wandoor 11.6149 92.6190 15
236 South Andaman Tarmugli Island 11.6028 92.5413 11
237 South Andaman Alexandra Island 11.5850 92.6060 42
238 South Andaman Alexandra Island 11.5770 92.6030 38
239 South Andaman Redskin Island 11.5691 92.5931 34
240 South Andaman Chidiyatapu 11.5162 92.6992 13
241 South Andaman Chidyatapu 11.5081 92.6915 11
242 South Andaman Rutland Island 11.5080 92.6439 40
243 South Andaman Rutland Island 11.5078 92.6436 36
244 South Andaman Rutland Island 11.5066 92.6426 37
245 Little Andaman V. K. Pur 10.7590 92.5530 21
246 Little Andaman V. K. Pur 10.7460 92.5410 27
247 Little Andaman Donghighat 10.7410 92.5750 17
248 Little Andaman Rabinder Nagar Dam 10.7150 92.5360 67
249 Little Andaman Rabinder Nagar Dam 10.7080 92.5350 62
250 Little Andaman Rabinder Nagar Dam 10.7050 92.5430 70
251 Little Andaman RK Pur Dam 10.7020 92.5490 45
252 Little Andaman Krishna Nallah 10.6783 92.5396 72
253 Little Andaman Krishna Nalla 10.6710 92.5130 117
254 Little Andaman Netaji Nagar 10.6630 92.5440 30
255 Little Andaman Netaji Nagar 10.6493 92.5409 60
256 Little Andaman Kalapather 10.6407 92.5423 5
257 Little Andaman White Surf Water Fall 10.6290 92.5280 88
258 Little Andaman Rabinder Dam 10.5945 92.5326 -1
Minervarya nicobariensis
259 Nicobar, Central group Bompoka Island 8.2494 93.2218 36
260 Nicobar, Central group Kamorta Island, Kakana 8.1731 93.5070 22
261 Nicobar, Central group Kamorta Island, Vikas Nagar 8.1198 93.5138 31
262 Nicobar, Central group Kamorta Island, Changhua 8.0212 93.4916 72
263 Nicobar, Central group Nancowry Island, Champin 8.0202 93.5548 63
264 Nicobar, Central group Kamorta Island, Munak 8.0123 93.5045 69
265 Nicobar, Central group Kamorta Island, Alukian 8.0057 93.4932 63
266 Nicobar, Central group Nancowry Island, Malacca 8.0053 93.5675 73
267 Nicobar, Central group Katchal Island, Kapanga 7.9992 93.3928 85
268 Nicobar, Central group Katchal Island, Beachdera 7.9969 93.3585 62
269 Nicobar, Central group Nancowry Island, Itoi 7.9961 93.5315 74
270 Nicobar, Central group Katchal Island, Lal Munak 7.9879 93.3737 52
271 Nicobar, Central group Katchal Island, Upper Katchal 7.9407 93.4434 69
272 Nicobar, Southern group Little Nicobar Island, Makachua 7.4069 93.7096 41
273 Nicobar, Southern group Little Nicobar Island, Pulo Panja 7.3760 93.7395 39
274 Nicobar, Southern group Great Nicobar Island, Afra Bay 7.1662 93.7662 166
275 Nicobar, Southern group Great Nicobar Island, Navy Dera 7.1353 93.8840 38
276 Nicobar, Southern group Great Nicobar Island, Navy Dera 7.1239 93.8870 34
277 Nicobar, Southern group Great Nicobar Island, Laxman Beach 7.0214 93.9176 27
278 Nicobar, Southern group Great Nicobar Island, East West Road 7.0189 93.9233 36
279 Nicobar, Southern group Great Nicobar Island, Old East West Road 7.0176 93.9231 28
280 Nicobar, Southern group Great Nicobar Island, Campbell Bay 7.0152 93.9230 40
281 Nicobar, Southern group Great Nicobar Island, Govind Nagar 7.0040 93.9095 52
282 Nicobar, Southern group Great Nicobar Island, GNBR Check Post 7.0016 93.8834 56
283 Nicobar, Southern group Great Nicobar Island, Govind Nagar 7.0011 93.8958 40
284 Nicobar, Southern group Great Nicobar Island, East West Road 6.9957 93.8831 49
285 Nicobar, Southern group Great Nicobar Island, Magar Nallah 6.9945 93.9124 18
286 Nicobar, Southern group Great Nicobar Island, East West Road 6.9814 93.8644 92
287 Nicobar, Southern group Great Nicobar Island, Chingam Basti 6.9705 93.9192 106
288 Nicobar, Southern group Great Nicobar Island, Jogindar Nagar 6.9513 93.9199 13
289 Nicobar, Southern group Great Nicobar Island, Laxmi Nagar 6.9039 93.8920 35
290 Nicobar, Southern group Great Nicobar Island, Vijay Nagar 6.8729 93.8893 50
291 Nicobar, Southern group Great Nicobar Island, Gandhi Nagar 6.8404 93.8907 14
292 Nicobar, Southern group Great Nicobar Island, Galathea Bay 6.8231 93.8631 32
293 Nicobar, Southern group Great Nicobar Island, Sastri Nagar 6.8104 93.8920 37
294 Nicobar, Southern group Great Nicobar Island, Old Chingam Basti 6.8026 93.8458 34
295 Nicobar, Southern group Great Nicobar Island, Indira Point 6.7597 93.8257 35
Minervarya agricola
296 North Andaman Badur Tikrey 13.3685 92.9632 18
297 North Andaman Ram Nagar 13.2759 93.0186 7
298 North Andaman Durgapur 13.2671 93.0382 22
299 North Andaman Madhupur 13.2585 92.9772 10
300 North Andaman Shibpur 13.2339 93.0490 7
301 North Andaman Khudirampur 13.2033 92.9691 34
302 North Andaman Kishori Nagar 13.2025 92.9690 31
303 North Andaman Lamiya Bay 13.2010 93.0380 37
304 North Andaman Lamiya Bay 13.1930 93.0340 53
305 North Andaman Sita Nagar 13.18533 92.9246 93
306 Middle Andaman Mayabunder, Hanspuri 12.7581 92.8059 74
307 Middle Andaman Mayabunder, Chainpur 12.7396 92.8068 28
308 Middle Andaman Rangat, Parnashala 12.5265 92.9053 23
309 Middle Andaman Rangat, Yeratta 12.5038 92.9028 41
310 Middle Andaman Rangat, Shyamkund 12.4910 92.8480 36
311 Middle Andaman Rangat, Sabari 12.4861 92.9002 14
312 Middle Andaman Rangat, Panchawati 12.4078 92.8877 7
313 Middle Andaman Baratang Island, Lolachang 12.1603 92.7936 24
314 Middle Andaman Baratang Island, Baludera 12.1357 92.8032 5
315 Middle Andaman Baratang Island, Wrafters Creek 12.1127 92.7680 46
316 Middle Andaman Baratang Island, Naya Dera 12.0974 92.7535 54
317 South Andaman Havelock Island, Govind Nagar 12.0337 92.9866 6
318 South Andaman Havelock Island, Shyam Nagar 12.0087 92.9635 57
319 South Andaman Havelock Island, Krishna Nagar 12.0076 92.9612 62
320 South Andaman Havelock Island, Kalapather 11.982 93.0161 21
321 South Andaman Jirkatang 11.9453 92.6812 127
322 South Andaman Shoal Bay – 19 11.8950 92.7650 16
323 South Andaman Shoal Bay – 19 11.8910 92.7790 11
324 South Andaman Shoal Bay – 1 11.8820 92.7470 57
325 South Andaman Shoal Bay 11.8770 92.7410 29
326 South Andaman Shoal Bay 11.8747 92.7402 27
327 South Andaman Shoal Bay 11.8746 92.7406 29
328 South Andaman Shoal Bay 11.8710 92.7420 88
329 South Andaman Shoal Bay 11.8570 92.7350 21
330 South Andaman Shoal Bay –10 11.8410 92.7290 37
331 South Andaman Neil Island 11.8354 93.0362 6
332 South Andaman Shoal Bay – 8 11.8270 92.7220 8
333 South Andaman Kalatang 11.7958 92.7118 19
334 South Andaman Wimberlygunj 11.7375 92.7132 42
335 South Andaman Kadakachang, Stewartgunj 1 11.7330 92.7150 54
336 South Andaman Tirur 11.7288 92.6127 17
337 South Andaman Mazar Pahad 11.7030 92.6370 12
338 South Andaman Mazhar Pahad 11.7028 92.6380 13
339 South Andaman Gandhi Park 11.6617 92.7408 33
340 South Andaman Ograbraj 11.6577 92.6631 4
341 South Andaman BSI Garden 11.6390 92.7367 16
342 South Andaman Chouldhari 11.6225 92.6685 3
343 South Andaman Garacharma 11.6180 92.7062 2
344 South Andaman Garacharma 11.6151 92.7000 15
345 South Andaman Wandoor 11.6149 92.6190 15
346 South Andaman Sippighat 11.6125 92.6931 12
347 South Andaman Corbyns Cove 11.5906 92.6749 4
348 South Andaman Burmanallah 11.5225 92.7209 37
349 South Andaman Chidiyatapu 11.5162 92.6992 13
350 South Andaman Chidyatapu 11.5081 92.6915 10
351 Little Andaman V. K. Pur 10.7460 92.5410 29
352 Little Andaman Rabinder Nagar Dam 10.7080 92.5350 63
353 Little Andaman Netaji Nagar 10.6630 92.5440 33
354 Little Andaman Netaji Nagar 10.6493 92.5409 59
355 Little Andaman Kalapather 10.6407 92.5423 4
356 Little Andaman Farm Tikery 10.5890 92.5241 72
357 Little Andaman Ongi Tikery 10.5710 92.5540 33

Minervarya andamanensis (Stoliczka, 1870)

Figs 1, 2, 5, 6; Tables 1, 2 Andamanese minervaryan frog

Note

This species was originally described as a variety of Rana gracilis var. andamanensis Stoliczka, 1870. The description was based on four specimens—one “about one-third of an inch long” (~9 mm), “two next above one inch” (~ 25 mm), and “the fourth 2⅓rd inches” (~ 60 mm). Of these, ZSIC 3539 (ZSIC 8539 according to Chanda et al. 2001 “2000”) was designated as the lectotype by Annandale (1917). Furthermore, three of the original syntypes—two from the ZSI collection and one in the NHM collection—were suggested to represent two other dicroglossid species (see detailed taxonomic remarks for Limnonectes doriae and L. hascheanus). Hence, Minervarya andamanensis was restricted to a single juvenile specimen, which we found to be in an extremely dehydrated condition (Fig. 6). Since the lectotype is not reliable for identification, much of what is known of this nomen is based on its original description (Stoliczka 1870) and a subsequently published illustration (Annandale 1917). Additional specimens were reported by Annandale (1917), and further, based on tentatively identified records its phylogenetic position and relationships have also been discussed (Kotaki et al. 2010; Sanchez et al. 2018; Garg and Biju 2021). Recently, Chandramouli et al. (2021) provided a redescription of the species based on new collections. In our study, we further report the prevalence of high morphological variations among individuals of this species. Typically, M. andamanensis has been identified based on its chestnut-brown dorsal colouration and dark brown lateral surfaces (e.g., Annandale 1917; Sarkar 1990; Chandramouli 2017). However, we observe that this character is not constant, and several genetically confirmed individuals with uniform colouration and other colour morphs from our study are conspecific (Figs 5, 6). In addition, we find the Little Andaman population to be divergent from that found in South Andamans (see Phylogenetic Results). Hence, in order to aid further studies, below we provide a revised morphological diagnosis for the species, compare it with other closely related members of the M. andamanensis species group, discuss morphological variations accompanied with detailed illustrations, and also shed light on the possibility of this species having been confused with other dicroglossids found in the regions (see taxonomic remarks for M. charlesdarwini, Limnonectes doriae and L. hascheanus).

Redescription (all measurements in mm)

A medium-sized species (males: SVL 36.2–42.2, 39.2±2.1, N=6; females: SVL 39.4–57.1, 48.6±7.4, N=6), body stout and robust; head longer in males (HL 14.3–17.0, 15.2±1.0 vs. HW 12.4–15.9, 13.9±1.2, N=6) and subequal in females (HL 14.2–20.9, 17.6±3.1, N=6 vs. HW 13.8–21.6, 17.7±2.9, N=6); snout rounded or subovoid in dorsal and ventral view, rounded or obtuse in lateral view; snout length (males: SL 5.6–7.4, 6.4±0.7; females: SL 5.8–8.6, 7.3±1.1) longer than horizontal diameter of eye (males: EL 4.4–5.4, 4.8±0.5; females: EL 4.0–6.6, 5.2±1.0); loreal region obtuse; indistinct canthus rostralis; interorbital space flat; tympanum diameter (males: TYD 2.4–3.3, 2.8± 0.3; females: TYD 2.9–4.4, 3.3±0.6) nearly ⅗th of the eye diameter (males: EL 4.4–5.4, 4.8±0.5; females: EL 4.0–6.6, 5.2±1.0); pineal ocellus present; supratympanic fold well developed, extending from the posterior corner of the eye down to nearly the shoulder; vomerine ridge present, bearing small teeth; tongue moderately long, emarginated (Figs 5, 6). Forearm length (males: FAL 7.2–9.1, 8.0±0.8; females: FAL 8.7–11.8, 9.6±1.4) shorter than hand length (males: HAL 8.6–9.8, 9.2±0.5; females: HAL 10.1–13.2, 11.6±1.2); subarticular tubercles prominent, single, circular, all present; prepollex oval, prominent; two rounded palmar tubercles; supernumerary tubercles absent; relative length of fingers II<I=IV<III; tip of fingers bluntly rounded, not enlarged into discs. Hind limbs shorter in comparison to the body length with tibiotarsal articulation reaching up to the anterior end of eye when hind limb is stretched along the body; thigh (males: TL 18.4–21.9, 19.9±1.3; females: TL 20.9–30.1, 24.8±3.4) shorter than shank (males: SHL 20.1–24.1, 21.7±1.6; females: SHL 24.5–31.3, 27.4±2.8) and foot (males: FOL 20.1–23.7, 21.7±1.5; females: FOL 23.4–29.6, 25.7±2.9); total foot length (males: TFOL 28.1–34.9, 31.3±2.9; females: TFOL 33.0–41.4, 36.5±2.8); toe tips rounded, slightly swollen without discs, toes without dermal fringes, webbing between toes moderate: I1+–2II1+–2III1+–2IV2–1+V; subarticular tubercles prominent, all present; inner metatarsal tubercle prominent, elongate; outer metatarsal tubercle small, prominent, rounded; supernumerary tubercles absent (Figs 5, 6).

Comparison (only with males)

Minervarya andamanensis cannot be confused with other known members of the genus Minervarya, except three members of the M. andamanensis group (M. charlesdarwini, M. nicobariensis, and M. muangkanensis). Minervarya andamanensis can be distinguished from M. nicobariensis by its head longer than wide, HL 15.2±1.0 vs. HW 13.9±1.2 (vs. wider, HW 17.5±1.0 vs. HL 16.5±1.1); shank nearly equal to foot, SHL 21.7±1.6 vs. FOL 21.7±1.5 (vs. shorter, SHL 20.9±1.0 vs. FOL 22.1±1.5); presence of outer metatarsal tubercle (vs. absent); and posterior part of thighs light to dark brown with yellowish reticulations (vs. light to dark red with thin black reticulations). Further, it differs from M. muangkanensis (based on Köhler et al. 2019) in having a larger adult male size, SVL 36.2–42.2, 39.2±2.1, N=6 (vs. SVL 25.8–35.1, 31.2±3.1, N=7); supratympanic fold distinct, extending from posterior corner of upper eyelid, along upper margin of tympanum, down to the shoulder (vs. indistinct supratympanic fold and not down to the shoulder); webbing between the toes relatively reduced, up to the second subarticular tubercle on either side of toe IV (vs. above). For comparison with M. charlesdarwini, see the comparison section of that species.

Distribution

Minervarya andamanensis is endemic to the Andaman Archipelago of India, where we find it to be widely distributed in all the major groups of islands: North and Middle Andamans (North Andaman Is., Landfall Is., East Is., Paget Is., Interview Is., Smith Is., Long Is., North Passage Is., North Reef Is., Baratang Is., and Middle Andaman Is.), South Andamans (South Andaman Is., Boat Is., Alexandra Is., Tarmugli Is., Rutland Is., Neil Is., and Havelock Is.), down to the Little Andaman Island. This species has been observed between elevations of sea level up to nearly 400 m asl (Fig. 2; Table 2).

On the occurrence of Limnonectes doriae (Boulenger, 1887) and Limnonectes hascheanus (Stoliczka, 1870) in Andaman Islands

Two species of the genus Limnonectes Fitzinger, 1843 are purported to occur in the Andaman Islands. The reports of both L. doriae (Boulenger 1887) by Annandale (1917) and L. hascheanus by Boulenger (1920) are based on three out of the four reported type specimens of Rana gracilis var. andamanensis Stoliczka, 1870 (current name combination: Minervarya andamanensis). While describing M. andamanensis, Stoliczka (1870) mentioned examination of “four specimens from Port Blair”, of which three types available in the collection of ZSI, Kolkata were stated as “2732, 3538–9” “Types of R. gracilis, var. andamanensis, Stol.” by Sclater (1892) under the name Rana limnocharis (on page 6), and not as Rana doriae (on page 4, reported only from Burma) as later suggested by Chanda et al. (2001 “2000”). Of these, Annandale (1917) found two to be labelled as types and selected 3539 as the type; therefore by implication designating it as the lectotype, which he found distinct enough to be recognised as a subspecies or a local race of R. limnocharis (current name combination: Fejervarya limnocharis Gravenhorst, 1829). At the same time, however, it was Annandale (1917) who stated that the larger and better preserved of the two labelled types undoubtedly belongs to R. doriae Boulenger, 1887 (current name combination: Limnonectes doriae) and the same was followed by Boulenger (1920), who additionally discussed that “one of the types received from the Indian museum in 1893” belonged to Rana hascheana Stoliczka, 1870 (current name combination: Limnonectes hascheanus). Following these works, Smith (1941) included L. doriae in the herpetofauna of Andamans, but did not mention L. hascheanus. Sarkar (1990) reported the distribution of L. doriae in both the Andaman and Nicobar group of islands based on examination of “16 frogs”—two from Stoliczka’s Andaman collection (possibly referring to two syntypes of M. andamanensis), another of Stoliczka’s Nicobar collection, and several other collections made by subsequent workers. He also included L. hascheanus in the faunal list of Andamans, following Boulenger (1920), although clearly stating “I have got no specimen in my disposal” (Sarkar 1990). In addition, Sarkar (1990) provided a vouchered record of Rana macrodon var. blythii Boulenger, 1920 (currently, a composite of Limnonectes blythii, L. leporinus, and possibly L. malesianus) based on material from “Tribeni Nullah, Campbell Bay, Great Nicobar” collected in 1977. Dutta (1997) stated the number of the type of Rana gracilis var. andamanensis housed in the NHM, London collection as BMNH 1947.2.1.23. Later, Chanda et al. (2001 “2000”) corrected the catalogue numbers for two types deposited at ZSI, including the lectotype, as ZSI 8538 and ZSI 8539, while also stating that two of the three types “cannot be located at present” (possibly referring to ZSI 2732 and ZSI 3538 / 8538 that were regarded as belonging to L. doriae). The available lectotype of Minervarya andamanensis, however in our observation, carries the number “3539” on the original label found inside the specimen jar and “ZSI 8539” on the outside label.

Over the years, both Limnonectes doriae and L. hascheanus have been included in the regional faunal lists of the Andaman Islands (e.g., Das 1999; Harikrishnan et al. 2010, 2012; Chandramouli et al. 2015; Rangasamy et al. 2018), however without any new vouchered records. Neither has any subsequent study attempted to provide morphological diagnoses or clear explanations in support of what became the first reports of these species and the genus Limnonectes from the region. Harikrishnan and Vasudevan (2018) emphasised on the need for detailed studies to confirm the occurrence of L. doriae and L. hascheanus, and two unnamed Limnonectes mentioned by Das (1999), in the Andaman group of islands. Inger and Stuart (2010) have previously discussed that L. hascheanus is restricted to high elevations of about 1000 feet above sea level in southern parts of the Malay Peninsula, and expressed doubts on its occurrence in the Andamans. Following this, Harikrishnan and Vasudevan (2018) suggested the record of L. hascheanus from Andamans to be considered tentative.

The present study failed to locate the original syntypes (now paralectotypes) of Rana gracilis var. andamanensis that were identified as belonging to Limnonectes hascheanus and L. doriae (SDB personal observation at NHM in 2010; SDB and SG personal observation at ZSI in 2018). Neither did we locate any other specimens referable to these species from this region in potential museums such as ZSIC (Kolkata, India), ZSI/ANRC (Andaman and Nicobar, India), and NHM (London). The additional material reportedly studied by Sarkar (1990) for L. doriae originated from various surveys and lacks accompanying voucher or museum information, making their traceability difficult. Hence, during our study, we made an extensive effort to locate frogs possibly referable to L. doriae and L. hascheanus in the Andaman Islands, particularly at the type locality of Minervarya andamanensis in Port Blair and surroundings. Instead of locating these species, we found the populations of M. andamanensis collected from Andaman Islands to be extremely variable in size, skin texture, dorsal colouration and markings (Figs 5, 6), including the absence of the distinctive chestnut-brown dorsal colouration with dark brown lateral surfaces that are considered typical of this species (Annandale 1917; Chandramouli et al. 2015, 2021). Several morphologically variable individuals were also included in our molecular analyses and found to be conspecific or shallowly divergent, providing evidence that even though these populations exhibit morphological variations they represent a single widely distributed species. Hence, the variation among M. andamanensis individuals (such as variable skin colouration, markings, texture, and their overall robust and stout appearance) could have been a source of confusion leading to the presumed occurrence of Limnonectes doriae and L. hascheanus in India.

Figure 5. 

Morphological variation in skin colouration and markings observed among individuals of Minervarya andamanensis. A–J Dorsolateral views. A SDBDU 2021.4206 (♀). B SDBDU 2021.4207 (♀). C–D Not preserved (♂). E SDBDU 2020.4179 (♀). F SDBDU 2010.4178a (♀). G SDBDU 2019.4011 (♂). H SDBDU 2020.4155 (♂). I Not preserved (♂). J SDBDU 2019.3956 (♂). Photographs: S. D. Biju, G. Gokulakrishnan & Sonali Garg.

Figure 6. 

Morphological variation observed among individuals of Minervarya andamanensis. A Lectotype (ZSIC 3539 / ZSIC 8539). B–H Dorsal views. B SDBDU 2020.4181 (♀). C SDBDU 2020.4154 (♂). D SDBDU 2021.4207 (♀). E SDBDU 2020.4171a (♀). F SDBDU 2020.4179 (♀). G SDBDU 2020.4155 (♂). H SDBDU 2020.4180 (♂). I–K Ventral views. I SDBDU 2020.4180 (♂). J SDBDU 2020.4154 (♂). K SDBDU 2020.4171a (♀). L Lateral view, SDBDU 2021.4291 (♀). M–N Ventral view of hand, SDBDU 2021.4207 and SDBDU 2000.4179, respectively). O Schematic illustration of foot webbing, SDBDU 2021.4207 (♀). P–Q Ventral view of foot, SDBDU 2020.4179 and SDBDU 2001.4207, respectively. R Posterior view of thigh, SDBDU 2020.4179 (♀). S. Dorsal view of thigh, SDBDU 2021.4207 (♀). Photographs: S. D. Biju.

At the same time, we observed that Minervarya charlesdarwini and M. andamanensis occur sympatrically in most of the reported and surveyed localities. With both the species being extremely variable in dorsal colour and markings, the possibility of L. doriae and L. hascheanus being misidentifications of M. charlesdarwini cannot be ruled out. While describing L. hascheanus from Peninsular Malaysia, Stoliczka (1870) discussed a “W mark” (page 147 and pl. IX, fig. 3), which was also discussed to be present in the NHM specimen of Rana gracilis var. andamanensis (BMNH 1947.2.1.23) by Boulenger (1920). We have found several similar-sized specimens of M. charlesdarwini possessing a W-shaped mark (Figs 3, 4), providing support for possible misidentifications between the two taxa. As for L. doriae, based on the description of specimens Sarkar (1990) regarded as belonging to this species, most of the discussed characters could be confused with Limnonectes species, as well as their ecology “collected from marshy area in deep forests” appear to be comparable with M. charlesdarwini. Hence, we believe that the suggested occurrence of both L. doriae and L. hascheanus in Andamans is likely to have been based on misidentifications of either M. charlesdarwini or M. andamanensis, or possibly even a mix of both these morphologically variable and highly confusing species (Figs 36). Chandramouli (2017) also reported on some overlooked museum specimens collected by Annandale and deposited under the name “Rana doriae andamanensis” as belonging to M. charlesdarwini.

In light of the above and the fact that no recent surveys, especially since the description of Minervarya charlesdarwini, have reported new specimens referable to the two Limnonectes species, except for their mostly unverified inclusion in regional checklists, the occurrence of both L. doriae and L. hascheanus in Andamans should not only be considered erroneous but the two should be excluded from the list of Andaman amphibians to avoid further confusions. It is also interesting that Stoliczka could have collected the enigmatic M. charlesdarwini over a century ago, in 1869. However, we may not know with certainty, unless the discovery of the ‘lost’ specimens from Stoliczka’s collection, or the verification of at least some specimens examined by Sarkar (1990), whose judgement was based on both Stoliczka’s and subsequent additional collections.

Affinity of Minervarya nicobariensis (Stoliczka, 1870) of the Nicobar Islands

The only minervaryan species to be reported from the Nicobar group of the Andaman and Nicobar Archipelago is Minervarya nicobariensis (Stoliczka, 1870). This taxon was originally described as a new variety “var. nicobariensis” of Rana gracilis Wiegmann sensu Günther, 1864 (= Fejervarya limnocharis Gravenhorst, 1829) from “the Nicobars, in the neighbourhood of the Nancowri harbour”. The description was based on “one peculiar young specimen” measuring “1¼th inch” (= 31.75 mm), which was later stated to be ZSIC 2679 by Sclater (1892). The type was reported as lost (Dubois 1984) or unlocatable (Chanda et al. 2001 “2000”), and later, as “lost or destroyed” by Chandramouli and Prasad (2020) who also designated ZSI/ANRC/T/12326 from “Munak, Camorta Island [in the vicinity of the holotype locality fide Stoliczka 1870]” as a neotype. While trying to locate the original name-bearing type at ZSI Kolkata we found two young specimens ZSIC 3567 (SVL 13.6 mm) and ZSIC 3570 (SVL 13.4 mm) both labelled as “syntype”. However, these numbers have not been reported in any of the previous works, hence a further investigation will be necessary to ascertain their type status.

Since the original description, this taxon has been moved to three currently recognised dicroglossid genera, Limnonectes, Fejervarya, and Minervarya, chiefly owing to the different genus-level reorganisations proposed within the family (e.g., Dubois 1987; Dubois and Ohler 2000; Sanchez et al. 2018). Chandramouli and Prasad (2020) redescribed the species based on fresh adult and larval collections and provided a revised diagnosis as M. nicobariensis. They also briefly reported on the natural history, call characteristics, and distribution of the species in the Nicobar Islands. Garg and Biju (2021) assigned this species to the M. andamanensis species group based on morphological affinities. In the present study, our detailed morphological study of several additional new and museum specimens of this species, including the neotype, reveals a close relationship between M. nicobariensis and M. charlesdarwini of the Andaman Islands (Fig. 7).

Not only do these two species share several unique morphological traits (such as scattered dorsal and lateral tubercles with black spots, presence of discontinuous skin folds on dorsum, upper ⅔rd of tympanum and inner margin of tympanic fold dark brown, absence of prominent markings on groin, and ventral surfaces of hand and foot light grey to blackish-brown) compared to other members of the Minervarya andamanensis group, but also exhibit similarities in being primarily associated with forest habitats and their phytotelm breeding preferences. In view of the surprising phylogenetic position of M. charlesdarwini revealed in the present study, which had alluded researchers for several years, a sister relationship of M. nicobariensis with M. charlesdarwini is likely to be expected, for which a future molecular assessment can provide a conclusive evidence.

Distribution. Minervarya nicobariensis is endemic to the Nicobar Archipelago of India, where we find it to be widely distributed in the central and southern group of islands: Central Nicobar (Bompoka Is., Kamorta Is., Nancowry Is., and Katchal Is.) and South Nicobar (Little Nicobar and Great Nicobar). This species has been observed between elevations of nearly sea level up to 170 m asl (Fig. 2; Table 2).

New distribution record of Minervarya agricola (Jerdon, 1853) from Andaman Islands

Minervarya agricola is one of the most widely distributed species of minervaryan frogs having a distribution across the Indian mainland (from Tamil Nadu, Kerala, Karnataka, Maharashtra, Gujarat, Rajasthan, Punjab, Haryana, Delhi, Uttarakhand, Uttar Pradesh, Chhattisgarh, Andhra Pradesh, Odisha, West Bengal, Bihar, up to Assam), Nepal, Bangladesh, and Sri Lanka (Garg and Biju 2021). Our samples of a smaller-sized minervaryan species from North, Middle, South, and Little Andamans were phylogenetically (Fig. 1; Table 1) and morphologically (Fig. 8) conspecific with M. agricola, providing the first record of this species from these islands. The 16S gene sequences from the Andamanese M. agricola are identical to those from the typical mainland populations of the species. Morphologically also, the individuals from Andamans exhibit only minor variations in skin colouration and markings (Fig. 8) that are usually observed in this species across its entire known range. This species could have been previously misidentified either as Fejervaryalimnocharis’ or Minervarya andamanensis, both of which are frequently reported to occur in the Andaman Islands (e.g., Sclater 1892; Sarkar 1990; Pillai 1991; Dutta 1997; Das 1999; Harikrishnan and Vasudevan 2018; Rangasamy et al. 2018). However, the taxon with which M. agricola may have been confused with remains unclear as the name F.limnocharis’ was also applied to F. moodiei populations from the Andamans by studies in the past (Chandramouli et al. 2020b), while M. andamanensis, even though widely reported and frequently included in regional checklists, is only known with certainty from a handful of available museum specimens (Annandale 1917; Chandramouli et al. 2021). A record of Rana keralensis (= Minervarya keralensis) from Andamans based on a specimen “measuring 30 mm” (Pillai 1991) could also be a misidentification of M. agricola; although none of the subsequent studies seem to have included this taxon in the regional checklists. During our examination of the ZSI/ANRC collection, we did though locate some specimens of M. agricola labelled as Fejervarya limnocharis, a name that has been used extensively for several misidentified minervaryan and fejervaryan species across South and South-east Asia for nearly two centuries. Hence, in addition to providing a new distribution record of M. agricola from the Andaman Archipelago, our study provides further support for the absence of F. limnocharis from this region.

Figure 7. 

Morphological variation in skin colouration and markings observed among individuals of Minervarya nicobariensis in Nicobar Islands (all males). A–C Dorsolateral views. A SDBDU 2021.4250. B SDBDU 2021.4249. C SDBDU 2021.4251. D–G Dorsal views. D SDBDU 2021.4251. E SDBDU 2021.4250. F SDBDU 2021.4252. G SDBDU 2021.4249. H–I Ventral views. H SDBDU 2021.4250. I SDBDU 2021.4249. J Lateral view (SDBDU 2021.4249). K Dorsal view of thighs (SDBDU 2021.4249). L–N Posterior view of thighs. L SDBDU 2021.4250. M SDBDU 2021.4249. N SDBDU 2021.4256. O Ventral view of thighs (SDBDU 2021.4249). P Ventral view of hand (SDBDU 2021.4249). Q Ventral view of foot (SDBDU 2021.4249). R Schematic illustration of foot webbing (SDBDU 2021.4249). Photographs: S. D. Biju and G. Gokulakrishnan.

Figure 8. 

Morphological variation observed among individuals of Minervarya agricola. A–E Dorsolateral views. A Not preserved (♂). B SDBDU 2020.4151 (♂). C SDBDU 2019.3987 (♀). D SDBDU 2019.3986 (♂). E SDBDU 2019.3988 (♂). F Dorsal view, SDBDU 2020.4151 (♂). G–H Ventral view, SDBDU 2020.4151 (♂) and SDBDU 2019.3987 (♀), respectively. I Lateral view, SDBDU 2020.4151(♂). J Posterior view of thigh, SDBDU 2020.4151 (♂). K Dorsal view of thigh, SDBDU 2019.4027 (♀). L Ventral view of hand, SDBDU 2020.4151 (♂). M Ventral view of foot, SDBDU 2020.4151 (♂). N Schematic illustration of foot webbing, SDBDU 2020.4151 (♂). Photographs: S. D. Biju and Sonali Garg.

Distribution. Minervarya agricola is a widely distributed species of South and Southeast Asia, being found in India, Sri Lanka, Bhutan, Nepal, Bangladesh, Myanmar, Thailand, and southern China (Garg and Biju 2021). In the Andaman Archipelago of India, we provide new reports of this species from all the major groups of islands: North and Middle Andamans (North Andaman Is., Baratang Is., and Middle Andaman Is.), South Andamans (South Andaman Is., Neil Is., and Havelock Is.), up to the Little Andaman Island. This species has been observed between elevations of sea level up to elevations of nearly 130 m asl (Fig. 2; Table 2).

Discussion

The surprising systematic relationships of Minervarya charlesdarwini and the intertwined taxonomic histories of other minervaryan species in the Andaman and Nicobar Islands provide an opportunity to reflect on the need and importance of dedicated taxonomic studies even in relatively less diverse regions. The Andaman and Nicobar are home to barely 21 recognised species of amphibians. Nonetheless, contrary to the widespread belief that all of the floral and faunal components of this region have affinities with the Indo-Burma and Sundaland, the archipelago houses some unique and endemic species that were previously thought to have shared distributions with neighbouring regions. Despite the fact that many of the endemic species were long known to be fairly common and locally abundant their identities remained ambiguous for decades and centuries; for example, M. andamanensis (Sanchez et al. 2018; Chandramouli et al. 2021; Garg and Biju 2021; present study), M. nicobariensis (Chandramouli and Prasad 2020; present study), M. charlesdarwini (Chandramouli 2017; present study), Kaloula ghoshi (Chandramouli and Prasad 2018), Microhyla chakrapanii (Garg et al. 2019) and M. nakkavaram (Garg et al. 2022). The dicroglossid frogs of the islands have received the least attention, again owing to their presumed widespread distributions. The findings from our study, as well as other recent works, have shown that three out of four species of the Minervarya andamanensis species group (M. andamanensis, M. charlesdarwini, and M. nicobariensis) are endemic to the archipelago (Chandramouli 2017; Harikrishnan and Vasudevan 2018; Chandramouli and Prasad 2020; Chandramouli et al. 2021; present study). At the same time, the puzzling systematic relationships of these species have resulted in erroneous reports of two other genera, Ingerana and Limnonectes, from these islands. Our study confirms the absence of genus Ingerana from the Andamans and further provides evidence for the exclusion of Limnonectes members from the Andaman amphibian fauna. In view of these findings, the identities and systematic affinities of dicroglossid frogs of Nicobar also require a detailed reassessment using integrative approaches. For example, based on morphological similarities, Minervarya nicobariensis is expected to phylogenetically nest within the M. andamanensis group, while the occurrence of the genus Limnonectes in the Nicobars, based on reports of L. doriae and L. macrodon by Sarkar (1990), and L. shompenorum described by Das (1996) from the Nicobars, remains uninvestigated. Of these, L. shompenorum is particularly interesting and remains poorly known. This taxon was previously shown to represent a Limnonectes member based on extralimital populations from the neighbouring regions of Sumatra (Tjong et al. 2010), however, the typical Nicobar population of L. shompenorum have not been assessed and lack genetic data.

The benefits of molecular data, particularly in aiding rapid resolution of long-standing taxonomic confusions, are shown by many recent amphibian studies (e.g., Zimkus and Schick 2010; Bellati et al. 2018; Brown et al. 2017; Garg et al. 2018; Mahony et al. 2020; Scherz et al. 2020; Bisht et al. 2021; Garg and Biju 2021; Patel et al. 2021). The integration of such approaches in taxonomy can have significant implications on the known diversity, distribution patterns, as well as conservation requirements. Often, species are considered data deficient in conservation assessments due to lack of sufficient knowledge, but in fact some could be facing extinction threats while researchers attempt to study them using traditional and time-consuming taxonomic approaches alone. Hence, in regions with a manageable number of known taxa, such as Andaman and Nicobar, a rapid molecular assessment of all species, combined with detailed morphological studies, and possibly other aspects such as acoustics, larval morphology, and breeding biology, can go a long way in improving the knowledge and protecting the region’s unique amphibian fauna. Although dicroglossids represent a large proportion of the known diversity of the Andaman and Nicobar archipelago, several other groups lack proper taxonomic studies (Harikrishnan and Vasudevan 2018), with molecular data altogether absent for most species. Currently, out of 21 species, only 10 have been genetically assessed, that too during the past decade alone: M. andamanensis (Kotaki et al. 2010, Sanchez et al. 2018, Garg and Biju 2021, Chandramouli et al. 2021, present study), Blythophryne beryet (Chandramouli et al. 2016), Microhyla chakrapanii, M. nakkavaram (Garg et al. 2019, 2022), Fejervarya limnocharis, F. moodiei (Chandramouli et al. 2020b), Bijurana nicobariensis (Chandramouli et al. 2020a), Rohanixalus vittatus (Biju et al. 2020), and now M. agricola and M. charlesdarwini (present study). The currently known members of the family Ranidae, for example, are all reported from neighbouring regions. Some of these species identifications (Chalcorana chalconota and Hylarana erythraea) are solely based on their presumed extended distributions from the neighbouring regions and lack detailed studies. Hence, our study emphasises on the need to expand the use of molecular data in taxonomic studies for all known frog groups of the Andaman and Nicobar.

Extensive surveys can also yield additional new taxa and distribution records. Chandramouli et al. (2016) recently described a new genus of arboreal toads (Blythophryne) and Biju et al. (2020) revealed the presence of a previously unreported family in the Andamans (Rhacophoridae). To this, our study adds a new report of Minervarya agricola from the Andaman group of islands. This species is known to occur widely in mainland South Asia, including Sri Lanka based on previously misidentified DNA sequences (Garg and Biju 2021). Its occurrence in Andamans provides another insular record for the species. The fact that the Andaman populations of M. agricola are genetically identical to the mainland populations could also indicate the possibility of it having been introduced into these islands through human agencies, as in general suggested to be the case for several herpetofaunal components, particularly on the larger islands that have human presence (Das 1999). Nonetheless, this finding opens new questions on the patterns of distribution of minervaryan frogs, particularly how some species acquired widespread distributions including colonisation of islands (such as members of the M. agricola species group), whereas other groups exhibit considerable species-level endemism, such as M. andamanensis species group in the Andaman and Nicobar, M. greenii species group in Sri Lanka, and most of others being restricted to the Western Ghats of Peninsular India (M. sahyadris group, M. mysorensis group, M. rufescens group, and M. nilagirica), except M. syhadrensis group. Therefore, with an improved understanding of the diversity and distribution patterns, the genus Minervarya certainly emerges as an interesting model group for future phylogeographic studies, especially with respect to the unique location and geological history of the Andaman and Nicobar group of islands. Geologically, the Andamans are known to have had land connections with the Arakan mountain range of Myanmar owing to the lowering of sea levels during the Late Pleistocene, and are therefore considered to have Indo-Chinese faunal affinities; whereas the islands of Nicobar are of oceanic origin and much of their herpetofauna is believed to have been acquired through short-distance transoceanic dispersal of the Indo-Malayan components (Das 1999). Animal groups that have limited overseas dispersal abilities, such as frogs, can therefore provide opportunities to understand whether this long chain of islands could have served as a dispersal route for amphibians between the Indo-Burma and Sundaland regions, and also as a refuge for remnants of ancient lineages that may be surviving precariously in the wake of increasing anthropogenic pressures, developmental threats, and anticipated long-term impacts of climate change on these islands.

Acknowledgements

We thank the Department of Environment and Forests, Andaman and Nicobar Islands, India for study permissions and logistic support; Kailash Chandra and Kaushik Deuti (ZSI, Kolkata), and Barry Clarke and David Gower (NHM, London) for access to specimens under their care and museum support to SDB and SG; Gunther Köhler for photograph of Minervarya muangkanensis used in Fig. 1. This study was partially supported by grants from Ministry of Environment, Forest and Climate Change, Government of India, and SERB, Department of Science and Technology, Government of India to CS; Faculty Research Programme Grant–Institution of Eminence (Ref. No./IoE/2021/12/FRP) from University of Delhi to SDB; and a research grant (5409-0260) from Re:wild (formerly Global Wildlife Conservation), USA to SG. SG is also supported by the Council for Scientific and Industrial Research [CSIR No. 09/045(1694)/2019-EMR-I], Government of India. GC receives Junior Research Fellowship from CSIR-UGC. CS and GG express sincere thanks to the Director, Zoological Survey of India for cooperation and encouragement during the period of the study.

References

  • Annandale N (1917) Zoological results of a tour in the Far East. Batrachia. Memoirs of the Asiatic Society of Bengal 6: 119–155.
  • Bellati A, Scherz MD, Megson S, Roberts SH, Andreone F, Rosa GM, Noël J, Randrianirina JE, Fasola M, Glaw F, Crottini A (2018) Resurrection and re-description of Plethodontohyla laevis (Boettger, 1913) and transfer of Rhombophryne alluaudi (Mocquard, 1901) to the genus Plethodontohyla (Amphibia, Microhylidae, Cophylinae). Zoosystematics and Evolution 94(1): 109–135. https://doi.org/10.3897/zse.94.14698
  • Biju SD, Garg S, Gokulakrishnan G, Chandrakasan S, Thammachoti P, Ren J, Gopika C, Bisht K, Hamidy A, Shouche Y (2020) New insights on the systematics and reproductive behaviour in tree frogs of the genus Feihyla, with description of a new related genus from Asia (Anura, Rhacophoridae). Zootaxa 4878(1): 1–55. https://doi.org/10.11646/zootaxa.4878.1.1
  • Bisht K, Garg S, Sarmah ANDA, Sengupta S, Biju SD (2021) Lost, forgotten, and overlooked: Systematic reassessment of two lesser-known toad species (Anura, Bufonidae) from Peninsular India and another wide-ranging northern species. Zoosystematics and Evolution 97(2): 451–470. https://doi.org/10.3897/zse.97.61770
  • Bossuyt F, Milinkovitch MC (2000) Convergent adaptive radiations in Madagascan and Asian ranid frogs reveal covariation between larval and adult traits. Proceedings of the National Academy of Sciences of the United States of America 97(12): 6585–6590. https://doi.org/10.1073/pnas.97.12.6585
  • 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. Systematic Biology 55: 579–594. https://doi.org/10.1080/10635150600812551
  • Boulenger GA (1887) An account of the Reptiles and Batrachians obtained in Tenasserim by M. L. Fea of the Genoa Civic Museum. Annali del Museo Civico di Storia Naturale di Genova. Serie 2, 5: 474–486.
  • Boulenger GA (1920) A monograph of the South Asian, Papuan, Melanesian and Australian frogs of the genus Rana. Records of the Indian Museum 20: 1–226.
  • Brown RM, Siler CD, Richards SJ, Diesmos AC, Cannatella DC (2015) Multilocus phylogeny and a new classification for Southeast Asian and Melanesian forest frogs (family Ceratobatrachidae). Zoological Journal of the Linnean Society 174: 130–168. https://doi.org/10.1111/zoj.12232
  • Brown RM, Prue A, Onn CK, Gaulke M, Sanguila MB, Siler CD (2017) Taxonomic reappraisal of the Northeast Mindanao stream frog, Sanguirana albotuberculata (Inger 1954), Validation of Rana mearnsi, Stejneger 1905, and Description of a New Species from the Central Philippine. Herpetological Monographs 31: 182–203. https://doi.org/10.1655/HERPMONOGRAPHS-D-16-00009.1
  • Chanda SK, Das I, Dubois A (“2000” 2001) Catalogue of amphibian types in the collection of the Zoological Survey of India. Hamadryad 25(2): 100–128.
  • Chandramouli SR, Khan T, Yathiraj R, Deshpande N, Yadav S, Tejpal C, de Groot S, Lammes I (2015) Diversity of amphibians in Wandoor, South Andaman, Andaman and Nicobar Islands, India. Alytes 32: 47–54.
  • Chandramouli SR, Vasudevan K, Harikrishnan S, Dutta SK, Janani SJ, Sharma R, Das I, Aggarwal RK (2016) A new genus and species of arboreal toad with phytotelmonous larvae, from the Andaman Islands, India (Lissamphibia: Anura: Bufonidae). ZooKeys 555: 57–90. https://doi.org/10.3897/zookeys.555.6522
  • Chandramouli SR (2017) Rediscovery and redescription of a little known, insular endemic frog, Ingerana charlesdarwini (Das, 1998) (Amphibia: Anura: Dicroglossidae) from the Andaman Islands, Bay of Bengal. Alytes 33(1): 47–54.
  • Chandramouli SR, Hamidy A, Amarasinghe AAT (2020a) A reassessment of the systematic position of the Asian ranid frog Hylorana nicobariensis Stoliczka, 1870 (Amphibia: Anura) with the description of a new genus. Taprobanica 09(01): 121–132. https://doi.org/10.47605/tapro.v9i1.226
  • Chandramouli SR, Ankaiah D, Prasad KVD, Arul V (2020b) On the identity of two Fejervarya frog (Dicroglossidae) species from the Andaman and Nicobar Archipelago. Taprobanica 09(02): 194–204. https://doi.org/10.47605/tapro.v9i2.231
  • Chandramouli SR, Prasad KVD (2020) Redescription of Minervarya nicobariensis (Stolizka, 1870) (Amphibia: Dicroglossidae) with a neotype designation. Taprobanica 09(02): 205–209. https://doi.org/10.47605/tapro.v9i2.232
  • Chandramouli SR, Ankaiah D, Prasad KVD, Arul V (2021) Redescription of a poorly known, insular endemic frog Minervarya andamanensis (Stoliczka, 1870) with notes on distribution and natural history. Spixiana 44(1): 43–53.
  • Das I (1996) Limnonectes shompenorum, a new species of ranid frog of the Rana macrodon complex from Great Nicobar, India. Journal of South Asian Natural History 2: 127–134.
  • Das I (1998) A remarkable new species of ranid (Anura: Ranidae), with phytotelmonous larvae, from Mount Harriet, Andaman Island. Hamadryad 23: 41–49.
  • Das I (1999) Biogeography of the amphibians and reptiles of the Andaman and Nicobar Islands, India. In: Ota H (Ed.) Tropical Island Herpetofauna: Origin, Current Diversity, and Conservation. Elsevier Science B. V, Amsterdam, Lausanne, New York, Oxford, Shannon, Singapore, Tokyo, 43–77.
  • Das I, Dutta SK (2007) Sources of larval identities of amphibians of India. Hamadryad 31(2): 152–181.
  • Dinesh KP (2009) An annotated checklist of Amphibia of India with some insights into the patterns of species discoveries, distribution, and endemism. Records of Zoological Survey of India, Occasional Paper No. (302): 1–152.
  • Dinesh KP, Vijayakumar SP, Channakeshavamurthy BH, Torsekar VR, Kulkarni NU, Shanker K (2015) Systematic status of Fejervarya (Amphibia, Anura, Dicroglossidae) from South and SE Asia with the description of a new species from the Western Ghats of Peninsular India. Zootaxa 3999(1): 79–94. http://doi.org/10.11646/zootaxa.3999.1.5
  • Dubois A (1984) Note preliminaire sur le groupe de Rana limnocharis Gravenhorst, 1829 (Amphibiens, Anoures). Alytes 3: 143–159.
  • Dubois A (1987) Miscellanea taxinomica Batrachologica (I). Alytes 5: 7–95.
  • Dubois A, Ohler A (2000) Systematics of Fejervarya limnocharis (Gravenhorst, 1829) (Amphibia, Anura, Ranidae) and related species. 1. Nomenclatural status and type-specimens of the nominal species Rana limnocharis Gravenhorst, 1829. Alytes, 18(1–2): 15–50.
  • Dubois A, Ohler A, Biju SD (2001) A new genus and species of Ranidae (Amphibia, Anura) from south-western India. Alytes 19(2–4): 53–79.
  • Dubois A, Crombie RI, Glaw F (2005) Amphibia Mundi. 1.2. Recent amphibians: generic and infrageneric taxonomic additions (1981–2002). Alytes 23(1–2): 25–69.
  • Dutta SK (1997) Amphibians of India and Sri Lanka (Checklist and Bibliography). Odyssey Publishing House, Bhubaneswar, xiii+342+xxii pp.
  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32(5): 1792–1797. https://doi.org/10.1093/nar/gkh340
  • Fitzinger LJ (1843) Systema Reptilius. Fasciculus Primus Amblyglossae. Vindobonae [Vienna], Braumüller et Seidel, 106+vi+3 pp. [reprinted 1973 by the Society for the Study of Amphibians and Reptiles, Oxford, Ohio].
  • Frost DR (2006) Amphibian Species of the World: an Online Reference. Version 4.0.
  • Frost DR, Grant T, Faivovich J, Bain RH, Haas A, Haddad CFB, de Sá RO, Channing A, Wilkinson M, Donnellan SC, Raxworthy CJ, Campbell JA, Blotto BL, Moler PE, Drewes RC, Nussbaum RA, Lynch JD, Green DM, Wheeler WC (2006) The amphibian tree of life. Bulletin of the American Museum of Natural History 297: 1–370. https://doi.org/10.1206/0003-0090(2006)297[0001:TATOL]2.0.CO;2
  • Garg S, Biju SD (2017) Description of four new species of Burrowing frogs in the Fejervarya rufescens complex (Dicroglossidae) with notes on morphological affinities of Fejervarya species in the Western Ghats. Zootaxa 4277(4): 451–490. https://doi.org/10.11646/zootaxa.4277.4.1
  • Garg S, Biju SD (2021) DNA barcoding and systematic review of minervaryan frogs (Dicroglossidae: Minervarya) of Peninsular India: resolution of a taxonomic conundrum with description of a new species. Asian Herpetological Research 12(4): 1–34. https://doi.org/10.16373/j.cnki.ahr.210023
  • Garg S, Das A, Kamei RG, Biju SD (2018) Delineating Microhyla ornata (Anura, Microhylidae) mitochondrial DNA barcodes resolve century-old taxonomic misidentification. Mitochondrial DNA Part B 3(2): 856–861. https://doi.org/10.1080/23802359.2018.1501286
  • Garg S, Suyesh R, Das A, Jiang J, Wijayathilaka N, Amarasinghe AAT, Alhadi F, Vineeth KK, Aravind NA, Senevirathne G, Meegaskumbura M, Biju SD (2019) Systematic revision of Microhyla (Microhylidae) frogs of South Asia: a molecular, morphological, and acoustic assessment. Vertebrate Zoology 69(1): 1–71. https://doi.org/10.26049/VZ69-1-2019-01
  • Garg S, Suyesh R, Das S, Bee MA, Biju SD (2021) An integrative approach to infer systematic relationships and define species groups in the shrub frog genus Raorchestes, with description of five new species from the Western Ghats, India. PeerJ 9: e10791. https://doi.org/10.7717/peerj.10791
  • Garg S, Sivaperuman C, Gokulakrishnan G, Chandramouli SR, Biju SD (2022) Hiding in plain sight: rain water puddles in Nicobar Islands of India reveal abundance of a new frog species of the genus Microhyla Tschudi, 1838 (Anura: Microhylidae). Zoological Studies 61: 2. https://doi.org/10.6620/ZS.2022.61-02
  • Gravenhorst JLC (1829) Deliciae Musei Zoologici Vratislaviensis. Fasciculus primus. Chelonios et Batrachia. Leipzig: Leopold Voss, 106 pp.
  • Günther ACLG (1864) The Reptiles of British India. London: Taylor and Francis.
  • Harikrishnan S, Vasudevan K, Choudhury BC (2010) A review of herpetofaunal descriptions and studies from Andaman and Nicobar Islands, with an updated checklist. In: Ramakrishna, Raghunathan C, Sivaperuman C (Eds) Recent Trends in Biodiversity of Andaman and Nicobar Islands. Zoological Survey of India, Kolkata, 387–398.
  • Harikrishnan S, Chandramouli SR, Vasudevan K (2012) A survey of herpetofauna on Long Island, Andaman and Nicobar Islands, India. Herpetological Bulletin 2012(119): 19–28.
  • Harikrishnan S, Vasudevan K (2018) Amphibians of the Andaman and Nicobar Islands: distribution, natural history, and notes on taxonomy. Alytes 36(1–4): 238–265.
  • Howlader MSA (2011) Cricket frog (Amphibia: Anura: Dicroglossidae): two regions of Asia are corresponding two groups. Bonnoprani: Bangladesh Wildlife Bulletin 5(1–2): 1–7.
  • Huelsenbeck JP, Ronquist F, Neilsen R, Bollback JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294(5550): 2310–2314. https://doi.org/10.1126/science.1065889
  • Iskandar DT (1998) The Amphibians of Java and Bali. Research and Development Centre for Biology. Bogor: LIPI and GEF Biodiviersity Collections Project, xix+117 pp.+26 pl.
  • Jerdon TC (1853) Catalogue of reptiles inhabiting the Peninsula of India. Journal of the Asiatic Society of Bengal 22: 22–534.
  • Khatiwada JR, Wang B, Zhao T, Xie F, Jiang JP (2021) An integrative taxonomy of amphibians of Nepal: An updated status and distribution. Asian Herpetological Research 12(1): 1–35. https://doi.org/10.16373/j.cnki.ahr.200050
  • Köhler G, Mogk L, Khaing K, Than NL (2019) The genera Fejervarya and Minervarya in Myanmar: description of a new species, new country records, and taxonomic notes (Amphibia, Anura, Dicroglossidae). Vertebrate Zoology 69(2): 183–226. https://doi.org/10.26049/VZ69-2-2019-05
  • Kotaki M, Kurabayashi A, Matsui M, Kuramoto M, Djong TH, Sumida M (2010) Molecular phylogeny of the diversified frogs of genus Fejervarya (Anura: Dicroglossidae). Zoological Science 27(5): 386–395. https://doi.org/10.2108/zsj.27.386
  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33(7): 1870–1874. https://doi.org/10.1093/molbev/msw054
  • Kuramoto M, Joshy SH, Kurabayashi A, Sumida M (2008 “2007”). The genus Fejervarya (Anura: Ranidae) in central Western Ghats, India, with descriptions of four new cryptic species. Current Herpetology 26: 81–105.
  • Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B (2017) Partition Finder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34(3): 772–773. https://doi.org/10.1093/molbev/msw260
  • Linnaeus C (1758) Systema Naturae Per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, Cum Characteribus, Differentiis, Synonymis, Locis. Editio Decima, Reformata. Tomus I. Laurentius Salvius, Holmiae [Stockholm], IV+823+(1) pp. [reprinted 1956, British Museum (Natural History), London].
  • Mahony S, Kamei RG, Teeling EC, Biju SD (2020) Taxonomic review of the Asian horned frogs (Amphibia: Megophrys Kuhl and Van Hasselt) of Northeast India and Bangladesh previously misidentified as M. parva (Boulenger), with descriptions of three new species. Journal of Natural History 54(1–4): 119–194. https://doi.org/10.1080/00222933.2020.1736679
  • Myers CW, Duellman WE (1982) A new species of Hyla from Cerro Colorado, and other tree frog records and geographical notes from western Panama. American Museum novitates 2752: 1–32.
  • Patel NG, Garg S, Das A, Stuart BL, Biju SD (2021) Phylogenetic position of the poorly known montane cascade frog Amolops monticola (Ranidae) and description of a new closely related species from Northeast India. Journal of Natural History 55(21–22): 1403–1440. https://doi.org/10.1080/00222933.2021.1946185
  • Pillai RS (1991) Contribution to the amphibian fauna of Andaman and Nicobar with a new record of the mangrove frog, Rana cancrivora. Records of the Zoological Survey of India 88: 41–44.
  • Pyron RA, Wiens JJ (2011) A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of advanced frogs, salamanders, and caecilians. Molecular Phylogenetics and Evolution 61(2): 543–583. https://doi.org/10.1016/j.ympev.2011.06.012
  • Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. (2018) Posterior summarization in bayesian phylogenetics using Tracer 1.7. Systematic Biology 67: 901–904. https://doi.org/10.1093/sysbio/syy032
  • Rangasamy V, Sivaperuman C, Gokulakrishnan G, Parthipan P (2018) Herpetofauna of Andaman and Nicobar Islands. In: Sivaperuman C, Venkatraraman K (Eds) Indian Hotspots: Vertebrate Faunal Diversity, Conservation and Management. Vol. 2. Springer, Singapore, 37–56. https://doi.org/10.1007/978-981-10-6983-3_3
  • Richards CM, Moore W (1996) A molecular phylogeny of the Old World tree frog family Rhacophoridae. Journal of herpetology 8: 41–46.
  • Roelants K, Jiang J, Bossuyt F (2004) Endemic ranid (Amphibia: Anura) genera in southern mountain ranges of the Indian subcontinent represent ancient frog lineages: evidence from molecular data. Molecular Phylogenetics and Evolution 31: 730–740. https://doi.org/10.1016/j.ympev.2003.09.011
  • Sanchez A, Biju SD, Islam M, Hasan M, Ohler A, Vences M, Kurabayashi A (2018) Phylogeny and classification of fejervaryan frogs (Anura: Dicroglossidae). Salamandra 54(2): 109–116.
  • Sarkar AK (1990) Taxonomic and ecological studies on the amphibians of Andaman and Nicobar Islands, India. Records of the Zoological Survey of India 86: 103–117.
  • Savage JM, Heyer WR (1967) Variation and distribution in the tree-frog genus Phyllomedusa in Costa Rica, Central America. Studies on Neotropical Fauna and Environment 5(2): 111–131. https://doi.org/10.1080/01650526709360400
  • Scherz MD, Rasolonjatovo SM, Köhler J, Rancilhac L, Rakotoarison A, Raselimanana AP, Ohler A, Preick M, Hofreiter M, Glaw F, Vences M (2020) ‘Barcode fishing’ for archival DNA from historical type material overcomes taxonomic hurdles, enabling the description of a new frog species. Scientific Reports 10: 19109. https://doi.org/10.1038/s41598-020-75431-9
  • Sclater WL (1892) List of the Batrachia in the Indian Museum. Taylor and Francis, London, i–viii+1–43 pp.
  • Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87(6): 651–701. https://doi.org/10.1093/aesa/87.6.651
  • Stoliczka F (1870) Observations on some Indian and Malayan Amphibia and Reptilia. Journal of the Asiatic Society of Bengal 39(2): 134–157.
  • Swofford DL (2002) PAUP*: Phylogenetic Analysis Using Parsimony (* and other methods). Version 4.0b10. Sinauer Association Inc., Sunderland, Massachusetts. [program]
  • Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics 68(4): 978–989. https://doi.org/10.1086/319501
  • Tjong DH, Iskandar DT, Gusman D (2010) Hubungan filogenetik spesies Limnonectes (Ranidae: Amphibia) asal Sumatera Barat dan asal Asia Tenggara berdasarkan gen 16S ribosomal RNA. Makara, Sains 14(1): 79–87. [In Bahasa Indonesia].
  • Trifinopoulos J, Nguyen LT, von Haeseler A, Minh BQ (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 44(W1): W232–W235. https://doi.org/10.1093/nar/gkw256
  • Yuan ZY, Zhow WW, Chen X, Poyarkov NA, Chen HM, Jang-Liaw NH, Chou WH, Matzke NJ, Iizuka K, Min MS, Kuzmin SL, Cannatella DC, Hillis DM, Zhang YP, Che J (2016) Spatiotemporal diversification of the true frogs (genus Rana): a historical framework for a widely studied group of model organisms. Systematic Biology 65(5): 824–842. https://doi.org/10.1093/sysbio/syw055
  • Zhang P, Liang D, Mao RL, Hillis DM, Wake DB, Cannatella DC (2013) Efficient sequencing of Anuran mtDNAs and a mitogenomic exploration of the phylogeny and evolution of frogs. Molecular Biology and Evolution 30(8): 1899–915. https://doi.org/10.1093/molbev/mst091
  • Zimkus BM, Schick S (2010) Light at the end of the tunnel: insights into the molecular systematics of East African puddle frogs (Anura: Phrynobatrachidae). Systematics and Biodiversity 8(1): 39–47. https://doi.org/10.1080/14772000903543004