Journal of Threatened Taxa | www.threatenedtaxa.org | 26 May 2021 | 13(6): 18624–18630

ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print)

https://doi.org/10.11609/jott.7250.13.6.18624-18630

#7250 | Received 05 March 2021 | Final received 13 April 2021 | Finally accepted 09 May 2021

Occurrence of Tamdil Leaf-litter Frog Leptobrachella tamdil (Sengupta et al., 2010) (Amphibia: Megophryidae) from Manipur, India and its phylogenetic position

Ht. Decemson ¹ , Vanlalsiammawii ² , Lal Biakzuala ³ , Mathipi Vabeiryureilai ⁴ , Fanai Malsawmdawngliana ⁵ & H.T. Lalremsanga ⁶

^1–6 Developmental Biology and Herpetology Laboratory, Department of Zoology, Mizoram University, Aizawl, Mizoram , 796004, India.

¹ htdecemson@gmail.com (corresponding author), ² siammawiikito@gmail.com, ³ bzachawngthu123@gmail.com, ⁴ m.vabeiryureilai@gmail.com, ⁵ sawmattr.yx@gmail.com, ⁶ htlrsa@yahoo.co.in (corresponding author)

Editor: S.R. Ganesh, Chennai Snake Park, Chennai, India. Date of publication: 26 May 2021 (online & print)

Citation: Decemson, Ht., Vanlalsiammawii, L. Biakzuala, M. Vabeiryureilai, F. Malsawmdawngliana & H.T. Lalremsanga (2021). Occurrence of Tamdil Leaf-litter Frog Leptobrachella tamdil (Sengupta et al., 2010) (Amphibia: Megophryidae) from Manipur, India and its phylogenetic position. Journal of Threatened Taxa 13(6): 18624–18630. https://doi.org/10.11609/jott.7250.13.6.18624-18630

Copyright: © Decemson et al. 2021. Creative Commons Attribution 4.0 International License. JoTT allows unrestricted use, reproduction, and distribution of this article in any medium by providing adequate credit to the author(s) and the source of publication.

Funding: National Mission on Himalayan Studies (NMHS), Uttarakhand, Government of India (Grant No: GBPNI/NMHS – 2017/MG – 22/566);

Department of Biotechnology, New Delhi, Government of India (Grant No:  DBT-NER/AAB/64/2017).

Competing interests: The authors declare no competing interests.

Acknowledgements: Heartfelt gratitude to Dr. A.K. Joshi, IFS, PCCF (WL Division), Chief Wildlife Warden, Department of Forest Head Office, Govt. of Manipur, Sanjenthong, Imphal 795001 for permission No.3/22/2018-WL (Vol-II) to carry out herpetological surveys in Chandel District, Manipur. Financial support from funding agencies the Natonal Mission on Himalayan Studies (NMHS), Grant no: GBPNI/NMHS – 2017/MG – 22/566 and Department of Biotechnology, New Delhi, Government of India (Grant No: DBT-NER/AAB/64/2017). Note of special appreciation to David Huten, Monoel Sinruwng, Huten Peshumhring for companion in fieldwork. Developmental Biology and Herpetology Laboratory, Department of Zoology, Mizoram University, Tanhril, Aizawl, Mizoram, India.

Abstract: We present a new state record of Leptobrachella tamdil from Manipur State, northeastern India based on three individuals collected from Chakpi stream, Chandel District. This record represents the range extension of the species as well as the easternmost distribution record. We also provide additional morphological data as well as the first time genetic data for the species and inferred its phylogenetic position using mitochondrial 16S rRNA marker gene sequence.

Keywords: 16S rRNA, morphology, northeastern India, phylogeny, range extension.

Leptobrachid frogs are one of the most speciose groups comprising 166 species with four genera namely Leptobrachella Smith, 1925, Leptobrachium Tschudi, 1838, Oreolalax Myers and Leviton, 1962, and Scutiger Theobald, 1868. The Tamdil Leaf-litter Frog belongs to the genus Leptobrachella which consists of 86 congeners that are presently known from southern China, northeastern India, Myanmar through Thailand, Vietnam to Malaysia, Borneo, and Natuna Island (Frost 2021). Leptobrachella tamdil was originally described as Leptolalax tamdil based on two specimens collected from the Tamdil National Wetland, Mizoram, India (Sengupta et al. 2010). It had been known only from its type locality for about a decade. An additional specimen was reported from Dampa Tiger Reserve (DTR) (23.387–23.705N; 92.273–92.431E), Mamit District, Mizoram near the Bangladesh international boundary by Vanlalsiammawii et al. (2020). Herein, we report the occurrence of L. tamdil from Chakpi Stream, Chandel District, Manipur State with comments on the taxon’s phylogenetic position inferred using partial sequences of mitochondrial 16S rRNA gene.

Methods

Herpetological surveys were carried out in two different bouts. The first trip was conducted during 16 December 2020 to 5 January 2021, and the second trip during 18 January 2021 to 24 January 2021, with a total of 27-days field trip, and covering a total distance of ca. 120km. On 16 December 2020, we encountered the first two adult male individual frogs (MZMU 2224 and MZMU 2225) from the Chakpi Stream bed (24.1454N, 93.5856E; 1,122m) at around 17.40h, the sampling site is located ca. 30km south from Chandel Town, Chandel District, Manipur (Figure 1). The nearest village from the collection site is the Lamphou Charu located at ca. 4km. After a month, on 23 January 2021 at 19.59h, we encountered an adult female (MZMU 2226) at the upper stream bed (24.1453N, 93.5857E; 1,228m) ca. 7m away from the previous collection site. During the present work, the sampling sites were visited four times at day time, dusk, and night time.

Specimens of L. tamdil collected in this study were photographed by using Sony DSC-HX400V (50x optical zoom) digital camera. Specimens (MZMU 2224, MZMU 2225, and MZMU 2226) were fixed in 4% formalin, later preserved in 70% ethyl alcohol, liver tissues were stored in 95% ethyl alcohol for molecular processing, and deposited in Museum of Zoology, Mizoram University (MZMU), India. The altitude with the geo-locations was recorded by using global positioning system device (Garmin Montana 650-GPS navigator). A digital thermo hygrometer (Kusam Meco KM 918) was used for measurement of temperature and relative humidity. The morphometric parameters of the specimens were measured by using Mitutoyo^TM (505–730) dial calipers and are given to the nearest 0.1mm. The sex was determined through dissection. The parameters from Sengupta et al. (2010) and Vanlalsiammawii et al. (2020) were followed to measure the frog specimens (Table 1).

Genomic DNA was extracted from the 95% ethanol preserved liver tissues of the frog specimens using QIAamp DNA Mini Kit (Cat No.ID:51306) following the manufacturer protocol. PCR reaction was prepared for 20μL reaction mixture contained 1X amplification buffer, 2.5 mMMgCl₂, 0.25 mM dNTPs, 0.2 pM each forward and reverse primer, 1μL genomic DNA, and 1U Taq DNA polymerase with a pair of partial 16S rRNA primers: forward (L02510- CGC CTG TTT ATC AAA AAC AT) (Palumbi 1996) and reverse (H03063- CTC CGG TTT GAA CTC AGA TC) (Rassmann 1997). The PCR thermal regime for amplification was 5 min at 95°C for initial denaturation, followed by 35 cycles of 1 min at 95°C for denaturation, 30s for annealing at 50.3°C, elongation for 1 min at 72°C, and a final elongation for 5 min at 72°C. PCR products were checked by gel electrophoresis on a 1.5% agarose gel containing ethidium bromide. Samples were sequenced using Sanger’s dideoxy method and sequencing reactions were carried out in both directions on a sequencer (Agrigenome Labs Pvt Ltd., Kochin, India). The generated partial 16S rRNA sequences were deposited in the GenBank repository (accession numbers: MW665130.1; MW665131.1; MW665132.1). In our dataset of 16S rRNA, we included 34 congeneric sequences obtained from National Centre for Biotechnology Information (NCBI) database and our generated sequence of Duttaphrynus melanostictus (MW165455.1) sample was used as an outgroup. All sequences were aligned by using Muscle algorithm in MEGA 7 (Kumar et al. 2016), the Kimura 2 (K2P) and genetic distances (Kimura, 1980) were calculated using MEGA 7 (Kumar et al., 2016). The Bayesian Inference (BI) phylogenetic tree (Figure 2) was constructed in MrBayes 3.2.5 using GTR+I+G model. The MCMC (one cold and three hot chains) was run for one million generations by sampling every 1,000 generations and set the burn-in to 25%. The analysis was terminated when the standard deviation of split frequencies was less than 0.001. The percentage of trees in which the associated taxa clustered together is shown next to the branches (Ronquist & Huelsenbeck 2003). The generated phylogenetic tree was further illustrated using Figtree 1.44v (Rambaut 2014).

Results

The collected specimens are identified as L. tamdil based on the original morphological diagnostic features (Sengupta et al. 2010), and the new specimens showed genetic homogeneity on the phylogenetic tree with the mean intra-species K2P genetic distance of 0.0%. Our recently collected specimens are diagnosed in showing the following combination of characters: SVL between 27.8–28.7 mm in males and 33.2mm in the only female; dorsum tuberculate; eyelids with tubercles; tympanum and supratympanic fold distinct; supratympanic fold extending to posterior edge of tympanum; macroglands, including preaxillary, pectoral, femoral and ventrolateral glands present; Finger II > I; toe tips not dilated, bearing dermal fringes; relatively long hind limbs, with heels in contact when limbs are held perpendicular to body; dorsum with dark blotches; flanks with small dark blotches; dark tympanic mask present; venter pale; labial bars present and limbs with dark cross-bars (Sengupta et al. 2010). Current location extends the range of the species by ca. 122km aerial distance northeast from the type locality at Tamdil National Wetland, Mizoram, India.

Our generated partial 16S rRNA gene sequences of L. tamdil (MW665130.1; MW665131.1; MW665132.1) were compared with the congeners sequences obtained from NCBI database. From the estimated K2P genetic distances (Table 2), we infered that L. laui (MH406903.1) to be the closest species by showing 9% genetic distance with the sequences of L. tamdil (MW665130.1; MW665131.1; MW665132.1). Moreover, the phylogenetic relationship revealed that L. tamdil formed a distinct lineage within the monophyletic clade comprising L. puhoatensis + L. petrops (Figure 2); the former taxon (L. puhoatensis) is known only from its type locality in Pu Hoat Nature Reserve, Vietnam, and the later (L. petrops) is recorded only from four Provinces (Tuyen Quang, Lai Chau, Thanh Hoa, and Phu Tho) in Vietnam (Frost 2021).

Discussion

Live individuals of Leptobrachella tamdil were found in the secondary forests, ca. 30km south of Chandel Town. Chandel District is surrounded by tropical semi-evergreen and moist deciduous/secondary forest, subjugated by Schima wallichii, Albizzia sp. and Macaranga denticulata. The forest in the moist valleys is lofty, while steep slopes are covered with canopy (Singh et al. 2000; Forest Survey of India 2019). Chakpi’s slow-flowing streams where sampling was carried out, is surrounded by the subtropical semi-evergreen and the sub-tropical hill forests, predominantly subjugated by Juglans sp., Albizzia chinensis, Quercus sp., Macaranga denticulata, and Schima wallichi based on the classification of Champion & Seth (1968). Specimens were collected from beneath weathered sedimentary rocks and on the exposed sand stones in the vicinity close to slow-flowing stream. This is quite similar to the previous collection site of the species from Dampa Tiger Reserve, Mizoram State by Vanlalsiammawii et al. (2020). During the collection period, atmospheric temperature and relative humidity were 12.9°C and 83.6 %, respectively. Chakpi offshoots offer a unique ecosystem and congenial breeding grounds for many rare amphibian species especially near stagnant and flowing water. In Chakpi, streams were bounded by sedimentary rocks and weathered huge boulders and logs which provide suitable breeding spot for several anuran species. Sympatric frog species includes Amolops cf. indoburmanensis and Sylvirana cf. lacrima that were observed at the upper reaches of the elevated stream bed. The present study found a gravid female (MZMU 2226) with 105 eggs. We suggest that the breeding season is likely to start during dry season (December to January) as hinted by the presence of gravid females and deposition of eggs. The egg diameter of L. tamdil range between 1.4–1.5 mm (N= 10). The conservation status for the species remains unclear. Deuti (2013) categorized this species as data deficient (DD), but later Dinesh et al. (2020) corrected that to not assessed (NA). Thus, the proper assessment of its conservation status is lacking. The microhabitat of L. tamdil consisted primarily of intermediate-flowing stream within tropical semi-evergreen forest (Sengupta et al. 2010; Vanlalsiammawii et al. 2020). Other aspects of L. tamdil such as the breeding biology, tadpole morphology, diet, and general life history remain largely unknown and considerable works are needed to shed more light on this species. Legitimately, the present record of L. tamdil from northeastern part of India represents the northeastern-most locality with the highest altitude (1,220–1,228 m), against the records in Mizoram at 745 m (Sengupta et al. 2010) and 449 m (Vanlalsiammawii et al. 2020). This study provides a range extension of L. tamdil away from the type locality in Mizoram, north-east towards Manipur, and it is likely present in the adjacent country of Myanmar and possibly in Assam, Nagaland, and Tripura states. The new individuals represent the latest range of SVL (27.8–33.2 mm), and the breeding season might be commencing from late winter as indicated by the presence of gravid female. Further observations are necessary to know more information about the biology of L. tamdil.

The loss of forest canopy and natural streams were noted to directly threaten the habitats of the anuran species. Jhum cultivation, forestry effluents, and forest fires are also attributed to it (see Gupta 2000; Shimray 2004; Maithani 2005; Bhattacharya & Nanda 2005; Kerkhoff et al. 2006; Sastry et al. 2007; Jamir & Lianchawii 2013; Reimeingam 2017). The first step towards ensuring the long-term persistence of such anurans is addressing the lack of understanding of range, population trends, ecology, and potential threats. Mitigation measures must be put in place to stop the unchecked depletion of the resources of such little-known species, failing which L. tamdil and other such taxa will regrettably be wiped out from Manipur, to say the least (Banita & Bordoloi 2007). Overall, amphibian studies in the northeastern India is the least when compared to rest of the regions of the country and especially amphibian faunal inventorying is scanty in Manipur State. Safeguarding the ecological diversity of the existing areas is most likely to protect viable populations of such fragile wildlife. Surroundings of the Chandel Village include some intact habitats that are suitable for anurans where probable discovery of unique amphibians are reasonably high. Thus, extensive explorations can ascertain the true amphibian richness in the present study area.

Table 1. Detailed morphological (in mm) and eggs data of Leptobrachella tamdil from Chandel District, Manipur, India.

Voucher number	MZMU2224	MZMU2225	MZMU2226	Vanlalsiammawii et al. (2020)	Sengupta et al. (2010)
				MZMU 1631	ZSI A10962 (Holotype)	ZSI A10963 (Paratype)
Sex	Male	Male	Female	Male	Male	Female
Locality	Chandel, Manipur			Dampa Tiger Reserve, Mizoram	Tamdil National Wetland, Mizoram
SVL	28.7	27.8	33.2	31.3	32.3	31.8
IN	2.7	2.7	2.9	3.2	3.2	3.1
HL	9.8	9.9	11.4	9.2	8.7	8.8
HW	9.6	9.2	11	10.5	12.0	12.0
HD	4.2	4	4.3	4.4	5.2	4.8
ED	4	4.2	4.8	4.3	4.5	4.6
IO	3.9	3.8	4	4.8	5.1	5.8
E-S	3.5	3.9	4.4	4.6	4.7	4.7
E-N	2.1	1.7	2.2	2.5	2.8	2.7
UE	3	3.2	3.8	3.1	3.4	3.5
TL	12.6	12.7	15	14.2	16.0	15.7
IMT	1.8	1.5	1.8	1.8	1.9	1.8
IPT	1.8	1.5	2	2.1	2.2	1.8
A-G	14	13.6	16.3	13.7	13.8	13.8
BW	9.9	8.3	10.5	9.8	9.7	11.9
No. of eggs			n= 105
Diameter of eggs			1.4–1.5

Table 2. Genetic distance among Leptobrachella species using 16S rRNA partial gene sequence. Only the species showing low genetic distances with L. tamdil are provided in the table.

	Species	K2P distance
		1	2	3	4	5	6	7	8	9	10	11	12	13	14	15	16	17	18	19	20
1	L. tamdil MW665131.1
2	L. tamdil MW665132.1	0.00
3	L. tamdil MW665130.1	0.00	0.00
4	L. laui MH406903.1	0.09	0.09	0.09
5	L. liui MH923370.1	0.09	0.09	0.09	0.04
6	L. puhoatensis KY849587.1	0.09	0.09	0.09	0.07	0.09
7	L. wulingensis MT530316.1	0.10	0.10	0.10	0.08	0.06	0.08
8	L. petrops MH055903.1	0.09	0.09	0.09	0.07	0.09	0.00	0.08
9	L. bourreti KR018124.1	0.10	0.10	0.10	0.09	0.07	0.09	0.02	0.09
10	L. minimus JN848369.1	0.11	0.11	0.11	0.07	0.08	0.09	0.08	0.09	0.09
11	L. mangshanensis MH277365.1	0.10	0.10	0.10	0.05	0.02	0.09	0.08	0.09	0.08	0.08
12	L. dorsospina MW046194.1	0.10	0.10	0.10	0.09	0.07	0.09	0.03	0.09	0.03	0.09	0.08
13	L. nyx MH055818.1	0.10	0.10	0.10	0.08	0.07	0.09	0.07	0.09	0.08	0.06	0.07	0.08
14	L. pluvialis MT644610.1	0.10	0.10	0.10	0.07	0.07	0.09	0.08	0.09	0.08	0.05	0.07	0.09	0.04
15	L. purpuraventra MK414531.1	0.11	0.11	0.11	0.10	0.07	0.09	0.04	0.09	0.03	0.10	0.08	0.03	0.08	0.08
16	L. suiyangensis MK829650.1	0.12	0.12	0.12	0.10	0.09	0.10	0.05	0.10	0.04	0.11	0.10	0.04	0.10	0.10	0.04
17	L. alpinus MH406905.1	0.12	0.12	0.12	0.10	0.09	0.11	0.05	0.11	0.05	0.11	0.09	0.05	0.10	0.10	0.05	0.06
18	L. shangsiensis MK095461.1	0.12	0.12	0.12	0.08	0.08	0.10	0.09	0.10	0.10	0.06	0.09	0.09	0.05	0.05	0.09	0.11	0.11
19	L. aspera MW046202.1	0.12	0.12	0.12	0.10	0.10	0.10	0.08	0.10	0.09	0.08	0.10	0.10	0.06	0.06	0.10	0.11	0.11	0.06
20	L. bijie MK414539.1	0.12	0.12	0.12	0.09	0.08	0.10	0.05	0.10	0.05	0.10	0.09	0.04	0.10	0.10	0.03	0.04	0.06	0.10	0.11

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