The herpetofauna of Jigme Singye Wangchuck National Park in central Bhutan : status , distribution and new records

A checklist of herpetofauna in Jigme Singye Wangchuck National Park in central Bhutan based on field surveys and photographic records is presented. Twelve families, 30 genera, and 42 species of herpetofauna were recorded; 33 species from 24 genera and eight families were reptiles and nine species belonging to six genera and four families were amphibians. Two ophidians, Bungarus caerulus and B. lividus, and one anuran, Amolops formosus, are new records for Bhutan. The compiled record also includes three threatened species. We recommend enhanced monitoring and herpetofauna-oriented conservation and research for Jigme Singye Wangchuck National Park.


INTRODUCTION
Humans frequently depend on diverse sources for essentials such as food, refuge, medicine, combustibles, and industrial products (Dirzo & Raven 2003).Amphibians and reptiles are an essential component of the earth's biodiversity (Urbina-Cardona 2008) and play a key role in most ecosystems, both terrestrial and aquatic, as prey and predators (Schneider et al. 2001).Herpetofauna are excellent ecological indicators owing to their high sensitivity to environmental change (Roy 2002), and are also among the most threatened taxa (Böhm et al. 2013) with more than 30% of amphibians and 19% of reptile species listed under threatened categories in the IUCN Red List (Stuart 2004;Böhm et al. 2013).While many taxa are still data deficient, known amphibian and reptile species are reported to be declining on a global scale due to factors such as deforestation, draining of wetlands, and pollution from agricultural runoff (Alford & Richards 1999;Gibbon et al. 2000;Kiesecker et al. 2001;Becker et al. 2007).
Bhutan's biodiversity database is strong for vertebrates like mammals and birds, but herpetofauna is less well studied (Wangyal 2013).A recent review by Wangyal (2014) recorded 183 species of reptiles and amphibians; 84 species of snakes, 23 species of lizards, 20 species of tortoises and turtles, and 56 species of frogs.Currently, none of these are listed under Schedule I of the Forests and Nature Conservation Act (FNCA) 1995 (RGoB 1995), and without any specific conservation plan, these diverse species are likely to face considerable threats from habitat destruction and degradation (Wangyal 2014).Most existing records are based on opportunistic encounters by enthusiasts (Wangyal 2012), and for protected areas the limited reports describe the herpetofauna of Royal Manas National Park (RMNP) (Das et al. 2016), the diversity and distribution of snakes in Jigme Dorji National Park (JDNP) (Koirala et al. 2016), and snakes and lizards from Bumdeling Wildlife Sanctuary (BWS) (Wangyal & Tenzin 2009).Two decades after its gazettement in 1995 (JSWNP 2014), Jigme Singye Wangchuck National Park (JSWNP) still does not have a checklist of its herpetofauna.In this paper, we provide the first checklist of reptiles and amphibians from the biologically diverse JSWNP, thereby filling the information gap and establishing baseline information for future conservation measures.

Study Area
The study was conducted in JSWNP, located in the central part of Bhutan (27.022-27.488 0N & 90.069-90.693 0E; Figs. 1 & 2).With an area of 1,730km 2 , JSWNP is the third largest protected area in Bhutan, spread across 10 'gewogs' (sub-district administrative blocks) in five districts (JSWNP 2014).For effective conservation and sustainable management of resources, the park is divided into four park ranges: Langthel park range, Nabji park range, Taksha park range, and Tingtibi park range.JSWNP connects with JDNP and Wangchuck Centennial National Park (WCNP) in the north and with RMNP and Phibsoo Wildlife Sanctuary (PWS) in the south through biological corridors.Thus, JSWNP forms a vital link between the northern and southern protected areas network of Bhutan.JSWNP has a diverse habitat representation from subtropical forests at 464m to alpine scrubs with the centrally located Black Moutain (Jowo Durshing) going up as high as 4925m.This wide altitudinal variation has bestowed the park with six major forest types: (i) subtropical forests, (ii) chirpine forests, (iii) warm temperate broadleaf forest, (iv) cool temperate broadleaf forests, (v) subalpine conifer forests, and (vi) alpine meadows (JSWNP 2014).The national park has a good biodiversity database (Letro 2015) with a recording of 39 mammal species including the endangered tiger and Red Panda, 218 birds including the critically endangered White-bellied Heron, and 139 butterflies.These diverse ecological habitats, together with well-drained catchments and wetlands, prominent geophysical features, and agricultural farmlands, provide varied habitats for diverse herpetofauna.

Methods
The survey was conducted in all park range jurisdictions from May 2016 to June 2017.Searches were intensified in spring and summer months when reptiles and amphibians are most active.Data for reptiles were collected by randomly walking along opportunistic footpaths and trails between 9:00am and 3.30pm employing visual encounter surveys (Campbell & Christman 1982).For amphibians, the potential wetland habitats like marshes, ponds, streams, and riversides (Becker et al. 2007) were scanned by employing visual encounter searches between 7:00pm and 8:00pm.These areas were searched for all morphological stages of herpetofauna.Additional survey techniques to optimize detection success included night spot-light search, aural identification of species calls, recording road kills, and species killed by villagers.No voucher samples were collected during the survey, but all the species encountered were identified either in the field or were photographed for identification and released back to their natural habitat.For every individual encountered, details such as species name, number of individuals, sex, and habitat inhabited were recorded along with the GPS coordinates.Garmin eTrex 30 was used to record geographic coordinates of the sites.The field guides on reptiles and amphibians by authors Purkayastha (2013) , Ahmed et al. (2009), and Daniel (2002) were referred for species identification in the field.

RESULTS
A total of 42 species were recorded from the national park, belonging to 30 genera and 12 families.Of these, 32 species belonging to 24 genera and eight families were reptiles and nine species from six genera and four families were amphibians.

Snakes
We observed 24 species of snakes from 18 genera belonging to four families (Table 1; Images 1-23).The family Colubridae was the most diverse with 16 species belonging to 12 genera, whereas Pythonidae appeared to be the least diverse with only one species.In terms of relative abundance based on individuals sighted, Colubridae was the most abundant, accounting for 75% (n=56) of all snakes, followed by Elapidae with 18%.Individual counts were least for Pythonidae and Viperidae, at 3% each (Fig. 3).Among species, the Green Rat Snake Ptyas nigromarginata has the highest observation record with 10 sightings.Two ophidians, Bungarus caerulus and Bungarus lividus, are new records for Bhutan, and Python bivittatus was recorded at an elevation of 1350m, a new highest elevation record for the species.

Lizards
We recorded eight species of lizards belonging to three families (Table 2; Images 24-31).The family Scincidae was the most diverse with three species and two genera.In the families Gekkonidae and Agamidae, we recorded two species each.Based on the individual numbers, the family Scincidae was the most abundant accounting for

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52% (n=59) of the total individual lizards sighted, followed by Agamidae with 32% and Gekkonidae with 15% (Fig. 2).Himalayan Litter Skink Sphenomorphus indicus and Common Garden Lizard Calotes versicolor were the most sighted species with 23 and 15 sightings, respectively.We also recorded a lone turtle species, Cuora mouhotii belonging to Geometridae family (Image 32), which is listed as endangered in IUCN Red List of Threatened  Species.

Anurans
We recorded a total of nine frog species belonging to six genera and four families (Table 3; Images 33-40).Of these, Rhacophoridae was the most diverse with three species, followed by Bufonidae, Dicroglossidae, and Ranidae with two species each.Maximum count of individuals was recorded for the family Dicroglosidae accounting for 60% (n=336), followed by Rhacophoridae with 18%, Bufonidae with 14%, and least for family Ranidae with only 7% (Fig. 3).One species of anuran, Amolops formosus, is a new record for Bhutan.

DISCUSSION
Our results show JSWNP as a rich repository of reptiles and amphibians.With 42 species recorded, this diversity in JSWNP accounts for 23% (n=183) of the total species recorded from Bhutan.This can be attributed to the great elevation gradient and various habitat types of the park.The species were observed in diverse habitats such as along footpaths and agricultural fields, by streams and rivers, near villages, and in various forests types, indicating that holistic habitat management is vital for the conservation of herpetofauna.
Of the 42 species of herpetofauna recorded in JSWNP, at least three species are new records for Bhutan, namely Bungarus caeruleus, Bungarus lividus, and the anuran Amolops formosus.Bungarus caeruleus, which was earlier listed as an expected species in the country (Wangyal 2014), is now in the confirmed list with our first record from Tingtibi Park Range.Bungarus lividus was recorded during our survey at Adha under Taksha Range in May 2016, and later also observed in Langthel Range in 2017.Bungarus lividus differs from all other kraits like Bungarus niger and Bungarus caeruleus in having normalsized or only slightly enlarged mid-dorsal scales (arrows mark scales of the mid-dorsal row) (Kuch et al. 2011).Amolops formosus was also listed by Wangyal (2014) as an expected species, which we have recorded for the first time from Peka Chhu at an elevation of 1,350m, in the Taksha Park Range.
Two species of snakes and the lone turtle species are also found to be in the threatened category of the IUCN Red List of Threatened Species.The Burmese Python Python bivittatus, categorized as Vulnerable was reported from the tropical regions of India, Bangladesh, Nepal, China, and southeast China (Stuart et al. 2012).In Bhutan, it was first reported by Ahmed, Das & Dutta (2009) from an unspecified location but later its presence was reconfirmed when it was observed at Gortey and Kanamakura (245m) in Royal Manas National Park (Wangyal 2012), which has tropical climatic conditions.Unexpectedly, we recorded this threatened giant reptile at an altitude of 1,350m at Adha under Taksha Range during the recent survey, thus setting a new elevation record.The highest elevation at which the species was recorded was 1200m by Orlov, Murphy & Papenfuss (2000) in a bamboo forest of the Tam-Dao Mountain Range of Vietnam.Other higher records were without proper validation (Cota 2010).The King Cobra Ophiophagus hannah is another threatened snake species recorded in JSWNP.Listed as Vulnerable in the IUCN Red List, it is widely distributed in southern Asia (Stuart et al. 2012) with few sightings from Bhutan.Its presence was reported from Royal Manas National Park, Sarpang Dzongkhag, and Tashi Yangtse Dzongkhag (Wangyal & Tenzin 2009).In JSWNP, we observed one individual (SVL 120cm, TL 20cm) by the side of Berti Chhu in the Tingtibi Park Range, adding a new distribution record for the species in Bhutan.The Keeled Box Turtle Cuora mouhotii is the lone turtle species that we recorded in JSWNP and it too falls under the threatened category of the IUCN Red List.Found in freshwater and terrestrial habitats, the Keeled Box Turtle is native to China, India, Lao People's Democratic Republic, Myanmar, and Vietnam, and is listed as Endangered in the IUCN Red List of Threatened Species (Asian Turtle Trade Working Group 2000).In Bhutan, its presence was first reported by Wangyal et al. (2012) at an elevation of 370m in Zhemgang District.Some species could not be identified while some were identified at the genus level, and these will be added to the checklist after proper identification.While the national park has many intact habitats, the coming up of numerous developmental activities like hydropower construction, road construction, installation of high tension electric lines, and the use of fertilizers and pesticides by the park residents are likely to threaten the habitats of herpetofauna.Cross-sectoral consultation is necessary to safeguard prime habitats of herpetofauna and further studies with sample collection are vital to confirm the species that could not be identified from the photographs and field notes.The areas that were not covered during the present study should be explored as well.Besides that, it is also vital to educate the communities within the park regarding the implications of herpetofauna conservation, so that members of herpetofauna do not fall victim to killing by humans out of fear.

Figure 3 .
Figure 3.The diversity and abundance of herpetofauna in JSWNP