Inventory of butterfly fauna ( Lepidoptera : Rhopalocera ) of Tripura , India , in the Indo-Myanmar biogeographical zone , with records of threatened taxa

The Tripura province of northeast India, situated in the western fringe of the Indo-Myanmar biodiversity hotspot was extensively explored for butterfly fauna. We surveyed 28 wild and managed locations in the hot and humid environment of Tripura province (2009–2012) across different landscape gradients to observe and record butterfly diversity. We report here 212 butterfly species, 65 of which are considered threatened including 41 species protected by Indian Wildlife Protection Act 1972. Thirty-eight species are categorized as threatened by IUCN including one species also by CITES. We recorded the abundance of each butterfly species to highlight the population status of individual butterfly species in order to reveal the status of their conservation in Tripura, in India, and also at global scale. Geographic distribution of 142 species is extended to Tripura. Results of this study form a baseline data on the diversity and conservation of butterflies in this biodiversity hotspot.


INTRODUCTION
Insects constitute more than half of the world's known biodiversity (May 1992), perform multidirectional activities, viz., pollination, energy transformation, seed dispersal, and contribute to the productivity and stability of ecosystem (Naeem et al. 1994;Tilman et al. 1996).This is particularly true for tropical regions where insects show high abundance and species diversity (Samways 2005;Spector 2006).Among insects, butterflies are a taxonomically well studied group throughout the world (Ghazoul 2002) and are indicator taxa in terms of habitat quality and anthropogenic disturbance (Kocher and Williams 2000).More than 18,000 butterfly species have been documented worldwide (Heppner 1998;Larsen et al. 2011;Martinez et al. 2003) including 1501 species reported from India (Kehimkar 2008).Northeastern parts of India, consisting of eight provinces and having an area of 1,61,419 km 2 , shares about 65% of butterfly diversity of India (Haribal 1992;Gupta and Majumder 2006;Gupta and Maulik 2007;Gogoi 2012;Kunte et al. 2012).However, in geographical scale and in terms of species richness, the Tripura province (area: 10,491 km 2 ) had 72 species known (Agarwala et al. 2010;Majumder J. et al. 2012b;Roy Choudhury et al. 2011).This is far less in comparison to Sikkim, a smaller province having an area of 7,092 km 2 but with 695 species of butterflies known (Haribal 1992).
Tripura province of northeastern India is situated in the western fringe of Indo-Myanmar global hotspot (Mittermeier et al. 2005;Tordoff et al. 2012).It is rich in forests (ca.57.73% of the total land area) and is dominated by semi-evergreen to moist deciduous plants and secondary bamboo brakes (Majumdar K. et al. 2012a).The richness of biodiversity of the province is evident from occurrence of 1,583 plant species belonging to 862 genera in 193 families (Deb 1981(Deb -1983;;Majumdar K. et al. 2012b), 90 species of mammals (Gupta 1998), 17 species of amphibians, 35 species of reptiles (Majumder J. et al. 2012a) and 300 species of birds (Choudhury 2010;Bhattacharjee et al. 2013).Tripura province is unique due its location at the confluence of Indo-Myanmar, Indo-Malayan and parts of Indo-China geographical regions with close proximity to Bangladesh.The presence of mighty Brahmaputra River, originating in China and flows through Assam in the north and east of Tripura, acts as a barrier for gene flow from south-east Asian provinces, including Tripura (Datta-Roy et al. 2012).
To bridge the gap of information on the butterfly fauna, a sustained exploration was undertaken from June 2009 to December 2012 across different habitat gradients of the province.
Lodh and Agarwala | Checklist of butterflies in Tripura, India are observed: winter (late November to February), summer (March to May), monsoon (June to September) and autumn (October to mid November).Average annual temperature varies from the minimum average of 10°C in winter to the maximum average of 35°C in summer.During monsoon season, south-west monsoons bring maximum rainfall (65%) to the province.The average annual rainfall is 2,000-2,500 mm.The average humidity during the summer is 50-74%; during the monsoon season, it is above 85% (Keshari 2011).
The butterfly fauna at 28 locations in wild and managed habitats were inventoried.These were distributed in all the eight administrative districts of Tripura (Figure 2).Geo-coordinates and forest types are provided in Table 1 for each location (with their abbreviated names used in the systematic list of species recorded in this study).Among the 28 locations, 12 are located in South district and Gomati district, which have the maximum forest cover in the province (2,473 km 2 ) as well as three protected reserves, Trishna Wildlife Sanctuary (163.08 km 2 ), Rajbari National Park (31.63 km 2 ) and Gomati Wildlife Sanctuary (389.54 km 2 ).Another four locations are in Sepahijala district which includes Sepahijala Wildlife Sanctuary (18.53 km 2 ) and Clouded Leopard National Park.Four locations are in the North district that includes one protected reserve (Rowa Wildlife Sanctuary; 0.85 km 2 ).Among rest of the locations, three locations are distributed in West district, two locations in Khowai district, two locations in Dhalai district, and one location in Unakoti district (Figure 2).

Sampling Method
Two transect lines, each 1,000 m long × 10 m wide, using permanent markers (nylon rope tied to tree trunks at regular intervals along the transect) were laid at each of the 28 locations.These transects were visited twice in a year (once each in summer and winter) during the study period of three years: 2009-2010, 2010-2011, and 2011-2012.Transect lines were laid at sites that were rich in vegetation and showed a matrix of microhabitats.Transects were shifted every year within each location to give wider effect of exploration.As a result, six transects (two transects/year for three years) were laid at each location and these were visited 12 times during the study period.Thus, a total of 168 transects (28 locations × 6 transects) measuring 40.99 km 2 area (168 transects × 1000 m length × 10 m width) was covered for sampling following the Modified Pollard Walk Method (MPWM) (Pollard 1977).To maximize the encounter rate of butterflies, 10 minutes stops were made at every 100 m interval along transects and butterflies were observed within 10 m radius in all sides.Observations were done on sunny days between 06:00 h and 12:00 h local time on two consecutive days.
For each species, identifications were made and

MATERIAL AND METHODS Study area
In Southeast Asia, Tripura province of India lies between 22°56′ to 24°32′ N and 091°09′ to 092°20′ E, and represents the western fringe of Indo-Myanmar biogeographic zone of tropical Asia (Myers et al. 2000;Mittermeier et al. 2005).The province has an area of 10,490 km 2 , is largely forested along with its adjacent provinces of Mizoram, Manipur, Meghalaya and Assam in India, forms part of biodiversity hotspot, and is predominantly hilly with five hills ranges (elevations between 244-939 m above mean sea level) which run parallel from north to south.These ranges from west to east are: the Boromura-Deotamura, Atharamura, Longtharai, Shakhan, and Jampui hills.They decrease in elevation southwards and finally merge into the eastern plains.Four major valleys intersect these hill ranges: Dharmanagar-Kanchanpur, Kailasahar-Manu, Kamalpur-Ambasa and Khowai-Teliamura valleys (Figure 1).Tripura has secondary moist mixed deciduous forest in northern parts, and widely distributed moist deciduous teak forest in the south district and part of west district (Majumdar K. et al. 2012b).Four main seasons   numbers of individuals were counted.Photographs were taken when convenient, using high zoom Canon 50D and Lumix DMC FZ40 cameras.Butterfly species that could not be identified on flight were captured using butterfly net and released immediately after identification of sex and species, using field guides (Haribal 1992;Kunte 2000;Kehimkar 2008).At least one individual of every available species that were encountered were collected for taxonomic study with prior permission by the Department of Forests, Government of Tripura.All the specimens of this study were spread and preserved following the standard taxonomic procedure (Winston 1999).Butterflies are classified according to Ackery (1984), Campbell et al. (2000) and Savela (2013).Monomorphic butterfly species that were collected or photographed were not identified by sex; therefore, they are tagged as male or female (♂/♀).Sexually polymorphic species that were collected or photographed are tagged either as male (♂) or female (♀).All specimens and photographs used in the study were given voucher numbers and are maintained in the Ecology and Biodiversity Laboratory, Department of Zoology, Tripura University, India.
Based on accumulated data of the three years of study, abundance of each of the recorded butterfly species is considered into five categories: very common represented by >200 individuals, common represented Lodh and Agarwala | Checklist of butterflies in Tripura, India by <200 individuals but >100 individuals, occasional represented by <100 individuals but >50 individuals, rare represented by <50 individuals but >10 individuals, and very rare represented by < 10 individuals.Conservation status of butterfly species documented in this study are determined according to national and international conservation categories and compared with their abundance records for better understanding of threatened taxa across local and global habitats.

RESULTS
This communication is the first to present a systematic list of butterfly species from Tripura, India based on the current taxonomic classification of butterflies (Savela 2013).It documents butterfly species by recording their locations with GPS data, dates of collection, and number and sex of specimens examined or photographed, voucher numbers of collected specimens, and geographical distribution in India and elsewhere in the world (Kehimkar 2008).Species recorded include 142 species that are newly reported from Tripura (Agarwala et al.2010;Roy Choudhury et al. 2011;Majumder J et al. 2012b).Also included are 65 species enlisted under threatened categories by national law (Anonymous 1997(Anonymous , 2007) ) and by international conservation agencies (IUCN 2007;UNEP-WCMC 2011).Photographs of the species considered threatened are provided based on actual material examined .
In this study, we report 212 butterfly species which belonged to 128 genera in 24 subfamilies and six families (Table 2).The systematic list of butterfly species is organized by family, subfamily, and tribe with following information: i. Valid scientific name of the species with authority and English name; scientific name as originally proposed along with publication data to the original description; names of species within a tribe are presented in alphabetical order.ii.Specimen examined: Details of specimen(s) examined including the number of specimen(s) seen and their sex (male ♂; female ♀; male or female ♂/♀), collection location using abbreviations as used in  Specimen examined: 1 ♂/♀ (monomorphic), DB, 29. vii.2009, Pap.6.img.♂/♀,R. Lodh.
Conservation status: Tripura: rare; IUCN/CITES: not evaluated.Distribution: India (Himachal Pradesh in the west to Arunachal Pradesh in the east in Himalaya, South, central and eastern India, Tripura), Bangladesh, Bhutan, Myanmar, Nepal, Pakistan, Sri Lanka.
Distribution: India (South India, Uttaranchal in the west to Arunachal Pradesh in the east in Himalaya, Tripura), Bangladesh, Bhutan, China, Myanmar, Nepal, Sri Lanka.
Distribution: India (Northeast, South India up to Gujarat, Tripura, Uttaranchal in the west to Arunachal Pradesh in the east in Himalaya), Bangladesh, Myanmar, Sri Lanka.
Distribution: India (Northeast, Tripura, Uttaranchal in the west to Arunachal Pradesh in the east in Himalaya), Bangladesh, Bhutan, Myanmar, Nepal.Conservation status: Tripura: rare; IUCN/CITES: not evaluated.
Distribution: India (Himachal Pradesh in the west to Arunachal Pradesh in the east in Himalaya, Northeast, Tripura), Bangladesh, Bhutan, Myanmar, Nepal.Conservation status: Tripura: rare; IUCN: Near Threatened.

*Elymnias patna (Westwood, 1851); Blue-Striped Palm Fly
Melanitis patna Westwood, 1851, The genera of diurnal Lepidoptera, comprising their generic characters, a notice of their habitats and transformations, and a catalogue of the species of each genus (2): 405.TL: East India.
Distribution: India (Jharkhand, Madhya Pradesh, Northeast, Orissa, South India, Tripura, Uttaranchal in the west to Arunachal Pradesh in the east in Himalaya, West Bengal), Bhutan, Myanmar, Nepal.
Distribution: India (Himachal Pradesh in the west to Arunachal Pradesh in the east in Himalaya, Madhya Pradesh, Maharashtra, Northeast, South India, Tripura, West Bengal), Bangladesh, Bhutan, China, Myanmar, Nepal, Sri Lanka.
Distribution: India (Northeast, Tripura, Uttaranchal in the west to Arunachal Pradesh in the east in Himalaya, Western Ghats), Bhutan, Myanmar, Nepal.
Distribution: India (Madhya Pradesh, Northeast, Sikkim to Arunachal Pradesh in the east in Himalaya, South India up to Goa, Tripura), Bangladesh, Indonesia, Myanmar, Sri Lanka.Conservation status: Tripura: very common; IUCN/ CITES: not evaluated.
Distribution: India (Sikkim to Arunachal Pradesh in the east in Himalaya, Tripura), Bangladesh, Bhutan, China, Myanmar, Nepal.
Tribe Spalgini 121.Spalgis epius (Westwood, 1852); Ape Fly Lucia epius Westwood, 1852, The genera of diurnal Lepidoptera, comprising their generic characters, a notice of their habitats and transformations, and a catalogue of the species of each genus (2): 502.TL: North India.
Distribution: India (common in almost all states of India, Tripura), Bhutan, Myanmar, Nepal, Pakistan, Sri Lanka.
Distribution: India (Northeast, Orissa, Sikkim in the west to Arunachal Pradesh in the east in Himalaya, Tripura), Bangladesh, Bhutan, Indonesia, Myanmar, Nepal.Conservation status: Tripura: very rare; IUCN/CITES: not evaluated.
Distribution: India (peninsular India up to Gujarat and Madhya Pradesh, Tripura, Uttaranchal in the west to Arunachal Pradesh in the east in Himalaya, West Bengal), Bangladesh, Bhutan, Myanmar, Nepal, Sri Lanka.
Distribution: India (common in almost all states of India, Tripura), Bangladesh, Myanmar, Pakistan, Sri Lanka.

DISCUSSION
The butterfly fauna reported here is found to be rich and an important asset for conservation in this part of Southeast Asia.Altogether, 65 butterfly species (30.66% of the recorded species) are found to be threatened, including 41 species protected by law in India under Schedules I (9 species), II (27 species) and IV (5 species) of IWPA 1972 (Anonymous 1997).Another 38 species are categorized as critically endangered (CR), endangered (EN), vulnerable (VU), or near threatened (NT) according to IUCN Red Lists either at the global scale or at regional scale (IUCN 2007;Anonymous 2007).One species, Troides helena (Linnaeus, 1758), is protected under Appendix II G of CITES (UNEP-WCMC 2011).Fifteen species are threatened in India as well as at global scale.Interestingly, six species -T.helena, protected by CITES, Castalius rosimon (Fabricius, 1775) and Papilio memnon Linnaeus, 1758, protected by IWPA 1972 (schedule I), Papilio nephelus Boisduval 1836 and Tanaecia lepidea protected by IWPA 1972 (schedule II), and Udaspes folus (Cramer 1775), protected by IUCN -are found to be abundant in Tripura.These species receive the highest level of protection in other parts of the world.According to species' abundance data recorded in this study, 141 species are found to be rare or very rare in Tripura province including 56 species which are protected by the IWPA (1972) and the IUCN.However, the rest of the 85 species are considered to be of either least concern (LC) or not evaluated for their conservation status according to IUCN.Conservation efforts for these 85 speies are required in view of increasing threats of anthropogenic disturbances that are faced by this biogeographic zone in general and Tripura province in particular.Two sampling sites, Debbari (DB) and Ballianchip (BC), were found to be the most species rich locations each of which supported 112 and 94 species, respectively, and together shared 132 species representing 62.26% of the recorded butterfly fauna of Tripura.Each of the two locations contained 7 and 6 species, respectively, as unique with regard to their exclusive distribution in these locations in Tripura.Eight of the 65 species recorded in threatened categories from Tripura were collected from these locations.
Thus, Tripura province not only possesses rich butterfly diversity but it also supports a large number of rare and legally protected species and is, therefore, an important destination of study of butterflies and other wildlife in the tropics of Southeast Asia.

Figure 1 .Figure 2 .
Figure 1.Line drawning of Southeast Asia and google earth image, captured on 3 May 2013, showing location of the study area, Tripura province and its adjoining provinces (Mizoram, Meghalaya, Assam) in India and adjacent countries (Bangladesh, Myanmar), in the western fringe of Indo-Myanmar hotspot region.
87. *Mycalesis suaveolensWood-Mason & de Nicéville, 1883; Wood-Mason's Bush Brown Mycalesis suaveolens Wood-Mason and de Nicéville, 1883, The Butterflies of India, Burmah and Ceylon, a descriptive Handbook of all the known Species of rhopalocerous Lepidoptera inhabiting that Region, with Notices of allied Species occurring in the neighbouring Countries along the Border, with numerous Illustrations 1(2): 125.TL: Cachar, India.

Table 1 .
Geo -coordinates, elevation and forest types of locations in different districts surveyed for butterflies in Tripura province, India.
Mycalesis anaxias Hewitson, 1862, Illustrations of new species of exotic butterflies selected chiefly from the collections of W. Wilson Saunders and William C. Hewitson 4: 54.TL: Karnataka, South India.