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Introduction
The Bengal slow loris Nycticebus bengalensis is the only strepsirrhine primate in north-east India. It is categorized as Vulnerable on the IUCN Red List (Streicher et al., Reference Streicher, Singh, Timmins and Brockelman2008). Although five species of slow loris (Bengal slow loris Nycticebus bengalensis, greater slow loris Nycticebus coucang, Javan slow loris Nycticebus javanicus, Bornean slow loris Nycticebus menagensis and pygmy slow loris Nycticebus pygmaeus) are considered threatened (Roos, Reference Roos2003), few field data are available to confirm their conservation status. Several surveys of the Bengal slow loris in north-east India have found this nocturnal primate to be rare or absent despite a well-developed protected area network in north-east India (Radhakrishna et al., Reference Radhakrishna, Goswami and Sinha2006). However, nocturnal surveys have been restricted by the presence of armed insurgents and poachers, the presence of species such as elephants Elephas maximus and wild buffalo Bubalus bubalis, and local beliefs about entering the forest at night (Radhakrishna et al., Reference Radhakrishna, Goswami and Sinha2006).
Throughout Asia slow lorises are in demand for use in traditional medicine and as pets (Nekaris & Nijman, Reference Nekaris and Nijman2007). The range of the Bengal slow loris extends from Vietnam to China but in India it is confined to seven north-eastern states (Srivastava & Mohnot, Reference Srivastava and Mohnot2001; Brandon-Jones et al., Reference Brandon-Jones, Eudey, Geissmann, Groves, Melnick and Morales2004). The species is threatened by habitat destruction, hunting (Choudhury, Reference Choudhury1992) and the wildlife trade (Radhakrishna et al., Reference Radhakrishna, Goswami and Sinha2006) despite being listed in Schedule I of India's 1972 Wildlife Protection Act. The limited information on its status and ecology is the main hindrance to developing a conservation strategy for this species in India. We investigated the status and distribution of the Bengal slow loris, and the threats facing it in protected areas of Assam and Arunachal Pradesh, in north-east India.
Study area
We conducted a survey of Bengal slow loris in 16 protected areas in north-east India: three National Parks, 10 Wildlife Sanctuaries and two Reserve Forests in Assam and one National Park in Arunachal Pradesh (Fig. 1). This region is characterized by diverse biota and a high level of endemism as it falls on the confluence of the Indo-Malayan and Palearctic biogeographical realms. The region's lowland and moist to wet tropical evergreen forests are the northernmost limit of tropical rainforests (Proctor et al., Reference Proctor, Haridasan and Smith1998). The surveyed areas are characterized mainly by evergreen, semi-evergreen and deciduous forest as a result of their location in the subtropical zone and the prevalence of a monsoonal climate (Champion & Seth, Reference Champion and Seth1968).
Locations of the 16 sites where we surveyed for the Bengal slow loris Nycticebus bengalensis in Assam and Arunachal Pradesh, north-east India. The rectangle on the inset shows the location of the main map in India. (NP, National Park; WLS, Wildlife Sanctuary; RF, Reserve Forest).
Methods
We conducted our survey during February 2009–May 2010. We estimated encounter rates by reconnaissance sampling (Walsh & White, Reference Walsh and White1999), using pre-cut paths to maximize access to forested areas over a short period of time (Burnham et al., Reference Burnham, Anderson and Laake1980; Hedges & Lawson, Reference Hedges and Lawson2006). We carried out night-time surveys (18.00–22.00 and 22.00–03.00) on foot and, in three instances, by vehicle (where walking at night was prohibited). Each night we selected two transects a minimum of 1 km apart to avoid counting the same individual more than once, as lorises generally move at < 1 km per hour (White & Edwards, Reference White, Edwards, White and Edwards2000; Nekaris, Reference Nekaris2003). Transects were 2 km in length and marked with flagging tape every 50 m. Three to four surveyors walked each transect once, slowly (1 km h−1), observing both sides of the transect (Nekaris & Jayewardene, Reference Nekaris and Jayewardene2004). We searched all types of vegetation at all heights, using a headlamp to detect the loris's characteristic orange eye-shine.
We used a red filter to observe and confirm the animal, to minimize disturbance (Nekaris, Reference Nekaris2003). To facilitate comparisons with other nocturnal primate studies (Singh et al., Reference Singh, Anand Kumar, Kumara and Mohnot2000; Nekaris et al., Reference Nekaris, Blackham and Nijman2008) we used the number of sightings per km as an indicator of relative abundance (Sutherland, Reference Sutherland and Sutherland2002).
On encountering a loris we recorded its distance from the start of the transect, its perpendicular distance from the transect, the number of individuals, the distance between the animal and the observer, the angle between the animal and the transect line, latitude and longitude, time of detection, the behaviour of the animal when detected (active behaviour: feeding, moving, grooming; inactive behaviour: sleeping, resting, sitting), its height from the ground, the tree species in which it was detected, and the vegetation type. For analysis of loris behaviour we divided observations into three: early night (18.00–21.00), mid night (21.00–24.00) and late night (24.00–03.00). We carried out both full and partial night surveys, where a full night is defined as a session from 18.00–03.00 hours and a partial night is defined as a session of > 4 hours but less than a whole night, suspended because of heavy rain, elephant attack or fog. We gathered information on habitat and the disturbance caused by poaching, illegal logging, and habitat destruction through extraction of non-timber forest products and crop cultivation, by walking the transects during the day and recording the presence or absence of each of these factors.
We assessed the overall level of threat at each site, on an arbitrary scale of 0–very high. We also asked local forest officials, forest guards and local experts, using open questions, if they had encountered lorises.
Results
During 99 full survey nights and 28 partial survey nights we covered 370 km of transects within protected areas and reserve forest in Assam and Arunachal Pradesh. We encountered 25 lone Bengal slow lorises, at 10 survey sites. The mean overall encounter rate was in the range 0.06–0.2 km−1. The highest encounter rate (0.2 km−1) was in Namdapha National Park, in Arunachal Pradesh, followed by Gibbon Wildlife Sanctuary (0.18 km−1) and Bherjan Borajan Podumani Wildlife Sanctuary (0.17 km−1) in Assam (Table 1). In Namdapha National Park we encountered three slow lorises during 5 full survey nights covering 15 km of transects.
Data from surveys of Bengal slow loris Nycticebus bengalensis in protected areas of Assam and Arunachal Pradesh (Fig. 1), with survey sites, number of night surveys, total distance covered, number of sightings, number of sightings per km, and any additional information.
1 NP, National Park; WLS, Wildlife Sanctuary; RF, Reserve Forest
2 All of single loris
3 Evaluated on arbitrary scale: +, Low; ++, Medium; +++, High; ++++, Very high
In Assam we encountered Bengal slow lorises at nine of 15 survey sites (Table 1). No lorises were seen on the transect line. The mean distance of observed lorises from the transect was 15.04 m (range 3–27 m) and the lorises encountered closest to the transect (3 and 4 m) were in bushes and bamboo thickets.
Lorises were seen at a mean height above ground of 12.36 m (range 3–17 m). Poor visibility made it difficult to identify sex and age. The time of night did not have any influence on loris activity, with inactive and active behaviours as likely to occur during any of the three periods (χ 2 = 1.30, df = 2, P > 0.05). There was a slightly increasing trend in the number of loris sightings from early to late night (χ 2 = 1.04, df = 2, P > 0.05). Lorises commonly fed and travelled in trees of the families Combretaceae and Magnoliaceae, with trees of the genus Terminalia being most commonly used (Supplementary Table S1).
Other mammals we encountered during our night surveys included the red giant flying squirrel Petaurista petaurista, the small Indian civet Viverricula indica, the large Indian civet Viverra zibetha, the Asian palm civet Paradoxurus hermaphroditus, the Asian elephant Elephas maximus, the leopard Panthera pardus, the leopard cat Prionailurus bengalensis, the jungle cat Felis chaus, the wild pig Sus scrofa, the Indian hare Lepus nigricollis and the Bengal fox Vulpes bengalensis.
Habitat destruction through anthropogenic activities was a potential threat to the Bengal slow loris and other species at the study sites (Table 1). There was evidence of deforestation at all sites. Local people log for both domestic (housing and furniture) and commercial purposes. Hunting is another threat to the loris: its body parts are used in traditional medicine and local people believe that loris meat can increase male power and act as an aphrodisiac.
Discussion
We present findings about the Bengal slow loris in the westernmost part of its distribution range, confirming its presence in Chirrang Reserve Forest (part of Manas Biosphere Reserve), in Assam. We also confirmed the presence of the Bengal slow loris in protected areas in Assam, including Nameri National Park and Barnadi Wildlife Sanctuary, although mean encounter rates were low. Higher encounter rates (0.20 km−1) in Namdapha National Park and Gibbon Wildlife Sanctuary suggest that these areas may hold substantial populations of lorises and should be targeted as key sites for conservation.
Our findings can be compared with recorded encounter rates for the Bengal slow loris elsewhere in India and South-east Asia (Table 2). Radhakrishna et al. (Reference Radhakrishna, Goswami and Sinha2006, Reference Radhakrishna, Datta-Roy, Swapna and Sinha2010) found 0.03–0.33 lorises per km in parts of Assam and Meghalaya, with a mean of 0.17. Radhakrishna et al. (Reference Radhakrishna, Goswami and Sinha2006) found slow lorises at only four of 27 sites surveyed in Assam, with similar results from a later study in Meghalaya (Radhakrishna et al., Reference Radhakrishna, Datta-Roy, Swapna and Sinha2010), where they found lorises at two of 16 sites, whereas we detected slow lorises at 10 of our 16 survey sites. The higher encounter rate in our study may be attributable to the methods employed. The number of surveyors has a significant effect on the detectability of this shy animal (Nekaris et al., Reference Nekaris, Blackham and Nijman2008), with smaller teams recommended. Duckworth (Reference Duckworth1998) highlighted the inherent difficulties of assessing abundance at night and the importance of detecting animals by their eye shine. We used red lights rather than large search lights as per the previous survey by Radhakrishna et al. (Reference Radhakrishna, Goswami and Sinha2006). Lorises do not shy away from red lights (Charles-Dominique & Bearder, Reference Charles-Dominique, Bearder, Doyle and Martin1979), nor do many other nocturnal mammals (Supplementary Table S2).
Encounter rates for the Bengal slow loris in north-east India and South-east Asia, based on nocturnal field surveys, excluding surveys where lorises were not encountered.
We sought slow lorises from dusk until 03.00, after which time animals often dispersed to sleep. Earlier studies (Charles-Dominique & Bearder, Reference Charles-Dominique, Bearder, Doyle and Martin1979) suggested that nocturnal primates reduce their activity during the middle period of the night. However, our results are in accordance with other work on the genus Nycticebus, suggesting that these animals are active throughout the night, with the exception of periods of torpor (Starr et al., Reference Starr, Nekaris, Streicher and Leung2010; Coudrat et al., Reference Coudrat, Rogers and Nekaris2011). Bengal slow lorises were most often found in trees of the genus Terminalia (Combretaceae), from which they are known to consume both leaves and gum (Swapna et al., Reference Swapna, Radhakrishna, Gupta and Kumar2009; Rogers & Nekaris, Reference Rogers and Nekaris2011; Das, pers. obs.), therefore we conclude that this tree genus is important for the conservation of Nycticebus spp.
Considering our findings in Assam and Arunachal Pradesh in the context of recent studies in north-east India we conclude that the persistently low encounter rates for the Bengal slow loris, and the threats to its survival, are consistent with its categorization as Vulnerable on the IUCN Red List. However, this categorization is based only on the threats of habitat loss and hunting. We recommend that a comprehensive survey of Bengal slow loris and other threatened primates be carried out in all seven states of north-east India (Assam, Arunachal Pradesh, Mizoram, Nagaland, Tripura, Manipur and Meghalaya), to inform conservation action in this biodiversity hotspot.
Acknowledgements
We thank the Department of Environment and Forest of the Governments of Assam and Arunachal Pradesh for permission to carry out the study. We thank the officials at the survey sites who allowed us to study at night, and provided logistical support. This work was supported by the Margot Marsh Biodiversity Foundation, the Rufford Small Grants Foundation, Primate Conservation Inc. and People's Trust for Endangered Species.
Biographical sketches
Nabajit Das is interested in the conservation of non-human primates in north-east India. His research currently focuses on the ecology and conservation of the Bengal slow loris. K.A.I. Nekaris has studied Asian lorises for over 20 years and conducted field studies of all recognized taxa of slow and slender lorises in South and South-east Asia. She has also initiated awareness and capacity-building programmes for loris conservation in several countries. J. Biswas has extensive field experience in primate conservation and has studied non-human primates in the forests of north-east India, particularly in Assam and Arunachal Pradesh. He is especially interested in conservation of the western hoolock gibbon in north-east India. J. Das is a large-mammal conservationist in north-east India, with extensive experience of surveying non-human primates in the region. P.C. Bhattacharjee is an ecologist and pioneering conservation biologist in north-east India. He led the Indo–US Primate Project until its conclusion in 2000.
