First camera-trap confirmation of Tibetan Brown Bear Ursus arctos pruinosus Blyth, 1854 (Mammalia: Carnivora: Ursidae) with a review of its distribution and status in Nepal

: The Tibetan Brown Bear Ursus arctos pruinosus is a large mammalian carnivore of high-altitude environments that is closely associated with the pastoral landscape. Limited information is available on this species, probably due to its rarity in the Himalaya. To date, scientific evidence of the presence of Tibetan Brown Bears has not been reported officially. The information presented here is based on data collected in the central Himalayan region of Nepal in 2003–2014 during biodiversity surveys and other research. Methods included random walks along livestock trails, transect surveys, opportunistic camera trapping, and herders’ reports & interviews. This is the first camera-trap confirmation of the Tibetan Brown Bear in the central Himalaya. The distribution map was updated based on direct observation, signs and field reports gathered from reliable sources. The presence of signs (diggings, footprints, and feces) and direct observation in the Annapurna-Manaslu landscape reveal that bears are closely associated with Himalayan marmots and other small rodents. Local folklore, legends, and cultural beliefs have played important roles in Brown Bear conservation in the central Himalaya.


INTRODUCTION
Bears are distributed in a wide variety of habitats.Of eight global species, three are found in Nepal: the Sloth Bear Melursus ursinus, the Asiatic Black Bear Ursus tibetanus, and the Brown Bear Ursus arctos (Chetri 2008).The habitats of these species in Nepal are separated by altitude; Sloth Bears are mainly distributed in the lowland protected areas and Terai plains (<1,000 m), the Asiatic Black Bear in the middle mountains up to the treeline (>1,000 m up to 4,000 m), and the Brown Bear above the treeline (4,000-6,000 m; Madhu Chetri pers.obs.).The Brown Bear is a protected species under the National Park and Wildlife Conservation Act of 1973 of the government of Nepal (GoN).The taxonomic classification of this species at the subspecies level is contradictory (https://dnpwc.gov.np/en/mammals/).In the protected list of GoN it is listed as Himalayan Brown Bear.Similarly, a recent taxonomic study revealed that the Asiatic Black Bear found in the Nepal Himalaya belongs to a subspecies Himalayan Black Bear Ursus tibetanus laniger (Kadariya et al. 2018).
In the Himalaya, information concerning Brown Bears is limited (Chetri 2008;Aryal et al. 2010).In nearby China, a population of about 5,000 bears has been reported (Wu 2014).Brown Bears often come into conflict with humans by killing livestock.In Qinghai-Tibetan Plateau they are considered dangerous as they damage houses and injure people (Worthy & Foggin 2008).The population of Brown Bear in Nepal is estimated to be as few as 20 individuals (Jnawali et al. 2011), based on anecdotal reports.Bear signs (diggings, pugmarks, and feces) are mostly seen during the summer in highaltitude pastures.Their fur color ranges from sandy to reddish-brown, and varies individually and seasonally from dark to light.White tips in their hair give the coat a silvery tinge, nose color variable, patches of variable size, and often show a shoulder hump distinctive from other bears.Usually, they have a highly variable white, cream, or buffy collar across the shoulder.They feed on grasses, forbs, berries, roots, insects, and other small mammals as well (Aryal et al. 2012;Nawaz et al. 2019).
To date, very little ecological research has been done on Brown Bears in the Himalaya.The species is listed on the IUCN Red List of Threatened Animals as 'Least Concern' (McLellan et al. 2017).In Nepal, the Brown Bear is listed as Critically Endangered in the National Red Data List (Jnawali et al. 2011)  The main objective of this study was to provide information with regards to the camera trap records of Tibetan Brown Bear in upper Mustang, and update distribution information for the Nepal Himalaya.The present manuscript resulted from the long-term systematic biodiversity surveys and monitoring (2003)(2004)(2005)(2006)(2007)(2008)(2009)(2010)(2011)(2012)(2013)(2014) in the Annapurna-Manaslu landscape.

Study area
The main study area is located (28-29 °N, 83-85 °E) in the northern part of Annapurna Conservation Area (ACA) and the Manaslu Conservation Area (MCA) in the central Himalaya of Nepal (Figure 1).These two conservation areas represent 27% of the protected areas (http:// www.dnpwc.gov.np) and harbor a unique assemblage of trans-and semi-Himalayan flora and fauna diversity of global significance.The distribution of species is also governed by topography, microhabitats, and altitudinal gradients.Above the treeline, the areas represent a grassland typical of the Tibetan plateau and landscapes continue to the Tibetan Autonomous Region of the People's Republic of China.The Bharal Pseudois nayaur, Tibetan Argali Ovis ammon hogdsoni, Kiang Equus kiang, and Tibetan Gazelle Procapra picticaudata are the dominant ungulates found in Brown Bear habitats.The grassland habitats also support the Himalayan Marmot Marmota himalayensis, along with several species of pikas and voles.The high-altitude habitats are also home to several predator species such as Snow Leopard Panthera uncia, Himalayan Wolf Canis lupus chanco, Golden Jackal Canis aureus, Red Fox Vulpes vulpes, Tibetan Sand Fox Vulpes ferrilata, Eurasian Lynx Lynx lynx, weasels Mustela spp., and marten Martes spp.
The local economy is mainly based on animal husbandry.The main livestock consists of yaks, cattleyak hybrids (dzo, jhopas), dwarf lulu cows, horses, goats, and sheep.Local people residing within the conservation area use all accessible areas for livestock grazing.In the study area, the density of livestock is five times higher than that of wild ungulates (Chetri et al. 2017).

Field surveys, data collection and compilation
Information about Brown Bears was compiled from various biodiversity and monitoring surveys, village reports, and interviews.(2013)(2014).The occurrence of the Tibetan Brown Bear was confirmed through camera trap images.Observation of signs such as digging, feces, and footprints were also recorded from the same landscape.The Brown Bear digging signs are easy to identify as it excavates the pasture area in search of Himalayan Marmot, which is also an important prey (Chetri 2008;Aryal et al. 2010).Additionally, digging areas contain claw marks, pugmarks and sometimes hairs.Feces is easy to identify as it is usually deposited in the form of a dung pile (Image 1).Feces in the form of single scat are very large compared to Snow Leopards, Wolves, and Red Foxes, whose habitats are closely associated with Brown Bear in the study area.Only fresh signs were recorded as bear presence.In addition, during 2013-2014, six Reconyx HC550 HyperFire camera traps were used to obtain photographs of the species.The cameras were set in a strategic location where the probability of getting pictures was higher.Camera traps were deployed in 12 locations and the number of camera traps days varied (1-42 days) depending on survey time, availability of suitable habitats, human disturbances, and duration of field works (Figure 1).Besides, possible areas were scanned from the vantage point in the early morning and the afternoon using binoculars (10 x 50 and 12 x 50) and spotting scopes (Nikon ED III spotting scope).In addition, villagers and herders, whenever encountered in the pastures, were also asked about the bear sighting and fresh diggings signs.

Camera traps and signs
Of the 12 camera locations, Tibetan Brown Bear were only photographed in Kopchum Jhalam (29.24 °N, 84.15 °E, 5,000 m) in Dhalung-Chhujung rangeland of upper Mustang of ACA (Image 2A-C).The camera was deployed in a cliff area having single livestock trail leading to a narrow gorge and a small stream.Other interesting species photographed by the camera traps are: Himalayan Wolf, Snow Leopard, Red Fox, Steppe Polecat Mustela eversmanii, and Tibetan Dwarf Hamster Cricetulus alticola.Among all these species, the most frequently photographed species were the livestock and the Himalayan Wolf.The Tibetan Brown Bear signs -footprints, diggings, and feces were encountered in an area where Himalayan Marmots are present.

Distribution update of Brown Bear in Nepal
Various survey records show five important areas of Tibetan Brown Bear distribution in the Annapurna-Manaslu landscape.These include the upper Mustang region-the Damodar Kunda valley, Dhalung-Chhujung valley, Ghemi lekh in upper Mustang of ACA-and the upper reaches of Tsum and Nubri valley in MCA (Table 1, Figure 1).Recent information reveals that the Brown Bear is also present in Limi valley in Humla district (Naresh Kusi pers.comm.November 2021).Local villagers have also photographed this species from Yangma in Kanchenjunga Conservation Area (Hem Raj Acharya pers.comm.August 2021).In 2020, Brown Bears were

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captured in a camera trap from 'musi gaun' in Shey Phoksundo National Park (Gopal Khanal pers.comm.September 2021).All these areas abut with the Tibetan border in the north.Based on direct observation, signs, and field reports obtained from confirmed sources, a distribution map of Brown Bears was updated (Figure 2).

DISCUSSION
In the Himalaya, two subspecies of Brown Bear are recognized: Ursus arctos isabellinus and Ursus arctos pruinosus.The population in the central Himalaya of Nepal is thought to be connected to the large Tibetan Brown Bear population (McLellan et al. 2016).Nepal's location is such that there is possibility of isabellinus in the west and pruinosus in the east.The ssp. isabellinus occurs in Uttarakhand, and hence it is plausible both subspecies may occur in the Nepal Himalaya.According to Pocock (1941), these two subspecies have a distinct skull feature.Also, the Himalayan Brown Bear is characterized by its paler and reddish-brown fur, while the Tibetan Brown Bear has generally darker fur with a developed, white or light yellowish 'collar' around the neck.Image 2 shows a distinct collar around the neck and a darker grizzly fur, small ears with black fur on legs and feet and well distinct shoulder hump are a common physical characteristic of the Tibetan Brown Bear (Lydekker 1897;Sowerby 1920;Pocock 1941).In 2014, a nomadic herdsman (Sonam Norbu) collected a hair sample from Chunjung upper Mustang, Nepal which is close to camera trap location and genetic analysis revealed that the sample belonged to Tibetan Brown Bear (Lan et al. 2017).
The photographs obtained from a camera trap in upper Mustang were sent for confirmation to experts, and based on morphology and pelage pattern, sighting of Tibetan Brown Bear was confirmed (Dave Garshelis pers.comm.December 2020; Xue Yadong pers.comm.December 2020).A small and isolated population of Himalayan Brown Bear was found at higher elevations in the western Himalaya, ranging from mid-Uttarakhand to Jammu & Kashmir in India up to Pakistan.It is unknown whether this subpopulation is connected to Tibet or not (McLellan et al. 2016).Recent genetic study shows that Ursus arctos isabellinus is one of the first branching clades within the Brown Bear lineage, and Ursus arctos pruinosus diverged much later (Lan et al. 2017).It was also shown that extant bears in the region are likely descendants of populations that survived in local refugia during the Pleistocene glaciations (Lan et al. 2017).This is the first camera trap confirmation of the extant of Tibetan Brown Bear in the central Himalaya of Nepal.Earlier in September 2007, the author captured a video of a Brown Bear from the eastern part of upper Mustangthe Damodar Kunda Valley (Chetri 2008).However, the subspecies could not be confirmed as the picture was blurry and taken from a long distance using a camera mount on the spotting scope.
In the Annapurna-Manaslu landscape, signs of Brown Bears are found at an altitude ranging from 4,000-6,000 m.The distribution of Brown Bears correlates with the presence of Himalayan Marmot and other small rodents.Flat alpine grassland with <10° slope, and the valley floor is the most suitable habitat for diggings.Livestock trails are also used by Brown Bears.The present distribution ranges show that the habitat of Tibetan Brown Bears is contiguous with the Tibetan border.In the Manang and Naar-Phu valley of ACA, no signs of Brown Bears have been detected (Figure 2).Evidence of marmot presence in these two valleys is not known until date, which is one of the key prey species of Brown Bears (Aryal et al. 2012).Brown Bear signs were also recorded farther west of upper Mustang, i.e., the area between Shey Phoksundo    2012) also reported the presence of bears in the area.Recent reports and evidence suggest that they are also distributed in the eastern and far-western regions of Nepal Himalaya (Figure 2).This suggests that research on Brown Bears has not been prioritized in Nepal, probably due to their rarity and logistical difficulties, as they inhabit harsh habitats.Long-term biodiversity monitoring surveys reveal that the Himalayan marmot population is highly fluctuating year-to-year, and in some areas they are locally extinct.Only traces of old dens can be seen in some pastures in upper Mustang.Monitoring of marmots and other small rodents is essential as they are also an important prey species of sympatric carnivores associated with the Brown Bear.Several important areas and habitats are identified in the upper Mustang of ACA.These include the Damodar Kunda valley, Dhalung-Chhujung valley, and Ghemi lekh.In the MCA, several signs were recorded in the eastern part (Nubri valley) as well as the western part (Tsum valley) in the flat plains and the areas close to the Tibetan border.Signs of Brown Bears can be seen in villagers.They are once said to be found even in the close vicinity of the villages in the upper Mustang of ACA.These days they are found only in a few high altitudes pastures that abut the Nepal-Tibet border and are occasionally observed by the herders while grazing their livestock in highland pastures during the summer season.The tale of legendary yeti still exists in the region and locals avoid the areas due to fear as Mithe are said to have no heels and extraordinary power.

CONCLUSION
This study provides the first photographic evidence of Tibetan Brown Bear in upper Mustang of Annapurna Conservation Area.Brown Bear sightings and signs (pugmark, hair, scat, and diggings) reveal a close association with Himalayan Marmot and pikas.Recently several sighting and camera-traps records reveals the presence of Brown Bear in eastern and western part of Nepal's Himalaya.Therefore, further research in Brown Bear ecology particularly focusing on taxonomy, population genetics, movement, habitat use, and human-bear interactions is warranted.Additionally, understanding rangeland ecology, human-induced land-use changes, and the impact of climate change in this important changing pastoral landscape will aid in conservation planning and biodiversity conservation in the region.
and protected under schedule 1 of the National Parks and Wildlife Conservation (NPWC) Act, 1973.Brown Bears are also listed under Appendix II of the Convention of International Trade in Endangered Species of Wild Fauna and Flora (CITES 2019).
In 2003-2006, four biodiversity monitoring efforts were conducted in the upper Mustang of ACA as part of the requirement of the J TT biodiversity conservation project funded by the UNDP-Global Environment Facility.The surveys in 2007-2008 and 2011-2012 in ACA and MCA were conducted as part of the biodiversity monitoring program of the National Trust for Nature Conservation through its Annapurna and Manaslu Conservation Area Project.The survey in 2013-2014 was a part of the author's Ph.D. fieldwork.Altogether, 10 years of survey data were compiled to show the distribution pattern of the Brown Bear in the Annapurna-Manaslu landscape.Data were collected from a random walk along the livestock trails (2003-2012), and well-defined transects

Figure 1 . 21804 Tibetan
Figure 1.Map showing the location of Tibetan Brown Bear record sites and distribution of signs in Annapurna-Manaslu landscape, central Himalaya.

Figure 2 .
Figure 2. Distribution update of Brown Bear in Nepal Himalaya.

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of Brown Bear in Annapurna-Manaslu landscape: A-Diggings for Himalayan Marmot | B-Feces (in the form of dung pile) Park and ACA.Aryal et al. (