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Mammalia 75 (2011): 257–268 2011 by Walter de Gruyter Berlin Boston. DOI 10.1515/MAMM.2011.023 2010/131 Article in press - uncorrected proof Assessing mammal distribution and abundance in intricate eastern Himalayan habitats of Khangchendzonga, Sikkim, India Sambandam Sathyakumar*, Tawqir Bashir, Tapajit Bhattacharya and Kamal Poudyal Wildlife Institute of India, P.O. Box 18, Chandrabani, Dehradun 248 001, Uttarakhand, India, e-mail: [email protected] *Corresponding author Abstract We assessed distribution and abundance of mammals in dense, rugged eastern Himalayan habitats of Khangchend- zonga Biosphere Reserve (BR), Sikkim, India, from April 2008 to May 2010, using field methods and remote cameras under varying rain and snow conditions. We report the occur- rence of 42 mammals including 18 species that have high global conservation significance. Three leopards (Panthera uncia, Panthera pardus, Neofelis nebulosa), Tibetan wolf (Canis lupus chanco), wild dog (Cuon alpinus), red panda (Ailurus fulgens), Asiatic black bear (Ursus thibetanus), and two musk deer species (Moschus chrysogaster, M. fuscus) were recorded. Species number decreased with increasing elevation, 22 were recorded in temperate habitats, 18 in sub- alpine and 11 in alpine. The yellow-throated marten (Martes flavigula) and black bear were found to have the most diverse distribution extending from temperate to alpine. Red fox (Vulpes vulpes) was the most abundant carnivore (8.98 "2.31 photo capture/100 days) while goral (Naemorhe- dus goral) was the most abundant prey (9.14 "5.27). Camera trap detected most of the mammals of the intensive study area (35/39). Considering the benefits and limitations, we recommend application of camera trapping along with sign surveys for monitoring of mammals in Khangchendzonga BR for effective conservation. Keywords: abundance; conservation; Khangchendzonga Biosphere Reserve; mammals; remote camera trapping. Introduction The mountainous state of Sikkim (7096 km 2 ) in the eastern Himalayan region lying wedged in between the Himalayan nations of Nepal in the west and Bhutan in the east, is bound- ed by Darjeeling District of West Bengal in the south and a stretch of Tibetan Plateau in the north. This area is positioned at the convergence of three biogeographic realms, viz., Palaearctic, Africo-tropical and Indo-Malayan (Mani 1974) and hence providing a variety of habitats for many primitive as well as newly evolved species resulting in high biodiver- sity in the region. This area is recognized as a global bio- diversity hotspots (Myers et al. 2000) and also one among the important Global 200 Ecoregions (Olson and Dinerstein 1998). The Khangchendzonga Biosphere Reserve (BR) in Sik- kim, being the country’s highest and world’s third highest protected area, is an important high altitude wildlife land- scape covering about 36.92% of the state’s biogeographic area. It is one of the most significant biodiversity hotspots of India with varying eco-zones from temperate to arctic (1220–8586 m), and a repository of many rare and endan- gered flora and fauna primarily due to its location and remarkable variations in altitude and rainfall. In spite of such rich biodiversity all the ecological studies and surveys in the region to date have been largely confined to reptiles (Chettri et al. 2010), birds (Chettri 2000), butterflies (Haribal 1992), vegetation (Chauhan et al. 2003, Tambe and Rawat 2010) and livestock grazing (Singh 2004, Tambe 2007), anthropo- genic pressures (Chettri et al. 2006) and social studies (Krishna et al. 2002). There has been no scientific survey or study on the assessment of mammalian diversity in the region. Effective conservation and management of biodiversity along with the maintenance of human use below the sustain- able level is the major aim of BR management. For achieving this goal, prior knowledge of species diversity, distribution and abundance is essential, so as to detect significant changes for appropriate management interventions. Efficient and reli- able methods for rapid assessment of species richness and abundance are crucial to determine conservation priorities (Silveira et al. 2003). With this background, a study for the establishment of baseline information on the mammalian assemblage of Khangchendzonga BR was initiated with the aid of modern non-invasive technique of remote camera trap- ping (Mace et al. 1994, Karanth 1995, Karanth and Nichols 1998, Carbone et al. 2001, Mackenzie and Royle 2005). Use of remote-triggered, infrared sensor camera units offers one of the best current techniques to reduce sampling discrep- ancies between habitats and observers (Cutler and Swann 1999, Silveira et al. 2003, Swann et al. 2004). Camera-trap- ping have been used across a broad range of mammals and birds (Cutler and Swann 1999), and to address specific research questions including presence/absence (Foster and Humphrey 1995, Whitefield 1998), abundance (Carbone et al. 2001, O’Brien et al. 2003, Rowcliffe et al. 2008), popu- lation parameter (Karanth 1995, Karanth and Nichols 1998), AUTHOR’S COPY | AUTORENEXEMPLAR AUTHOR’S COPY | AUTORENEXEMPLAR

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Page 1: Assessing mammal distribution and abundance in intricate … distribution.pdf · 2011-11-07 · Mammalia 75 (2011): 257–268 2011 by Walter de Gruyter • Berlin • Boston. DOI

Mammalia 75 (2011): 257–268 � 2011 by Walter de Gruyter • Berlin • Boston. DOI 10.1515/MAMM.2011.023

2010/131

Article in press - uncorrected proof

Assessing mammal distribution and abundance in intricate

eastern Himalayan habitats of Khangchendzonga, Sikkim,

India

Sambandam Sathyakumar*, Tawqir Bashir, TapajitBhattacharya and Kamal Poudyal

Wildlife Institute of India, P.O. Box 18, Chandrabani,Dehradun 248 001, Uttarakhand, India,e-mail: [email protected]

*Corresponding author

Abstract

We assessed distribution and abundance of mammals indense, rugged eastern Himalayan habitats of Khangchend-zonga Biosphere Reserve (BR), Sikkim, India, from April2008 to May 2010, using field methods and remote camerasunder varying rain and snow conditions. We report the occur-rence of 42 mammals including 18 species that have highglobal conservation significance. Three leopards (Pantherauncia, Panthera pardus, Neofelis nebulosa), Tibetan wolf(Canis lupus chanco), wild dog (Cuon alpinus), red panda(Ailurus fulgens), Asiatic black bear (Ursus thibetanus), andtwo musk deer species (Moschus chrysogaster, M. fuscus)were recorded. Species number decreased with increasingelevation, 22 were recorded in temperate habitats, 18 in sub-alpine and 11 in alpine. The yellow-throated marten (Martesflavigula) and black bear were found to have the mostdiverse distribution extending from temperate to alpine. Redfox (Vulpes vulpes) was the most abundant carnivore(8.98"2.31 photo capture/100 days) while goral (Naemorhe-dus goral) was the most abundant prey (9.14"5.27). Cameratrap detected most of the mammals of the intensive studyarea (35/39). Considering the benefits and limitations, werecommend application of camera trapping along with signsurveys for monitoring of mammals in KhangchendzongaBR for effective conservation.

Keywords: abundance; conservation; KhangchendzongaBiosphere Reserve; mammals; remote camera trapping.

Introduction

The mountainous state of Sikkim (7096 km2) in the easternHimalayan region lying wedged in between the Himalayannations of Nepal in the west and Bhutan in the east, is bound-ed by Darjeeling District of West Bengal in the south and astretch of Tibetan Plateau in the north. This area is positionedat the convergence of three biogeographic realms, viz.,Palaearctic, Africo-tropical and Indo-Malayan (Mani 1974)

and hence providing a variety of habitats for many primitiveas well as newly evolved species resulting in high biodiver-sity in the region. This area is recognized as a global bio-diversity hotspots (Myers et al. 2000) and also one amongthe important Global 200 Ecoregions (Olson and Dinerstein1998).

The Khangchendzonga Biosphere Reserve (BR) in Sik-kim, being the country’s highest and world’s third highestprotected area, is an important high altitude wildlife land-scape covering about 36.92% of the state’s biogeographicarea. It is one of the most significant biodiversity hotspotsof India with varying eco-zones from temperate to arctic(1220–8586 m), and a repository of many rare and endan-gered flora and fauna primarily due to its location andremarkable variations in altitude and rainfall. In spite of suchrich biodiversity all the ecological studies and surveys in theregion to date have been largely confined to reptiles (Chettriet al. 2010), birds (Chettri 2000), butterflies (Haribal 1992),vegetation (Chauhan et al. 2003, Tambe and Rawat 2010)and livestock grazing (Singh 2004, Tambe 2007), anthropo-genic pressures (Chettri et al. 2006) and social studies(Krishna et al. 2002). There has been no scientific survey orstudy on the assessment of mammalian diversity in theregion.

Effective conservation and management of biodiversityalong with the maintenance of human use below the sustain-able level is the major aim of BR management. For achievingthis goal, prior knowledge of species diversity, distributionand abundance is essential, so as to detect significant changesfor appropriate management interventions. Efficient and reli-able methods for rapid assessment of species richness andabundance are crucial to determine conservation priorities(Silveira et al. 2003). With this background, a study for theestablishment of baseline information on the mammalianassemblage of Khangchendzonga BR was initiated with theaid of modern non-invasive technique of remote camera trap-ping (Mace et al. 1994, Karanth 1995, Karanth and Nichols1998, Carbone et al. 2001, Mackenzie and Royle 2005). Useof remote-triggered, infrared sensor camera units offers oneof the best current techniques to reduce sampling discrep-ancies between habitats and observers (Cutler and Swann1999, Silveira et al. 2003, Swann et al. 2004). Camera-trap-ping have been used across a broad range of mammals andbirds (Cutler and Swann 1999), and to address specificresearch questions including presence/absence (Foster andHumphrey 1995, Whitefield 1998), abundance (Carbone etal. 2001, O’Brien et al. 2003, Rowcliffe et al. 2008), popu-lation parameter (Karanth 1995, Karanth and Nichols 1998),

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258 S. Sathyakumar et al.: Mammals of Khangchendzonga Biosphere Reserve, India

Article in press - uncorrected proof

and daily activity pattern (Pei 1998, Azlan and Sharma2006). The method is efficient for inventories, especially ofcryptic animals, as well as for population studies of speciesfor which individuals can be recognized by marks (Karanth1995, Carbone et al. 2001). Despite the merits of this meth-od, some landscapes can be so remote, steep or so denselyvegetated that the conventional sampling designs may bechallenged.

This study was primarily aimed to fill the above-men-tioned research gap and to prepare an inventory for mammalsof Khangchendzonga BR, but was also aimed to check theeffectiveness of camera trapping method in the steep, ruggedand high precipitation environment of KhangchendzongaBR. In this paper, we report the results of the first such studyon mammals conducted in the Sikkim Himalaya. Wedescribed the distribution, conservation status and relativeabundances of the mammals found in the BR and also dis-cussed the effectiveness of camera traps as a monitoring toolfor mammals in Khangchendzonga BR.

Materials and methods

Study area

The Khangchendzonga BR encompasses an area of 2619.92km2 including the Khangchendzonga National Park (NP)(1784 km2) and a buffer zone of about 836 km2 (Tambe2007). Located between 278309–278559 N and 888029–888379 E it is connected to the adjacent KhangchendzongaConservation Area in eastern Nepal, Barsey and MaenamWildlife Sanctuaries in Sikkim and Singalila BR in Darjee-ling district of West Bengal, through a number of corridors(Tambe 2007). The area is classified as a biogeographicprovince 2C – Central Himalaya with the northern partincluded in biogeographic province 1B – Trans-HimalayaTibetan Plateau (Rodgers et al. 2000). The varying elevationof 1220 m to 8586 m within an aerial distance of just 42 kmwith about 90% area above 3000 m and 70% above 4000 mmakes this park a unique natural heritage hotspot in theworld.

The area of Khangchendzonga BR has been divided intoseven watersheds or river subsystems (Figure 1) namelyLhonak (15%), Zemu (23%), Lachen (5%), Rangyong(36%), Rangit (6%), Prek (8%) and Churong (7%). In thisstudy, Prek chu (278219–278379 N, 888129–888179 E) (chu-sriver) catchment area (182 km2) was selected as the inten-sive study area (Figure 2) because it represents all the habitatcharacteristics of Khangchendzonga BR (Sathyakumar et al.2009), although surveys were also conducted in Lhonak,Zemu, Lachen and Churong watersheds. Its highest and low-est elevation being 6691 m (summit of Pandim) and 1200 m(Tambe 2007), the Prek chu watershed can be divided intosix habitat classes, viz., mixed sub-tropical (1%), mixed tem-perate (16%), sub-alpine (36%), alpine pastures (5%), rockand snow cover (41%) and water bodies (1%). The water-shed has a typical oceanic climate with an average annualrainfall of around 2230 mm (Tambe 2007).

The study was conducted for a period of 2 years fromApril 2008 to May 2010. Due to the topography and remote-ness of the area all field activities were carried out in theform of field expeditions, i.e., camping in different areas ofthe Prek chu watershed. One field survey was usually of7–8 days and all the sampling units were replicated and mon-itored after every 7–10 days.

Reconnaissance surveys

In order to get a fair knowledge of the area exploration sur-veys were carried out in the early months of the study periodin the five watersheds (Churong, Lachen, Zema, Lhonak andPrek) of the Khangchendzonga BR. This was followed byapplication of some conventional sampling methods such astrail sampling, scanning, sign surveys, camera trapping andlocal interviews for the assessment of mammalian fauna (dis-tribution and relative abundance) depending on the feasibilityof the terrain.

Trail sampling, scanning and sign surveys

Trail sampling was used for detection of mammals in differ-ent habitats of the study area. These trails were identifiedwith slight modification from conventional transects (Burn-ham et al. 1981) for Himalayan terrain (Sathyakumar 1994,Vinod and Sathyakumar 1999). Scan sampling, ridge walk-ing (Green 1978, Bhatnagar 1993, Sathyakumar 1994, 2004)and sign surveys along trails, ridges and nullahs (streams)(Bennet et al. 1940, Chundawat 1992, Sathyakumar 1994)were also carried out. Trail sampling (ns22; 1.5–7 km) with-in the intensive study area (Figure 3) was repeated (223walks), and sign surveys were carried out once in month forthe intensive study area (25 surveys). Trail sampling and signsurveys were carried out once in each of the other fourwatersheds.

Camera trapping

Based on the knowledge acquired through reconnaissancesurveys, as mentioned earlier, Prek chu watershed was select-ed as the intensive study area for camera traps studies. Thestudy area was divided into 4 km2 blocks within a Geograph-ic Information System (GIS) (ARC VIEW 3.2 and ARC GIS9.0). For simplicity, the area was categorized into three dif-ferent survey zones according to the habitats, viz., temperate(1200–3000 m), sub-alpine (3000–4000 m) and alpine(above 4000 m) and the camera traps were deployed corre-sponding to the area coverage of the survey zones and theiraccessibility (seven blocks in temperate, 12 blocks in sub-alpine and five blocks in alpine). Within each survey zone,cameras were placed in likely animal-use areas and )500 minter-camera distance. Twenty-seven camera traps weredeployed at 71 sites in 24 blocks (Figure 3). The cameratrapping was done continuously in all the seasons (winter:January–March; spring: April–May; summer: June–Septem-ber; autumn: October–December) using four models of infra-red-triggered camera units: two DeerCam (Deercam ScoutingCamera, Non Typical, Inc., Park Falls, WI, USA), two Wild-

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S. Sathyakumar et al.: Mammals of Khangchendzonga Biosphere Reserve, India 259

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Figure 1 Location of Khangchendzonga Biosphere Reserve in Sikkim, India showing the different watersheds including Prek Chu catch-ment – the intensive study area.

view (wildview xtreme2, Grand Prairie, Texas, USA), 18Stealthcam (Stealthcam, LLC, Grand Prairie, Texas, USA)and five Moultrie (Moultrie Feeders, Alabaster, Alabama,USA). Head-on, oblique and side-view camera configura-tions were used to obtain photographs at varying body ori-entations (Blomqvist and Nystrom 1980, Jackson et al.2006). Since the study species were rare and the area beingvast, the strategy was to survey more sampling units lessintensively rather than less sampling units more intensively(Mackenzie and Royle 2005), for rapid assessment of mam-malian assemblage. Monitoring of camera traps was done atleast twice a month which included changing the batteriesand memory card.

One major problem faced during this study was the lackof adequate data from direct evidences (visual encountersand camera trapping) for abundance estimation in order toovercome this problem the method of photographic rate wasused. Photographic rate is defined as the number of cameradays (24 h) per study species (G1-year-old) photographsummed across all camera traps in the study (Carbone et al.2001). Based on photo capture rates, an index of relativeabundance (RAI) as the number of days required for obtain-ing a photo capture of a species (Carbone et al. 2001) wascalculated. Photo capture rate was calculated as the number

of photographs of a species divided by the number of trap-days per site. Trap-days were computed as the number of24-h periods from deployment of camera until the film/mem-ory card was used up or the camera was retrieved. Instanceswhere the same species were captured by the same cameramore than once within 1 h were excluded from trap ratecalculation (Bowkett et al. 2007). This was a compromisebetween scoring the same individual multiple times andmissing individuals (Rovero et al. 2005) and is more con-servative than other published studies (e.g., Kinnaird et al.2003).

Total camera trap days in the study period were 6278 with1407 in temperate zone (26 sites), 3061 in sub-alpine zone(20 sites) and 1810 in alpine zone (25 sites), respectively.

Local interviews

In order to assess the awareness of local people regardingthe mammal diversity of the area and to verify it with cameratrapping results (Can and Togan 2009), interviews and infor-mal discussions (Mishra et al. 2006) were conducted in 15villages viz., eight in Prek and Churong, six in Zema andLachen and one in Lhonak watersheds. In Prek and Churongwe sampled six villages at the border of the catchment and

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260 S. Sathyakumar et al.: Mammals of Khangchendzonga Biosphere Reserve, India

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Figure 2 Major habitat categories and contours of Prek Chu Catchment, Khangchendzonga Biosphere Reserve, Sikkim, India.

one each at the core and buffer zones. In the greater Hima-layan zone of the northern part of Khangchendzonga BR,i.e., Zema and Lachen, surveys were conducted in six bor-dering villages of the watersheds. In northern part (Lhonak),surveys were conducted in one village adjacent to the trans-Himalayan zone during which Dokpa Yak herders and Indo-Tibet Border Police personnel were also interviewed. In total,interviews and informal discussions were conducted with theheads of 72 households which included farmers, livestockherders, former hunters and trekking guides. The respondentswere shown photographs and drawings of the mammal spe-cies provided in field guides (Prater 1971, Menon 2003) andtheir knowledge on species occurrence and natural historywas recorded.

Results

Mammal assemblage

We record the occurrence of 42 species of mammals belong-ing to seven orders and 16 families in the Khangchendzonga

BR out of which we confirm the presence of 40 speciesthrough visual encounters, photo-captures, signs and trails,and the remaining two based on the information from thelocals (Table 1). Of the 42 species recorded, 18 are of highglobal conservation significance, categorized as criticallyendangered (1), endangered (4), vulnerable (4) and nearthreatened (9) on the IUCN Red list (IUCN 2010). A totalof 21 species recorded are characteristically high altitudefauna, although some of them occur over a wide altitudinalrange (Table 1). Almost all the species of mammals (39)were recorded to occur in the Prek chu catchment excepttypical trans-Himalayan species – Tibetan wolf (Canis lupuschanco Gray, 1863), Himalayan marmot (Marmota hima-layana Hodgson, 1841) and Plateau pika (Ochotona curzo-niae Hodgson, 1858). Presence of three cryptic and nocturnalspecies such as golden cat (Pardofelis temminckii Vigors andHorsfield, 1827), large Indian civet (Viverra zibetha Linnae-us, 1758) and black musk deer (Moschus fuscus Li, 1981)were reported from Khangchendzonga BR for the first time.Villagers of Churong and Prek chu catchments reported pres-ence of common leopard (Panthera pardus Linnaeus, 1758)

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Figure 3 Map of intensive study area showing trails and locations of camera traps in 2 km=2 km grids in Prek Chu Catchment,Khangchendzonga Biosphere Reserve, Sikkim, India.

in Khangchendzonga BR as they mentioned about three live-stock depredation incidents by common leopard in recentpast. Binturong (Arctictis binturong Raffles, 1821) wasreported from Prek chu catchment; many eco-tourist guidesand local villagers confirmed its presence in the area as theyreadily identified the photograph of the species as Ruk-Bhalu(local, meaning tree-bear) in Nepali. Some aged livestockherders of Yuksam reported sighting of Chinese pangolin

(Manis pentadactyla Linnaeus, 1758) in lower moist tem-perate forests 20 years ago, but no recent sighting was report-ed, neither was it detected by any of the methods. In Lhonakcatchment (trans-Himalayan zone), Dokpa Yak herders con-firmed frequent sightings of Tibetan wolf as well as snowleopard (Panthera uncia Schreber, 1775) while Indo-TibetBorder Police (ITBP) personnel confirmed presence of bluesheep (Pseudois nayaur Hodgson, 1833) in large groups.

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262 S. Sathyakumar et al.: Mammals of Khangchendzonga Biosphere Reserve, India

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Tab

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port

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the

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ea.

Spec

ies

Red

list

Pres

ence

2E

vide

nce3

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nce

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capt

ure

rate

Phot

o-ra

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ain

habi

tat

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tudi

nal

stat

us1

five

wat

ersh

eds4

(pho

to/1

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mda

ys)5

(day

s/ca

ptur

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cupi

edra

nge

(m)

PL

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TS

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nivo

res

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NC

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PC,

SC,

TR

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0.25

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ther

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Figure 4 Scatter plot showing relationship between photo capture rates of species with their respective body weights.

Signs of Tibetan wolf, snow leopard, blue sheep and sigh-tings of Himalayan marmot were obtained during trail sam-pling and sign survey.

Distribution and abundance

Numbers of detected mammal species decreased withincreasing elevation, 21 species were recorded in temperatehabitats followed by 18 in sub-alpine and 11 in alpine hab-itats of Khangchendzonga BR. Snow leopard and blue sheepoccurred in all the surveyed catchments inhabiting the alpinehabitat above 4000 m elevation, while the distribution ofother species varied both across catchments and altitudes(Table 1). In this study, we document (photo captures) newaltitudinal limits of distribution for certain species whichwere not known earlier, viz., clouded leopard (Neofelis nebu-losa Griffith, 1821) (3720 m), golden cat (3990 m), junglecat (Felis chaus Schreber, 1777) (4010 m), Asiatic black bearwUrsus thibetanus G. (Baron) Cuvier, 1823x (4120 m), wilddog (Cuon alpinus Pallas, 1811) (4010 m), Himalayan yel-low-throated marten (Martes flavigula Boddaert, 1785)(4010 m) and wild pig (Sus scrofa Linnaeus, 1758) (4010 m).Interestingly, the yellow-throated marten and Asiatic blackbear were found to have the most diverse altitudinal rangeextending from temperate to alpine habitats, evident fromtheir photo-captures at 4010 m and 4120 m, respectively,although their main habitats of occurrence were temperateand sub-alpine. Clouded leopard, red panda (Ailurus fulgensF.G. Cuvier, 1825) and stone marten (Martes foina Endeben,1777) were recorded to inhabit the sub-alpine forests up to4000 m elevation, while leopard cat (Prionailurus bengalen-sis Kerr, 1792), jackal (Canis aureus Linnaeus, 1758) andall the viverid species were found to occupy the temperatezone.

Relative abundance indexes (photo capture/100 camdays"S.E.) showed red fox (Vulpes vulpes Linnaeus, 1758)to be the most abundant carnivore in the alpine zone(8.98"2.31) and yellow-throated marten in both sub-alpine(1.58"0.48) and temperate (6.85"3.32) zones. Among the

five species of felids, leopard cat was the most abundant(2.157"0.72) and clouded leopard the rarest (0.03"0.03)species. Among the prey species, blue sheep (2.73"1.90)was the most abundant ungulate in the alpine zone whileserow (Naemorhedus sumatraensis Bechstein, 1799)(1.01"0.65) and goral (Naemorhedus goral Hardwicke,1825) (9.14"5.27) in the sub-alpine and temperate zones,respectively. In case of small mammals including rodents andlagomorphs, Sikkim rat (Rattus sikkimensis Hinton, 1919)(7.63"3.57), and large-eared pika (Ochotona macrotis Gun-ther, 1875) (5.92"2.76), were the most abundant. The cam-era trapping effort was successful to record most of themammals irrespective of their body sizes (Figure 4).

Discussion

Mammal assemblage

The minimum knowledge needed for effective managementof mammals within protected areas includes knowing whatspecies are present, their distribution within the area, andtheir relative abundance across different habitat types (Shenget al. 2010). Presence of 18 globally threatened mammalsdepicts the priority of proper management interventions toprotect their habitats in Khangchendzonga BR. This mammalassemblage is comparable with mammal diversity of someother eastern and central Himalayan landscapes such as theproposed high altitude National Park, Arunachal Pradesh (35mammals, Mishra et al. 2006) and Langtang National Park,Nepal (32 mammals, Fox et al. 1996).

Distribution and abundance

Gradual increase in altitude results change in habitat condi-tions which affect the mammal distribution in Khangchend-zonga BR. Low temperature, harsh climatic conditions andfewer resources restricted mammal assemblage to 11 speciesin alpine zone of the study area. Moist and relatively warm

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habitats harbored more mammal species in sub-alpine (18species) and temperate zone (22 species) of Khangchend-zonga BR. Use of intensive camera trapping in Prek chu maybe the reason behind the good number of detections (39mammals) whereas in some cases proper identification ofdifferent mammal species was not possible in other valleyswhich may have the potential to be as diverse as this area interms of mammal assemblage.

Photo capture rates of different mammals in Prek chucatchment area indicate an altitudinal (thus forest type spe-cific) pattern of mammal distribution. Comparison betweenphoto capture rates in different habitats showed red fox andsnow leopard as the main predator of alpine zone and bluesheep and large-eared pika Ochotona macrotis as the mainprey base there. Himalayan musk deer (Moschus chrysogas-ter Hodgson, 1839), Pale weasel (Mustela altaica Pallas,1811) and Siberian weasel (Mustela sibirica Pallas, 1773)were rarely detected in the alpine zone indicating their lowabundance. According to the relative abundance index: yel-low-throated marten, stone marten and golden cat were themajor predators of sub-alpine zone and yellow-throated mar-ten, leopard cat, Himalayan palm civet (Paguma larvataC.E.H. Smith, 1827) and large Indian civet the major pred-ators of temperate zone. Similarly relative abundances ofungulate prey depicts serow as the major ungulate prey insub-alpine and goral (and barking deer Muntiacus muntjakZimmermann, 1780) in the temperate zone of the study area,respectively. Relative abundances of smaller mammals suchas rodents and lagopmorphs depicted Sikkim rat as the mostabundant smaller prey in both sub-alpine and temperate for-ests. Among the other rodent preys, hoary-bellied Himalayansquirrel (Callosciurus pygerythrus I. Geoffroy Saint Hilaire,1832) and Himalayan crestless porcupine (Hystrix brachyuraLinnaeus, 1758) were also abundant in temperate forests. Insub-alpine zone, clouded leopard and red panda (both semi-terrestrial in nature) were present and detected by the cam-eras very rarely. Chance of detection of these two mammalsby the present sampling design (where cameras weredeployed on ground level to detect other terrestrial mam-mals) was low, thus very low photo capture rate of these twospecies may not reflect their real status in the study area.Among other threatened mammals, infrequent detections andvery low relative abundance of wild dog suggest their non-resident nature (local movements in between adjacent water-sheds) about which local people had mentioned duringinterviews. Presence of Himalayan tahr (Hemitragus jemla-hicus C.H. Smith, 1826) was already reported from Rangitcatchment area, sexual segregation during monsoon mayhave resulted in the photo capture of males in Prek chu dur-ing monsoon only. An interesting finding of this explorativestudy on mammal assemblage may be the non-detection oflarge carnivores (apart from seasonal presence of Asiaticblack bear in low abundance) in the sub-alpine and temperateforests. Prey species diversity (Primates-2, Ungulates-4,Rodents-3) and relative abundance (Table 1) in the temperatezone may be adequate to harbor large carnivores such ascommon leopard, which is a common feature of the mam-malian fauna of the same altitude zones at different Protected

Areas throughout the Himalaya (Prater 1971, Chauhan andGoyal 2001, Aryal and Kriegenhoffer 2009, Dar et al. 2009).Report of very infrequent presence of common leopard inthe low altitude zones (1200–1850 m) of different valleys ofKhangchendzonga BR and only three livestock killing inci-dents at the lowermost part (1830 m) of the intensive studyarea in three years may indicate the extermination of thepredator from the study area due to retaliatory killings in therecent past.

Effectiveness of camera traps as a monitoring tool in

eastern Himalayan landscape

In this study, camera traps were used for the first time as abiodiversity monitoring tool in Sikkim. Camera trap detectedmost of the mammals of the intensive study area (35 of 39),among them three cryptic and nocturnal species (Golden cat,Large Indian civet and Black musk deer) were detected forthe first time in Khangchendzonga BR. Three small mam-mals (Sikkim rat, Moupin’s pika Ochotona thibetana Milne-Edwards, 1871 and Forrest’s pika O. forresti Thomas, 1923)were properly identified exclusively through camera trapphotographs. Our study using camera traps has been veryeffective in recording most of the mammal species irrespec-tive of their body size, but some limitations of this methodin this particular landscape were also realized. These are: (1)due to high sensitivity of infrared sensor camera units, pho-tographs of low moving clouds, movement of vegetation dueto wind were also captured which reduced the effective cam-era trapping period; (2) temporary camera failure due toextremely low temperature and high rainfall; (3) steep andrugged terrain of the study area limited camera monitoringsurvey by foot alone which reduced the effective cameratrapping period; (4) some camera units could not be checkedduring winter as the trails were rendered inaccessible due toheavy snowfall in the area; and (5) loss of the camera trapunits from remote alpine areas as well as from dense forestnear habitation along with several instances of loss of mem-ory card also reduced the effective camera trapping period.

Considering the benefits and limitations, we believe, inKhangchendzonga BR, camera-trapping can provide a reli-able and standardized means for BR staff to document thepresence of large and medium-sized mammals and, if sys-tematically placed and regularly monitored can help to esti-mate precise abundance of mammals with or withoutidentifiable features.

Following the example of newly initiated mammal andbird monitoring protocol programs using camera traps inChinese nature reserves (Sheng et al. 2010), we also suggestcamera trapping for other watersheds of KhangchendzongaBR with active involvement of forest staff and local people.But prior to that, intensive training of field staff on workingprinciple, survey design and handling of camera-traps andvillage level awareness meets for local people will be ofgreat help to popularize this technique. Thus, well-designedmonitoring programs using camera traps supplemented bylocal knowledge can provide robust data to wildlife managersto monitor the long-term population or biodiversity trends(Pereira and Cooper 2006, Marsh and Trenham 2008). We

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believe a higher initial outlay of funds and training for acamera trap based monitoring system will provide the frame-work needed for conservation programs in KhangchendzongaBR to move forward.

Acknowledgements

We are grateful to the Department of Forests, Environment andWildlife Management, Government of Sikkim for granting us per-mission to work in Sikkim. We thank the Wildlife Institute of India,Dehradun for providing us the grants and support. We thank thetwo anonymous reviewers for their valuable comments and sugges-tions for the improvement of this manuscript.

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268 S. Sathyakumar et al.: Mammals of Khangchendzonga Biosphere Reserve, India

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