Upload
others
View
1
Download
0
Embed Size (px)
Citation preview
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),
AUTHOR’S COPY | AUTORENEXEMPLAR
AUTHOR’S COPY | AUTORENEXEMPLAR
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-
AUTHOR’S COPY | AUTORENEXEMPLAR
AUTHOR’S COPY | AUTORENEXEMPLAR
S. Sathyakumar et al.: Mammals of Khangchendzonga Biosphere Reserve, India 259
Article in press - uncorrected proof
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
AUTHOR’S COPY | AUTORENEXEMPLAR
AUTHOR’S COPY | AUTORENEXEMPLAR
260 S. Sathyakumar et al.: Mammals of Khangchendzonga Biosphere Reserve, India
Article in press - uncorrected proof
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)
AUTHOR’S COPY | AUTORENEXEMPLAR
AUTHOR’S COPY | AUTORENEXEMPLAR
S. Sathyakumar et al.: Mammals of Khangchendzonga Biosphere Reserve, India 261
Article in press - uncorrected proof
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.
AUTHOR’S COPY | AUTORENEXEMPLAR
AUTHOR’S COPY | AUTORENEXEMPLAR
262 S. Sathyakumar et al.: Mammals of Khangchendzonga Biosphere Reserve, India
Article in press - uncorrected proof
Tab
le1
Mam
mal
sco
nfir
med
orre
port
edin
the
Kha
ngch
endz
onga
Bio
sphe
reR
eser
ve,
Sikk
im,
with
thei
rIU
CN
Red
list
stat
us,
the
type
ofev
iden
ce,
thei
roc
curr
ence
inth
efi
vew
ater
shed
s,ph
otog
raph
icra
tes,
mai
nha
bita
tsoc
cupi
edan
dth
eal
titud
inal
rang
ein
the
stud
yar
ea.
Spec
ies
Red
list
Pres
ence
2E
vide
nce3
Occ
urre
nce
inPh
oto-
capt
ure
rate
Phot
o-ra
teM
ain
habi
tat
Alti
tudi
nal
stat
us1
five
wat
ersh
eds4
(pho
to/1
00ca
mda
ys)5
(day
s/ca
ptur
e)oc
cupi
edra
nge
(m)
PL
ZC
La
TS
AT
SA
Car
nivo
res
*Sno
wle
opar
dE
NC
onf.
PC,
SC,
TR
,L
Iq
0.25
7"0.
1615
0.8
q)
4000
Pan
ther
aun
cia
Clo
uded
leop
ard
VU
Con
f.PC
,L
Iq
0.03
"0.
0330
61q
2500
–380
0N
eofe
lis
nebu
losa
Com
mon
leop
ard
NT
Rep
.SC
,K
,L
Iq
q-
2000
Pan
ther
apa
rdus
Gol
den
cat
NT
Con
f.PC
q0.
236"
0.19
0.61
8"0.
1821
2.7
2100
–395
0P
ardo
feli
ste
mm
inck
iJu
ngle
cat
LC
Con
f.S,
PC,
LI
q0.
136"
0.09
0.10
9"0.
0674
4.7
1750
–395
0F
elis
chau
sL
eopa
rdca
tL
CC
onf.
PC,
LI
q2.
157"
0.72
37.0
2q
1750
–275
0P
rion
ailu
rus
beng
alen
sis
*Asi
atic
blac
kbe
arV
UC
onf.
PC,
SC,
LI
q0.
546"
0.23
0.19
0"0.
080.
05"
0.05
279.
2q
q20
00–4
250
Urs
usth
ibet
anus
*Red
pand
aV
UC
onf.
PC,
LI
q0.
071"
0.05
1020
.3q
2500
–380
0A
ilur
usfu
lgen
sW
ilddo
gE
NC
onf.
PC,
LI
q0.
182"
0.07
0.08
"0.
0854
1.2
q31
00–4
200
Cuo
nal
pinu
s*T
ibet
anw
olf
CR
Con
f.T
R,
K,
SC,
LI
)40
00C
anis
lupu
sch
anco
*Red
fox
LC
Con
f.PC
,SC
,L
Iq
0.52
5"0.
368.
98"
2.31
14.2
q37
50–4
500
Vul
pes
vulp
esJa
ckal
LC
Con
f.S,
PC,
LI
0.08
"0.
0814
07q
-25
00C
anis
aure
us*H
imal
ayan
palm
cive
tL
CC
onf.
PC,
LI
1.90
"0.
7846
.9q
1750
–270
0P
agum
ala
rvat
aL
arge
Indi
anci
vet
NT
Con
f.PC
q1.
47"
0.66
67q
1750
–270
0V
iver
razi
beth
a*H
imal
ayan
yello
wth
roat
edm
arte
nL
CC
onf.
S,PC
,L
Iq
q6.
85"
3.32
1.58
"0.
480.
114"
0.09
30.7
1750
–420
0M
arte
sfl
avig
ula
*Sto
nem
arte
nL
CC
onf.
PC,
LI
0.62
3"0.
2711
7.7
q32
00–3
950
Mar
tes
foin
aB
intu
rong
VU
Rep
.SC
,L
Iq
2000
–300
0A
rcti
ctis
bint
uron
gSi
beri
anw
ease
lL
CC
onf.
S,PC
q0.
043"
0.03
1530
.5q
3000
–400
0M
uste
lasi
biri
ca*P
ale
wea
sel
NT
Con
f.S,
PCq
0.05
"0.
0590
5q
)40
00M
uste
laal
taic
a
AUTHOR’S COPY | AUTORENEXEMPLAR
AUTHOR’S COPY | AUTORENEXEMPLAR
S. Sathyakumar et al.: Mammals of Khangchendzonga Biosphere Reserve, India 263
Article in press - uncorrected proof
(Tab
le1
cont
inue
d)
Spec
ies
Red
list
Pres
ence
2E
vide
nce3
Occ
urre
nce
inPh
oto-
capt
ure
rate
Phot
o-ra
teM
ain
habi
tat
Alti
tudi
nal
stat
us1
five
wat
ersh
eds4
(pho
to/1
00ca
mda
ys)5
(day
s/ca
ptur
e)oc
cupi
edra
nge
(m)
PL
ZC
La
TS
AT
SA
Ung
ulat
es*B
lue
shee
pL
CC
onf.
S,PC
,L
Iq
2.73
"1.
9021
.04
q)
4000
Pse
udoi
sna
yaur
*Him
alay
anm
usk
deer
EN
Con
f.S,
PC,
LI
3700
–450
0M
osch
usch
ryso
gast
er*
Bla
ckm
usk
deer
EN
Con
f.PC
q0.
085"
0.06
0.13
"0.
106
974.
2q
3500
–400
0M
osch
usfu
scus
*Him
alay
anta
hrN
TC
onf.
PC,
LI
q0.
13"
0.07
0.05
"0.
0581
1.8
3700
–420
0H
emit
ragu
sje
mla
hicu
s*M
ainl
and
sero
wN
TC
onf.
S,PC
,L
Iq
q1.
064"
0.75
1.01
"0.
6565
.7q
q21
00–3
800
Nae
mor
hedu
ssu
mat
raen
sis
*Gor
alN
TC
onf.
S,PC
q9.
14"
5.27
0.97
"0.
6521
.3q
q20
00–3
800
Nae
mor
hedu
sgo
ral
Bar
king
deer
LC
Con
f.S,
PC,
LI
5.88
"2.
6719
.5q
2000
–260
0M
unti
acus
mun
tjak
Wild
pig
LC
Con
f.S,
PC,
LI
0.67
2"0.
290.
03"
0.03
140.
7q
2000
–420
0Su
ssc
rofa
Prim
ates
Ass
ames
em
acaq
ueN
TC
onf.
S,PC
2.56
"1.
0742
.6q
2000
–270
0M
acac
aas
sam
ensi
sM
’Cle
lland
,18
40*C
entr
alH
imal
ayan
lang
urN
TC
onf.
S,PC
1.40
"1.
3482
.8q
2000
–270
0Se
mno
pith
ecus
schi
stac
eus
Hod
gson
,18
40
Rod
ents
*Ora
nge-
belli
edH
imal
ayan
squi
rrel
LC
Con
f.S,
PCq
q0.
084"
0.06
703.
5q
2100
–285
0D
rem
omys
lokr
iah
Hod
gson
,18
36H
oary
-bel
lied
Him
alay
ansq
uirr
elL
CC
onf.
PCq
q3.
04"
2.43
25.1
q17
50–2
300
Cal
losc
iuru
spy
gery
thru
sPa
rtic
olor
edfl
ying
squi
rrel
LC
Con
f.PC
,L
Iq
0.07
"0.
047
1020
.3q
q20
00–3
800
Hyl
opet
esal
boni
ger
Hod
gson
,18
36Fi
ve-s
trip
edpa
lmsq
uirr
elL
CC
onf.
Sq
qF
unam
bulu
spe
nnan
tii
Wro
ught
on,
1905
*Him
alay
anm
arm
otL
CC
onf.
Sq
q)
4000
Mar
mot
ahi
mal
ayan
aH
imal
ayan
cres
tless
porc
upin
eL
CC
onf.
S,PC
,L
Iq
q2.
245"
0.83
35.2
q20
00–2
600
Hys
trix
brac
hyur
a*S
ikki
mra
tL
CC
onf.
S,PC
7.63
"3.
570.
63"
0.50
28.8
q20
00–3
750
Rat
tus
sikk
imen
sis
AUTHOR’S COPY | AUTORENEXEMPLAR
AUTHOR’S COPY | AUTORENEXEMPLAR
264 S. Sathyakumar et al.: Mammals of Khangchendzonga Biosphere Reserve, India
Article in press - uncorrected proof
(Tab
le1
cont
inue
d)
Spec
ies
Red
list
Pres
ence
2E
vide
nce3
Occ
urre
nce
inPh
oto-
capt
ure
rate
Phot
o-ra
teM
ain
habi
tat
Alti
tudi
nal
stat
us1
five
wat
ersh
eds4
(pho
to/1
00ca
mda
ys)5
(day
s/ca
ptur
e)oc
cupi
edra
nge
(m)
PL
ZC
La
TS
AT
SA
Lag
omor
phs
*Lar
ge-e
ared
pika
LC
Con
f.S,
PCq
5.92
"2.
7622
.9q
)40
00O
chot
ona
mac
roti
s*M
oupi
n’s
pika
LC
Con
f.PC
q0.
10"
0.10
612.
2q
3000
–400
0O
chot
ona
thib
etan
aFo
rres
t’spi
kaL
CC
onf.
S,SP
?O
chot
ona
forr
esti
Plat
eau
pika
LC
Con
f.S
4500
–550
0O
chot
ona
curz
onia
e
Inse
ctiv
ores
Shre
wC
onf.
SPq
q?
Chi
ropt
era
Pear
son’
sH
orse
shoe
Bat
LC
Con
f.S
-18
50R
hino
loph
uspe
arso
nii
Hor
sfie
ld,
1851
Spec
ies
nam
espr
efix
edw
ithas
teri
sks
indi
cate
high
altit
ude
mou
ntai
nfa
una.
1E
N,
enda
nger
ed;
VU
,vu
lner
able
;L
R,
low
erri
sk;
NT,
near
thre
aten
ed;
DD
,da
tade
fici
ent.
2C
onf.
,co
nfir
med
;R
ep.,
repo
rted
.3S,
sigh
ting;
SP,
spec
imen
;PC
,ph
oto
capt
ure;
SC,
Scat
/Dun
g;T
R,
trac
k;K
,ki
ll;L
I,lo
cal
info
rmat
ion.
4P,
Prek
;L
,L
hona
k;Z
,Z
ema;
C,
Chu
rong
;L
a,L
ache
n.5T,
tem
pera
te;
S,su
b-al
pine
;A
,al
pine
.
AUTHOR’S COPY | AUTORENEXEMPLAR
AUTHOR’S COPY | AUTORENEXEMPLAR
S. Sathyakumar et al.: Mammals of Khangchendzonga Biosphere Reserve, India 265
Article in press - uncorrected proof
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
AUTHOR’S COPY | AUTORENEXEMPLAR
AUTHOR’S COPY | AUTORENEXEMPLAR
266 S. Sathyakumar et al.: Mammals of Khangchendzonga Biosphere Reserve, India
Article in press - uncorrected proof
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
AUTHOR’S COPY | AUTORENEXEMPLAR
AUTHOR’S COPY | AUTORENEXEMPLAR
S. Sathyakumar et al.: Mammals of Khangchendzonga Biosphere Reserve, India 267
Article in press - uncorrected proof
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.
References
Aryal, A. and B. Kriegenhoffer. 2009. Summer diet composition ofthe common leopard Panthera pardus (Carnivora: Felidae) inNepal. J. Threat. Taxa. 1: 562–566.
Azlan, J.M. and D.S.K. Sharma. 2006. The diversity and activitypatterns of wild felids in a secondary forest in Peninsular Malay-sia. Oryx. 40: 36–41.
Bennet, L.J., P.F. English and R. McCoun. 1940. A study of deerpopulations by pellet group counts. J. Wildl. Manage. 4: 398–403.
Bhatnagar, Y.V. 1993. Origin and distribution of Himalayan ungu-lates and the factors affecting their present distribution. In:(Y.P.S. Pangtey and R.S. Rawal, eds.) High altitude of the Hima-laya. Nainital, Gyanodaya Prakashan. pp. 247–254.
Blomqvist, L. and V. Nystrom. 1980. On identifying snow leopardsby their facial markings. In: (L. Bloomqvuist, ed.) Internationalpedigree book of snow leopards. Vol. 2. Helsinki Zoo, Helsinki,Finland. pp. 159–167.
Bowkett, A.E., F. Rover and A.R. Marshall. 2007. The use of cam-era-trap data to model habitat use by antelope species in theUdzungwa Mountain forests, Tanzania. African J. Ecol. 46: 479–487.
Burnham, K.P., D.R. Anderson and J.L. Laake. 1981. Line transectestimation of bird population density using a Fourier series. In:(C.J. Ralph and J.M. Scott, eds.) Estimating the number of ter-restrial birds. Studies in Avian Biology 6. Cooper OrnithologicalSociety, Las Cruces. pp. 466–482.
Can, O.E. and I. Togan. 2009. Camera trapping of large mammals˙
in Yenice Forest, Turkey: local information versus camera traps.Oryx. 43: 427–430.
Carbone, C., S. Christie, K. Conforti, T. Coulson, N. Franklin, J.R.Ginsberg, M. Griffiths, J. Holden, K. Kawanishi, R. Laidlaw,A. Lynam, D.W. Macdonald, D. Martyr, C. McDougal, L. Nath,T. O’Brien, D. Seindensticker, J.L. Smith, M. Sunquist, R. Tilsonand W.N. Wan Shahruddin. 2001. The use of photographic ratesto estimate densities of tigers and other cryptic mammals. Ani-mal Conserv. 4: 75–79.
Chauhan, D.S. and S.P. Goyal. 2001. A study on distribution, rela-tive abundance and food habits of leopard (Panthera pardus) ingarhwal Himalayas, Technical report, Wildlife Institute of India.
Chauhan, A.S., N. Pradhan and D. Maity. 2003. Plant diversity ofthe Kangchendzonga Biosphere Reserve in Sikkim Himalaya.Himalayan Biosphere Reserves. Biannual Bull. 5: 21–31.
Chettri, N. 2000. Checklist of birds of Khecheopalri and Yuksam-Dzongri trekking corridor, Khangchendzonga BiosphereReserve, West Sikkim, India. Himalayan Biosphere Reserves. 2:53–62.
Chettri, S.K., K.K. Singh and A.P. Krishna. 2006. Anthropogenicpressure on the natural resources in fringe areas of the Khang-chendzonga Biosphere Reserve. Int. J. Ecol. Environ. Sci. 32:229–240.
Chettri, B., S. Bhupathy and B.K. Acharya. 2010. Distribution pat-tern of reptiles along an eastern Himalayan elevation gradient,India. Acta Oecol. 36: 16–22.
Chundawat, R.S. 1992. Ecological studies on snow leopard and itsassociated species in Hemis National Park, Ladakh. Ph.D. thesis,University of Rajastan, Jaipur. pp. 166.
Cutler, T.L. and D.E. Swann. 1999. Using remote photography inwildlife ecology: a review. Wildl. Soc. Bull. 27: 571–581.
Dar, N.I., R.A. Minhas and M. Zaman Linkie. 2009. Predicting thepatterns, perceptions and causes of human-carnivore conflict inand around Machiara National Park, Pakistan. Biol. Conserv.142: 2076–2082.
Foster, M.L. and S.R. Humphrey. 1995. Use of highway underpassesby Florida panthers and other wildlife. Wildl. Soc. Bull. 23:95–100.
Fox, J., P. Yonzon and N. Podger. 1996. Mapping conflicts betweenbiodiversity and human needs in Langtang National Park, Nepal.Conserv. Biol. 10: 562–569.
Green, M.J.B. 1978. The ecology and feeding behaviour of theHimalayan tahr (Hemitragus jemlahicus) in the Langtang Valley,Nepal. M.Sc. Dissertation, University of Durham, UK.
Haribal, M. 1992. The butterflies of Sikkim Himalaya and theirnatural history. Gangtok, Sikkim Nature Conservation Foundation.
IUCN. 2010. IUCN Red List of Threatened Species. Version 2010.2.-www.iucnredlist.org).
Jackson, R.M., J.D. Roe, R. Wangchuk and D.O. Hunter. 2006. Esti-mating snow leopard population abundance using photographyand capture-recapture techniques. Wildl. Soc. Bull. 34: 772–781.
Karanth, K.U. 1995. Estimating tiger (Panthera tigris) populationsfrom camera trapping data using capture-recapture models. Biol.Conserv. 71: 333–338.
Karanth, K.U. and J.D. Nichols. 1998. Estimation of tiger densitiesin India using photographic captures and recaptures. Ecology 79:2852–2862.
Kinnaird, M.F., E.W. Sanderson, T.G. O’Brien, H.T. Wibisono andG. Woolmer. 2003. Deforestation trends in a tropical landscapeand implications for endangered large mammals. Conserv. Biol.17: 245–257.
Krishna, A.P., S. Chettri and E. Sharma. 2002. Human dimensionsof conservation in the Khangchendzonga Biosphere Reserve: theneed for conflict prevention. Mountain Res. Develop. 22:328–331.
Mace, R.D., S.C. Minta, T.L. Manley and K.A. Aune. 1994. Esti-mating grizzly bear population size using camera sightings.Wildl. Soc. Bull. 22: 74–83.
Mackenzie, D.I. and A. Royle. 2005. Designing occupancy studies:general advice and allocating survey effort. J. Appl. Ecol. 42:1105–1114.
Mani, M.S. 1974. Biogeography of the Himalaya. In: (M.S. Mani,and W. Junk, eds.) Ecology and biogeography in India. B.V.Publishers, The Hague, The Netherlands.
Marsh, D.M. and P.C. Trenham. 2008. Current trends in plant andanimal population monitoring. Conserv. Biol. 22: 647–655.
Menon, V. 2003. A field guide to Indian mammals. Dorling Kin-dersley (India), Penguin Books India, Delhi, India.
Mishra, C., M.D. Madhusudanand and A. Datta. 2006. Mammals ofthe high altitudes of western Arunachal Pradesh, Eastern Hima-laya: an assessment of threats and conservation needs. Oryx. 40:29–35.
AUTHOR’S COPY | AUTORENEXEMPLAR
AUTHOR’S COPY | AUTORENEXEMPLAR
268 S. Sathyakumar et al.: Mammals of Khangchendzonga Biosphere Reserve, India
Article in press - uncorrected proof
Myers, N., R.A. Mittermier, C.G. Mittermier, G.A.B. da Fonsecaand J. Kent. 2000. Biodiversity hotspots for conservation pri-orities. Nature 40: 853–858.
O’Brien, T.G., M.F. Kinnaird and H.T. Wibisono. 2003. Crouchingtigers, hidden prey: sumatran tiger and prey populations in atropical forest landscape. Animal Conserv. 6: 131–139.
Olson, D. and E. Dinerstein. 1998. The Global 200. A representationapproach to conserving the Earth’s most biologically valuableecoregions. Conserv. Biol. 12: 502–515.
Pei, J.Q. 1998. An evaluation of using auto-trigger cameras to rec-ord activity patterns of wild animals. Taiwan J. Forest Sci. 13:317–324.
Pereira, H.M. and H.D. Cooper. 2006. Towards the global monitor-ing of biodiversity change. Trends Ecol. Evol. 21: 123–129.
Prater, S.H. 1971. The book of Indian animals. Bombay NaturalHistory Society, Oxford University Press, Oxford, UK. pp. 324.
Rodgers, W.A., H.S. Panwar and V.B. Mathur. 2000. Wildlife pro-tected area network in India: a review. Wildlife Institute of India,Dehradun.
Rovero, F., T. Jones and J. Sanderson. 2005. Notes on Abbott’sduiker (Cephalophus spadix True 1890) and other forest ante-lopes of Mwanihana Forest, Udzungwa Mountains, Tanzania, asrevealed from camera-trapping and direct observations. Trop.Zool. 18: 13–23.
Rowcliffe, J.M., J. Field, S.T. Turvey and C. Carbone. 2008. Esti-mating animal density using camera traps without the need forindividual recognition. J. Appl. Ecol. 45: 1228–1236.
Sathyakumar, S. 1994. Habitat ecology of major ungulates in Kedar-nath musk deer sanctuary, western Himalaya. Ph.D. thesis, Sau-rashtra University, Rajkot, India. pp. 242.
Sathyakumar, S. 2004. Conservation status of mammals and birdsin Nanda Devi National Park: an assessment of changes overtwo decades (IN) Biodiversity Monitoring Expedition NandaDevi 2003. Uttaranchal State Forest Department, Dehradun,India. pp. 1–14.
Sathyakumar, S., T. Bhattacharya, T. Bashir, K. Poudyal and U.Lachungpa. 2009. Developing spatial database on the mammaldistributions and monitoring programme for large carnivores,prey populations and their habitats in Khangchendzonga Bio-sphere Reserve, Sikkim. Interim Report (February 2008–July2009). Wildlife Institute of India, Dehradun, India. pp. 79.
Sheng, L., W. Dajun, G. Xiaodong, J. William and W.J. Mc Shea.2010. Beyond pandas, the need for a standardized monitoringprotocol for large mammals in Chinese nature reserves. Biodiv.Conserv. 19: 3195–3206.
Silveira, L., T.A. Jacomo Anah and J.A.F. Diniz-Filho. 2003. Cam-era trap, line transect census and track surveys: a comparativeevaluation. Biol. Conserv. 114: 351–355.
Singh, H.B. 2004. Grazing impact on plant diversity and productiv-ity along a tourist trekking corridor in the KhangchendzongaBiosphere Reserve of Sikkim, Ph.D. Thesis. G.B. Pant Instituteof Himalayan Environment and Development, Northeast Unit,Itanagar, Arunachal Pradesh, India.
Swann, D.E., C.C. Hass, D.C. Dalton and S.A. Wolf. 2004. Infrared-triggered cameras for detecting wildlife: an evaluation andreview. Wildl. Soc. Bull. 32: 357–365.
Tambe, S. 2007. Alpine vegetation ecology and livestock grazingin Khangchendzonga National Park, Sikkim. Ph.D. Thesis, FRIUniversity, Dehradun. pp. 232.
Tambe, S. and G.S. Rawat. 2010. The alpine vegetation of theKhangchendzonga landscape, Sikkim Himalaya. Communitycharacteristics, diversity, and aspects of ecology. Mountain Res.Develop. 30: 266–274.
Vinod, T.R. and S. Sathyakumar. 1999. Ecology and conservationof mountain ungulates in great Himalayan national park, westernHimalaya, Final Report (FREEP-GHNP). Vol. 3. Wildlife Insti-tute of India, Dehradun, India.
Whitefield, J. 1998. A saola poses for the camera. Nature 396:410.
AUTHOR’S COPY | AUTORENEXEMPLAR
AUTHOR’S COPY | AUTORENEXEMPLAR