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Hindawi Publishing CorporationInternational Journal of BiodiversityVolume 2013 Article ID 370905 8 pageshttpdxdoiorg1011552013370905

Research ArticleA Communal Sign Post of Snow Leopards (Panthera uncia) andOther Species on the Tibetan Plateau China

Juan Li1 George B Schaller2 ThomasMMcCarthy3 DajunWang1

Zhala Jiagong4 Ping Cai5 Lamao Basang6 and Zhi Lu1 4

1 Center for Nature and Society College of Life Sciences Peking University Beijing 100871 China2 Panthera and Wildlife Conservation Society 8 West 40th Street 18th Floor New York NY 10018 USA3 Snow Leopard Program Panthera 8 West 40th Street 18th Floor New York NY 10018 USA4 Shan Shui Conservation Center Beijing 100871 China5Wildlife Conservation and Management Bureau Qinghai Forestry Department Xining 810008 Qinghai China6 Sanjiangyuan National Nature Reserve Qinghai Forestry Department Xining 810008 Qinghai China

Correspondence should be addressed to Juan Li lijuan924gmailcom

Received 29 September 2012 Accepted 13 November 2012

Academic Editor Rafael Riosmena-Rodriacuteguez

Copyright copy 2013 Juan Li et al is is an open access article distributed under the Creative Commons Attribution License whichpermits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

e snow leopard is a keystone species in mountain ecosystems of Central Asia and the Tibetan Plateau However little is knownabout the interactions between snow leopards and sympatric carnivores Using infrared cameras we found a rocky junction of twovalleys in Sanjiangyuan area on the Tibetan Plateau where many mammals in this area passed and frequently marked and sniffedthe site at the junction We suggest that this site serves as a sign post to many species in this area especially snow leopards andother carnivores e marked signs may also alert the animals passing by to temporally segregate their activities to avoid potentialconictsWe used the Schoener index tomeasure the degree of temporal segregation among the species captured by infrared cameratraps at this site Our research reveals the probable ways of both intra- and interspecies communication and demonstrates that thedegree of temporal segregationmay correlate with the degree of potential interspecies competitionis is an important message tohelp understand the structure of animal communities Discovery of the sign post claries the importance of identifying key habitatsand sites of both snow leopards and other species for more effective conservation

1 Introduction

e snow leopard (Panthera uncia) an endangered specieslisted in IUCN Red List [1] occurs in remote and ruggedmountains across Central Asia and the Tibetan Plateau [2]As a keystone species this cat has an important role inthese mountain ecosystems [3] But with only an estimatedpopulation of 3500ndash7000 remaining the snow leopard gen-erally occurs at low densities Poaching retaliatory killingdue to livestock-snow leopard conict decimation of preyand habitat degradation have all contributed to its rarity [2]Most studies of snow leopard have focused on its habitat[4 5] and food habits [6ndash8] whereas little is known aboutthe interaction of snow leopards and their sympatric species

Olfactory and visual signals are known as crucial medi-ators for intraspecies communication Mammals especiallysolitary species use these signals to advertise reproductivestatus recognize sex identify individuals establish territoryand so on [9 10] Communal sign posts have for examplebeen found in snow leopard [11] giant panda (Ailuropodamelanoleuca) [12] and American black bear (Ursus amer-icanus) [13] habitats However previous studies did notdescribe interspecies interactions at such locations

In this study we discovered a site sniffed and markedby snow leopards and several other carnivores a sign postWhite et al (2003) used the term ldquobulletin boardrdquo to describesuch a site used by pandas [14] ere one animal leaves amessage (such as feces or urine) followed by another animal

2 International Journal of Biodiversity

which sees or smells this message Such communicationcould help different species avoid direct confrontation andmay lead to temporal segregation [15]

To identify the interaction between snow leopards andsympatric species we recorded the date time and corre-sponding behavior of the animals passing by this site withinfrared camera trapse analysis of these behaviors showedthat snow leopards and other carnivores frequently markedand sniffed at this site indicating the site functions as a signpost Our data also showed that the sympatric carnivoreswere temporally segregated in both annual and daily activitypatterns e degree of temporal segregation may be relatedto the degree of competition among the species

2 Materials andMethods

21 Study Area e eld study was conducted in SuojiaTownship in Yushu Prefecture (Figure 1) the core area of theSanjiangyuan National Nature Reserve Qinghai ProvinceChina is region has a high density of snow leopards[6 16] e climate is typically windy and dry e averageannual temperature is minus4∘C (range from minus12∘C to minus20∘C inJanuary and 8∘C to minus10∘C in July) and the average annualprecipitation is 150ndash420mm [17] Alpine meadow is themajor vegetation type consisting of mainly a layer up to30 cm thick of turf densely covered with sedge (Kobresiaspp) In addition to the snow leopard the main mammalspecies in this area include the gray wolf (Canis lupus)the Tibetan brown bear (Ursus arctos) the Eurasian lynx(Lynx lynx) the red fox (Vulpes vulpes) the Tibetan fox(Vulpes ferrilata) Pallasrsquos cat (Otocolobus manul) the stonemarten (Martes foina) the blue sheep (Pseudois nayaur)the Himalayan marmot (Marmota himalayana) the plateaupika (Ochotona curzoniae) the large-eared pika (Ochotonamacrotis) and various small rodents [17]

22 CameraTrapping From January 1 2011 toDecember 312011 one Reconyx (HC500 HyperFireTM) passive infraredcamera (Reconyx Inc USA) was installed 35 cm abovegroundbeside an overhanging rockwith several snow leopardscrapes and carnivore feces (site SJ001 in Figure 1) ecamera worked without delay between each consecutiveexposure Every time animals triggered the camera tencontinuous images were captured e camera was checkedabout every ten days to ensure the angle remained consistentand batteries were charged No bait or scent lure was usedIn the same way another 15 infrared cameras were placedat 15 sites from late April 2011 onward Unfortunately onlycameras on ve sites worked properly for around six monthsand these data are included here (site SJ002 SJ004 SJ008SJ010 and SJ012 in Figure 1) Other cameras were lost ordamaged

e behaviors of carnivores were divided into threecategories sniffing (receiving information) marking (send-ing information) and others Sniffing behavior was denedas smelling the ground or rock And the marking behav-ior included behaviors such as scraping cheek rubbingback rubbing spraying urinating or defecating Dogs were

included only when they were out on their own not whenthey followed people

23 Data Analysis Camera trap data are usually analyzed bygrouping detections occurring within ten or thirty minutesinto one capture [18 19] However this method has twoaws e rst aw is that the time frame used to group thedetections is articial Neither tenminutes nor thirtyminuteshas a clear biological explanation e second aw is thatgrouping detections occurring within a period of time intoone capture decrease data accuracy a method less suitablefor analysis of daily activity patterns erefore we dene asingle capture as one individual (including every individualwithin a group) passing by the camera once To build the dailyactivity curves we averaged the number of captures withinthe adjacent two hours as the number of captures for eachspecies For example the capture number at 300 is the 2-hour average of captures from 200 to 359 e annual anddaily overlap indexes between two species were calculatedaccording to the formula of Schoener [20]

To summarize we used the following formulas in ourstudy

(1) Activity index of time point119860119860 = (captures at this timepoint)(captures at the whole time frame)

(2) Capture = sum119899119899119894119894119894119894 Individuals (119899119899 = number of timesanimal passes by the camera)

(3)

120572120572119894119894119894119894 119894 119894 minus1198942

1198991198991005576100557611988611988611989411989410092501009250119901119901119894119894119886119886 minus 11990111990111989411989411988611988610092501009250 (1)

where 120572120572119894119894119894119894 is the overlap index of temporal nichebetween species 119894119894 and species 119894119894 119901119901119894119894119886119886 and 119901119901119894119894119886119886 are theproportions of 119886119886th month (for annual overlap index)or hour (for daily overlap index) used by species 119894119894 andspecies 119894119894 respectively

(4) Total overlap index = Annual overlap index times Dailyoverlap index

We employed the soware 119877119877 to do hierarchical clusteranalysis of the pairwise total overlap index with averagelinkage method and generated a cluster dendrogram [21]

We did not include marmot pika and stone marten inthese analyses because they were too small for our camera todetect with its 35 cmheight above ground or too infrequentlyrecorded for analysis

3 Results

31 Camera Trap Captures In 365 trap days from January 12011 through December 31 2011 we obtained 485 capturesof carnivores and 1100 captures of herbivores at the site SJ001(Figure 1) including snow leopards (145 captures) graywolves (106) domestic dogs (73) brown bears (14) red foxes(81) Tibetan foxes (44) Pallasrsquos cats (16) stone martens (6)blue sheep (891) and livestock (209) (Table 1 Figure 2) Snowleopards were the most frequently photographed carnivores

International Journal of Biodiversity 3

SJ001

SJ012

SJ010

SJ008

SJ004

SJ002

5 other sitesRoadRiver

Elevation value

High 5857Low 4163

ChinaRiverBeijing cityStudy area

0 6 123

(km)

3400N

3400N

9400E

N

9400E

ldquoSign postrdquo

F 1 Locations of camera traps in Suojia Township in Yushu Prefecture Qinghai Province China

145

106

73

14

81

44

166

44 4230

12

2816

2 2

86

5 3 7 113 1 0

0

20

40

60

80

100

120

140

160

Sno

wle

op

ard

Do

mes

tic

do

g

Bro

wn

bea

r

Red

fo

x

Tib

etan

fox

Pal

lasrsquo

s ca

t

Sto

ne

mar

ten

Nu

mb

ers

Species

Capture

Sniffing

Marking

Gra

y w

olf

F 2 Camera trap captures of each carnivore species withsniffing and marking behaviors on the communal sign post

and we identied six adults and one cub As for sympatriccarnivores no fewer than ve brown bears and six wolveswere identied We were unable to discriminate between theindividuals of red foxes (including one young) or Tibetanfoxes e species photographed represented almost all thecarnivores found in this area except the lynx and other smallmustelidse captures of camera traps from 5 other sites willbe used for comparison in discussion section

32 Behavior Most carnivores did not just pass by the siteSJ001 but spent time sniffing and marking it (Table 1 Figure

2) Snow leopards marked most actively doing so in 86 out of145 captures Wolves marked approximately ten meters fromthis camera but from October to December they began tomark the ground near by it Dogs also sniffed here frequentlyBrown bears sniffed this site almost every time they passedand oen rubbed their back Red and Tibetan foxes bothseemed to prefer to sniff more than to mark

33 Activity Patterns Among the large carnivores snowleopards visited this site (SJ001) throughout the year theirannual activity curve peaking in February (Figure 3(a)) Incontrast brown bears occurred mainly in May and Octoberand wolves appeared to be most active at this site in Februaryand October Domestic dogs showed a peak in winter (Figure3(a)) As for daily activity patterns snow leopards were activeat this site throughout the night with a slightly crepusculartrend Wolves passed by at noon and dusk whereas brownbears only appeared at the rock before dawn (Figure 3(b))

Among the small carnivores the annual activity patternof Tibetan foxes was very similar to that of brown bears whilered foxes passed by throughout the year (Figure 4(a)) Dailypatterns showed that red foxes typically visited only at nightwhereas Tibetan foxes and Pallasrsquos cats came here throughoutthe day (Figure 4(b))

e herbivores photographed at this site were livestock(only domestic yaks at this site) and blue sheep Livestockpassed by this site aer 800AMand returned before 200 PMtheir activity pattern depending on the herders (Figure 5(a))Blue sheep appeared to avoid livestock by appearing at thissite before 1000 AM and aer 200 PM but never at night(Figure 5(b))


T 1 Numbers of captures sniffing and marking behavior of each species captured by camera trapping at the communal sign post

Group English name Latin name IUCN1 CN2 Capture Sniffing Marking

Large carnivores

Snow leopard Panthera uncia EN I 145 44 86Gray wolf Canis lupus LC II 106 42 5

Domestic dog Canis lupus 73 30 3Brown bear Ursus arctos LC II 14 12 7

Small carnivores

Red fox Vulpes vulpes LC mdash 81 28 11Tibetan fox Vulpes ferrilata LC mdash 44 16 3Pallasrsquos cat Otocolobus manul NT II 16 2 1

Stone marten Martes foina LC II 6 2 0

Herbivores Blue sheep Pseudois nayaur LC II 891 NA NADomestic yak Bos mutus 209 NA NA

1IUCN endangered species category (Red List) EN endangered NT near threatened LC least concern

2Category of protected wildlife species under Chinarsquos Wildlife Protection Law mdash means not listed

05

06

07

1 2 3 4 5 6 7 8 9 10 11 12

Month

Snow leopard

Gray wolf

Domestic dog

Brown bear

Act

ivit

y in

dex

0

01

02

03

04

(a)

0 2 4 6 8 10 12 14 16 18 20 22 24

Time (h)

Snow leopard

Gray wolf

Domestic dog

Brown bear

Act

ivit

y in

dex

0

01

02

03

04

(b)

F 3 (a) Annual activity patterns and (b) daily activity patterns of large carnivores on the communal sign post Snow leopard (119899119899 119899 119899119899119899)gray wolf (119899119899 119899 119899119899119899) domestic dog (119899119899 119899 119899119899) and brown bear (119899119899 119899 119899119899) are included

4 Discussion

41 Sign Post Compared with the captures of 5 other cam-eras placed nearby (Figure 1) the number of snow leopardscaptured at site SJ001 was much greater (see in Table 2) isdifference indicates that this site had special relevance forintraspecies communication in this area Additionally thediversity of carnivore species photographed was the highestimplying that this site might also serve as a focal point forinterspecies communication (see in Table 2) Previous studieshave showed that mammals select conspicuous objects atmajor traffic hubs to communicate with each other Forexample snow leopards prefer to mark at mountain passescliff bases conuence of rivers and other conspicuous places[4 22] Brown bears tend to mark along travel routes [23]whereas wolves prefer crossroads [24 25] is site is locatedat a juncture of two major valleys with an overhanging rockat the base of a cliff Animals traveling along these valleyspass by here and the rock is at an appropriate height for

depositing scent and rubbing Whereas other 5 sites are notlocated at crossroads erefore it is not surprising that thissite is favored by so many carnivore species and serves as acommunal sign post

42 Temporal Segregation Many mammals shared this signpost especially the carnivores which sniffed and marked itfrequently In addition carnivores prey on herbivores andthey also prey on each other and age size and patterns ofgrouping largely determine the outcome of such interactions[26 27] Temporal segregation is an important mechanismfor these species to coexist and avoid direct confrontation[28] To understand this temporal segregation we rstanalyzed the probable factors affecting annual and dailyactivity patterns of the different species and then combinedthe pairwise annual and daily overlap indexes into a clusterdendrogram to show their interrelationship


05

06

07

1 2 3 4 5 6 7 8 9 10 11 12

Act

ivit

y in

dex

Month

Snow leopard

Red fox

Tibetan fox

Pallasrsquos cat

0

01

02

03

04

(a)

0 2 4 6 8 10 12 14 16 18 20 22 24

Act

ivit

y in

dex

Time (h)

Snow leopard

Red fox

Tibetan fox

Pallasrsquos cat

0

01

02

03

04

(b)

F 4 (a) Annual activity patterns and (b) daily activity patterns of snow leopard (119899119899 119899 119899119899119899) and small carnivores on the communal signpost Red fox (119899119899 119899 119899119899) Tibetan fox (119899119899 119899 119899119899) and Pallasrsquos cat (119899119899 119899 119899119899) are included

0

01

02

03

04

05

06

07

1 2 3 4 5 6 7 8 9 10 11 12

Act

ivit

y in

dex

Month

Snow leopard

Blue sheep

Domestic yak

(a)

0

01

02

03

04

0 2 4 6 8 10 12 14 16 18 20 22 24

Act

ivit

y in

dex

Time (h)

Snow leopard

Blue sheep

Domestic yak

(b)

F 5 (a) Annual activity patterns and (b) daily activity patterns of the snow leopard (119899119899 119899 119899119899119899) and herbivores on the communal signpost Blue sheep (119899119899 119899 119899119899119899) and livestock (119899119899 119899 119899119899119899) are included

Annual activity patterns are to a large extent determinedby the natural cycles and somewhat different habitat prefer-ences of species Snow leopards for example remain in steeprocky terrains the whole year but they are slightlymore activein the Februarymating seasonwhen theymay roamwidely tond a mate Wolves prefer to live in less precipitous terrains[29]e activity peak in Februarymay be due to theirmatingseason but we have no explanation for the October oneBears apparently mate mainly inMay and June and hibernatefrom about late October to early March according to ourpreliminary data We found several caves in which bears hadhibernated near this communal sign post Brown bears are

said to be much more active before hibernation to lay on fat[30] Consequently the annual activity curve of these bearsshows peaks in May and in October

Compared to annual activity patterns the daily onesappeared to be more exible Affected by various factorsamong them hunting and other human activities animalsmay become more nocturnal or seek different habitats einteractions among the various species may also affect it Tobe specic the snow leopard is active mainly at night andits prey the blue sheep which is active around this site onlyduring the day showed a conspicuous difference of theiractivity patterns Wolves tend to be nocturnal with activity


Liv

esto

ck

Blu

e sh

eep

Bro

wn

bea

r

Sno

w l

eop

ard

Red

fo

x

Tib

etan

fo

x

Pal

lasrsquo

s ca

t

Gra

y w

olf

Do

mes

tic

do

g

05

06

07

08

09

Cluster dendrogram

Hei

ght

F 6 Cluster analysis dendrogram of pairwise total overlap indexes It shows the interrelationship of the nine speciesrsquo activity patternsat the communal sign post Height represents the distance linkage between clusters

T 2 Number of captures of each species on six sites fromMay 1 to October 31 2011

Group Species SJ0011 SJ002 SJ004 SJ0082 SJ010 SJ012

Large carnivores

Snow leopard 49 14 8 6 7 36Gray wolf 17 2 0 0 0 1

Domestic dog 4 0 0 1 0 0Brown bear 9 0 0 0 3 1

Small carnivores

Red fox 41 5 14 46 7 2Tibetan fox 25 8 0 0 0 0Pallasrsquos cat 8 25 7 9 2 1

Stone marten 2 0 1 2 0 0

Herbivores Blue sheep 677 188 365 242 10 69Livestock 28 81 46 184 0 0

Total 860 323 441 490 29 1101e communal sign post

2e camera did not work from July 28 to August 9 because batteries were dead

levels peaking at dawn and dusk in other areas [31 32]whereas their activity patterns were diurnal at the communalsign postis could be due to avoidance between wolves andsnow leopards causing one species shi its activity patterninto an opposite phase [28] Brown bears only passed by thissite at night with peaks at 2300 and 500 as shown in our fewrecords We found that bears would follow snow leopards toscavenge on their kills and this is perhaps one reason theirdaily activity patterns are similar

To measure the degree of temporal segregation betweenany two species at this communal sign post we introducedthe total overlap index (see Section 2) which represents theoverall effect of annual and daily temporal segregation e

dendrogram concisely shows the result of hierarchical clus-tering of the complex pairwise total overlap indexes (Figure6) e species within the same group tend to have similaractivity patterns As shown in Figure 6 the nine species wereclustered into 3 large branches namely livestock blue sheepand the carnivores As expected herbivores avoid predationby large carnivores by staggering their presence at this siteen there are two apparent clusters under the carnivorebranch one composed of brown bears Pallasrsquos cats snowleopards and the two fox species and the other of graywolvesand domestic dogs Wolves occasionally kill dogs but theywere clustered together e three main large carnivoresthose with the greatest potential conictsnow leopard


wolf and brown bearmdashwere grouped into different clustersshowing that they might have developed a mechanism toavoid conicts especially the wolf and the snow leopardus the degree of segregation may relate to the position ofspecies in the food chain from herbivores small carnivoresto large carnivores as well as to body size

5 Conclusions

In summary using camera traps we identied an impor-tant marking site or sign post used by snow leopardsand several sympatric species for intra- and interspeciescommunication We introduced the Schoener index andclustering dendrogram to measure and represent the degreeof temporal segregation between species photographed andfound that they were temporally segregated more or less atthis location presumably to avoid direct confrontations Sucha communal sign post provided preliminary knowledge ofthe ner-scaled habitat use of snow leopards and of nichesegregation between species an important consideration forprotecting key habitats of snow leopards and other sympatricmammals Future research could locate and investigate othersuch sites in order to learn how intraspecies and interspeciescommunications are conducted as well as understandingthe community structures and role of snow leopards in theecosystem

Conict of nterest

We certify that there is no conict of interest in this paper

Acknowledgments

is study was a preliminary effort of a larger snow leopardresearch and conservation project jointly conducted byQing-hai Forestry Department Shan Shui Conservation Centerthe Center for Nature and Society of Peking Universityand the Panthera and the Snow Leopard Trust e authorsthank Tudengzhaxi Angye Nangcaicicheng NaobowendingBairang and others from Sub-Gongsa Monastery and LanWu Lingyun Xiao andMeiqi Liu from Peking University fortheir assistance in the eld work Others contributed to theproject among them Hang Yin Haiyuan Ma Dawajiangcaiand Zhaxiduojie ey also extend their special appreciationto Sandan Li Li Zhang Yu Zhang of the Qinghai ForestryDepartment and Ruofan Li Renzeng and others from Qing-hai Sanjiangyuan Nature Reserve

References

[1] R M Jackson D Mallon T McCarthy R A Chundaway andB Habib ldquoPanthera unciardquo in IUCN 2011 IUCN Red List ofreatened Species Version 2011 2 2008

[2] T M McCarthy and G Chapron Snow Leopard SurvivalStrategy ISLT and SLN Seattle Wash USA 2003

[3] Y V Bhatnagar V B Mathur and T McCarthy ldquoA regionalperspective for snow leopard conservation in the Indian Trans-Himalayardquo in Contributed Papers to the Snow Leopard Survival

Strategy Summit T McCarthy and J Weltzin Eds pp 25ndash47International Snow Leopard Trust Seattle Wash USA 2002

[4] RM Jackson andGAhlborn ldquoA preliminary habitat suitabilitymodel for the snow leopard (Panthera uncia)rdquo in InternationalPedigree Book of Snow Leopards vol 4 pp 43ndash52 1984

[5] MWolf and SAle ldquoSigns at the top habitat features inuencingsnow leopardUncia uncia activity in sagarmatha national parknepalrdquo Journal of Mammalogy vol 90 no 3 pp 604ndash611 2009

[6] G B Schaller R Junrang and Q Mingjiang ldquoStatus of thesnow Leopard Panthera uncia in Qinghai and Gansu ProvincesChinardquo Biological Conservation vol 45 no 3 pp 179ndash1941988

[7] S Bagchi and C Mishra ldquoLiving with large carnivores preda-tion on livestock by the snow leopard (Uncia uncia)rdquo Journal ofZoology vol 268 no 3 pp 217ndash224 2006

[8] T Sangay and K Vernes ldquoHuman-wildlife conict in theKingdom of Bhutan patterns of livestock predation by largemammalian carnivoresrdquo Biological Conservation vol 141 no5 pp 1272ndash1282 2008

[9] K Rails ldquoMammalian scent markingrdquo Science vol 171 no3970 pp 443ndash449 1971

[10] J F Eisenberg and D G Kleiman ldquoOlfactory communicationin mammalsrdquo Annual Review of Ecology and Systematics vol 3pp 1ndash32 1972

[11] R M Jackson Home range movements and habitat use of snowLeopard (Uncia uncia) in Nepal [PhD thesis] University ofLondon London UK 1996

[12] R R Swaisgood D G Lindburg A M White Z Heminand Z Xiaoping ldquoChemical communication in giant pandasexperimentation and applicationrdquo in Giant Pandas Biologyand Conservation D G Lindburg and K Baronga Eds pp106ndash120 Oxford University Press Oxford UK 2004

[13] T L Burst ldquoBlack bear mark trees in the Smoky Mountainsrdquoin Proceedings of the International Conference on Bear Researchand Management vol 5 pp 45ndash53 1983

[14] A M White R R Swaisgood and H Zhang ldquoChemicalcommunication in the giant panda (Ailuropoda melanoleuca)the role of age in the signaller and assessorrdquo Journal of Zoologyvol 259 no 2 pp 171ndash178 2003

[15] T W Schoener ldquoResource partitioning in ecological commu-nitiesrdquo Science vol 185 no 4145 pp 27ndash39 1974

[16] Y Liao ldquoe geographical distribution of ounces in QinghaiProvincerdquo Acta eriologica Sinica vol 5 pp 183ndash188 1985

[17] D P Mallon ldquoResearch survey and biodiversity planning onthe Tibet-Qinghai Plateau Chinardquo Final Report For DarwinInitiative For the Survival of Species 2004

[18] S Li W J Mcshea D Wang L Shao and X Shi ldquoe use ofinfrared-triggered cameras for surveying phasianids in SichuanProvince Chinardquo Ibis vol 152 no 2 pp 299ndash309 2010

[19] T G OrsquoBrien M F Kinnaird and H T Wibisono ldquoCrouchingtigers hidden prey Sumatran tiger and prey populations in atropical forest landscaperdquoAnimal Conservation vol 6 no 2 pp131ndash139 2003

[20] T W Schoener ldquoe Anolis lizards of Bimini resource parti-tioning in a complex faunardquo Ecology vol 49 pp 704ndash726 1968

[21] R Development Core Team R A language and Environment forStatistical Computing R Foundation for Statistical ComputingVienna Austria 2011

[22] G B SchallerMountain Monarchs Wild Sheep and Goats of theHimalaya University of Chicago Press Chicago Ill USA 1977


[23] G I Green and D J Mattson ldquoTree rubbing by yellowstonegrizzly bearsUrsus arctosrdquoWildlife Biology vol 9 no 1 pp 1ndash92003

[24] R P Peters ldquoScent-marking in wolves radio-tracking of wolfpacks has provided denite evidence that olfactory sign is usedfor territory maintenance and may serve for other forms ofcommunication within the pack as wellrdquo American Scientistvol 63 pp 628ndash637 1975

[25] I Barja F J De Miguel and F Baacutercena ldquoe importance ofcrossroads in faecal marking behaviour of the wolves (Canislupus)rdquoNaturwissenschaen vol 91 no 10 pp 489ndash492 2004

[26] G A Polis C A Myers and R D Holt ldquoe ecology andevolution of intraguild predation potential competitors that eateach otherrdquoAnnual review of ecology and systematics vol 20 pp297ndash330 1989

[27] F Palomares and T M Caro ldquoInterspecic killing amongmammalian carnivoresrdquo American Naturalist vol 153 no 5pp 492ndash508 1999

[28] N Kronfeld-Schor and T Dayan ldquoPartitioning of time as anecological resourcerdquo Annual Review of Ecology Evolution andSystematics vol 34 pp 153ndash181 2003

[29] L D Mech and L Boitani Wolves Behavior Ecology andConservation University of Chicago Press Chicago Ill USA2003

[30] J Naves A Fernaacutendez-Gil C Rodrigraveguez and M DelibesldquoBrown bear food habits at the border of its range a long-termstudyrdquo Journal of Mammalogy vol 87 no 5 pp 899ndash908 2006

[31] S B Merrill and L David Mech ldquoe usefulness of GPStelemetry to study wolf circadian and social activityrdquo WildlifeSociety Bulletin vol 31 no 4 pp 947ndash960 2003

[32] M Unit ldquoDaily patterns and duration of wolf activity in theBialowieza forest Polandrdquo Journal of Mammalogy vol 84 pp243ndash253 2003

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which sees or smells this message Such communicationcould help different species avoid direct confrontation andmay lead to temporal segregation [15]

To identify the interaction between snow leopards andsympatric species we recorded the date time and corre-sponding behavior of the animals passing by this site withinfrared camera trapse analysis of these behaviors showedthat snow leopards and other carnivores frequently markedand sniffed at this site indicating the site functions as a signpost Our data also showed that the sympatric carnivoreswere temporally segregated in both annual and daily activitypatterns e degree of temporal segregation may be relatedto the degree of competition among the species

2 Materials andMethods

21 Study Area e eld study was conducted in SuojiaTownship in Yushu Prefecture (Figure 1) the core area of theSanjiangyuan National Nature Reserve Qinghai ProvinceChina is region has a high density of snow leopards[6 16] e climate is typically windy and dry e averageannual temperature is minus4∘C (range from minus12∘C to minus20∘C inJanuary and 8∘C to minus10∘C in July) and the average annualprecipitation is 150ndash420mm [17] Alpine meadow is themajor vegetation type consisting of mainly a layer up to30 cm thick of turf densely covered with sedge (Kobresiaspp) In addition to the snow leopard the main mammalspecies in this area include the gray wolf (Canis lupus)the Tibetan brown bear (Ursus arctos) the Eurasian lynx(Lynx lynx) the red fox (Vulpes vulpes) the Tibetan fox(Vulpes ferrilata) Pallasrsquos cat (Otocolobus manul) the stonemarten (Martes foina) the blue sheep (Pseudois nayaur)the Himalayan marmot (Marmota himalayana) the plateaupika (Ochotona curzoniae) the large-eared pika (Ochotonamacrotis) and various small rodents [17]

22 CameraTrapping From January 1 2011 toDecember 312011 one Reconyx (HC500 HyperFireTM) passive infraredcamera (Reconyx Inc USA) was installed 35 cm abovegroundbeside an overhanging rockwith several snow leopardscrapes and carnivore feces (site SJ001 in Figure 1) ecamera worked without delay between each consecutiveexposure Every time animals triggered the camera tencontinuous images were captured e camera was checkedabout every ten days to ensure the angle remained consistentand batteries were charged No bait or scent lure was usedIn the same way another 15 infrared cameras were placedat 15 sites from late April 2011 onward Unfortunately onlycameras on ve sites worked properly for around six monthsand these data are included here (site SJ002 SJ004 SJ008SJ010 and SJ012 in Figure 1) Other cameras were lost ordamaged

e behaviors of carnivores were divided into threecategories sniffing (receiving information) marking (send-ing information) and others Sniffing behavior was denedas smelling the ground or rock And the marking behav-ior included behaviors such as scraping cheek rubbingback rubbing spraying urinating or defecating Dogs were

included only when they were out on their own not whenthey followed people

23 Data Analysis Camera trap data are usually analyzed bygrouping detections occurring within ten or thirty minutesinto one capture [18 19] However this method has twoaws e rst aw is that the time frame used to group thedetections is articial Neither tenminutes nor thirtyminuteshas a clear biological explanation e second aw is thatgrouping detections occurring within a period of time intoone capture decrease data accuracy a method less suitablefor analysis of daily activity patterns erefore we dene asingle capture as one individual (including every individualwithin a group) passing by the camera once To build the dailyactivity curves we averaged the number of captures withinthe adjacent two hours as the number of captures for eachspecies For example the capture number at 300 is the 2-hour average of captures from 200 to 359 e annual anddaily overlap indexes between two species were calculatedaccording to the formula of Schoener [20]

To summarize we used the following formulas in ourstudy

(1) Activity index of time point119860119860 = (captures at this timepoint)(captures at the whole time frame)

(2) Capture = sum119899119899119894119894119894119894 Individuals (119899119899 = number of timesanimal passes by the camera)

(3)

120572120572119894119894119894119894 119894 119894 minus1198942

1198991198991005576100557611988611988611989411989410092501009250119901119901119894119894119886119886 minus 11990111990111989411989411988611988610092501009250 (1)

where 120572120572119894119894119894119894 is the overlap index of temporal nichebetween species 119894119894 and species 119894119894 119901119901119894119894119886119886 and 119901119901119894119894119886119886 are theproportions of 119886119886th month (for annual overlap index)or hour (for daily overlap index) used by species 119894119894 andspecies 119894119894 respectively

(4) Total overlap index = Annual overlap index times Dailyoverlap index

We employed the soware 119877119877 to do hierarchical clusteranalysis of the pairwise total overlap index with averagelinkage method and generated a cluster dendrogram [21]

We did not include marmot pika and stone marten inthese analyses because they were too small for our camera todetect with its 35 cmheight above ground or too infrequentlyrecorded for analysis

3 Results

31 Camera Trap Captures In 365 trap days from January 12011 through December 31 2011 we obtained 485 capturesof carnivores and 1100 captures of herbivores at the site SJ001(Figure 1) including snow leopards (145 captures) graywolves (106) domestic dogs (73) brown bears (14) red foxes(81) Tibetan foxes (44) Pallasrsquos cats (16) stone martens (6)blue sheep (891) and livestock (209) (Table 1 Figure 2) Snowleopards were the most frequently photographed carnivores


SJ001

SJ012

SJ010

SJ008

SJ004

SJ002


Elevation value

High 5857Low 4163


0 6 123

(km)

3400N

3400N

9400E

N

9400E

ldquoSign postrdquo


145

106

73

14

81

44

166

44 4230

12

2816

2 2

86

5 3 7 113 1 0

0

20

40

60

80

100

120

140

160

Sno

wle

op

ard

Do

mes

tic

do

g

Bro

wn

bea

r

Red

fo

x

Tib

etan

fox

Pal

lasrsquo

s ca

t

Sto

ne

mar

ten

Nu

mb

ers

Species

Capture

Sniffing

Marking

Gra

y w

olf











Large carnivores



Small carnivores






05

06

07

1 2 3 4 5 6 7 8 9 10 11 12

Month

Snow leopard

Gray wolf

Domestic dog

Brown bear

Act

ivit

y in

dex

0

01

02

03

04

(a)

0 2 4 6 8 10 12 14 16 18 20 22 24

Time (h)

Snow leopard

Gray wolf

Domestic dog

Brown bear

Act

ivit

y in

dex

0

01

02

03

04

(b)


4 Discussion





05

06

07

1 2 3 4 5 6 7 8 9 10 11 12

Act

ivit

y in

dex

Month

Snow leopard

Red fox

Tibetan fox

Pallasrsquos cat

0

01

02

03

04

(a)

0 2 4 6 8 10 12 14 16 18 20 22 24

Act

ivit

y in

dex

Time (h)

Snow leopard

Red fox

Tibetan fox

Pallasrsquos cat

0

01

02

03

04

(b)


0

01

02

03

04

05

06

07

1 2 3 4 5 6 7 8 9 10 11 12

Act

ivit

y in

dex

Month

Snow leopard

Blue sheep

Domestic yak

(a)

0

01

02

03

04

0 2 4 6 8 10 12 14 16 18 20 22 24

Act

ivit

y in

dex

Time (h)

Snow leopard

Blue sheep

Domestic yak

(b)






Liv

esto

ck

Blu

e sh

eep

Bro

wn

bea

r

Sno

w l

eop

ard

Red

fo

x

Tib

etan

fo

x

Pal

lasrsquo

s ca

t

Gra

y w

olf

Do

mes

tic

do

g

05

06

07

08

09

Cluster dendrogram

Hei

ght




Large carnivores



Small carnivores











5 Conclusions


Conict of nterest


Acknowledgments


References








































Volume 2013


ISRN Biotechnology




Volume 2013




Advances in

Virolog y

ISRN Microbiology






ISRN Zoology




ISRN Cell Biology







Enzyme Research








SJ001

SJ012

SJ010

SJ008

SJ004

SJ002


Elevation value

High 5857Low 4163


0 6 123

(km)

3400N

3400N

9400E

N

9400E

ldquoSign postrdquo


145

106

73

14

81

44

166

44 4230

12

2816

2 2

86

5 3 7 113 1 0

0

20

40

60

80

100

120

140

160

Sno

wle

op

ard

Do

mes

tic

do

g

Bro

wn

bea

r

Red

fo

x

Tib

etan

fox

Pal

lasrsquo

s ca

t

Sto

ne

mar

ten

Nu

mb

ers

Species

Capture

Sniffing

Marking

Gra

y w

olf











Large carnivores



Small carnivores






05

06

07

1 2 3 4 5 6 7 8 9 10 11 12

Month

Snow leopard

Gray wolf

Domestic dog

Brown bear

Act

ivit

y in

dex

0

01

02

03

04

(a)

0 2 4 6 8 10 12 14 16 18 20 22 24

Time (h)

Snow leopard

Gray wolf

Domestic dog

Brown bear

Act

ivit

y in

dex

0

01

02

03

04

(b)


4 Discussion





05

06

07

1 2 3 4 5 6 7 8 9 10 11 12

Act

ivit

y in

dex

Month

Snow leopard

Red fox

Tibetan fox

Pallasrsquos cat

0

01

02

03

04

(a)

0 2 4 6 8 10 12 14 16 18 20 22 24

Act

ivit

y in

dex

Time (h)

Snow leopard

Red fox

Tibetan fox

Pallasrsquos cat

0

01

02

03

04

(b)


0

01

02

03

04

05

06

07

1 2 3 4 5 6 7 8 9 10 11 12

Act

ivit

y in

dex

Month

Snow leopard

Blue sheep

Domestic yak

(a)

0

01

02

03

04

0 2 4 6 8 10 12 14 16 18 20 22 24

Act

ivit

y in

dex

Time (h)

Snow leopard

Blue sheep

Domestic yak

(b)






Liv

esto

ck

Blu

e sh

eep

Bro

wn

bea

r

Sno

w l

eop

ard

Red

fo

x

Tib

etan

fo

x

Pal

lasrsquo

s ca

t

Gra

y w

olf

Do

mes

tic

do

g

05

06

07

08

09

Cluster dendrogram

Hei

ght




Large carnivores



Small carnivores











5 Conclusions


Conict of nterest


Acknowledgments


References








































Volume 2013


ISRN Biotechnology




Volume 2013




Advances in

Virolog y

ISRN Microbiology






ISRN Zoology




ISRN Cell Biology







Enzyme Research










Large carnivores



Small carnivores






05

06

07

1 2 3 4 5 6 7 8 9 10 11 12

Month

Snow leopard

Gray wolf

Domestic dog

Brown bear

Act

ivit

y in

dex

0

01

02

03

04

(a)

0 2 4 6 8 10 12 14 16 18 20 22 24

Time (h)

Snow leopard

Gray wolf

Domestic dog

Brown bear

Act

ivit

y in

dex

0

01

02

03

04

(b)


4 Discussion





05

06

07

1 2 3 4 5 6 7 8 9 10 11 12

Act

ivit

y in

dex

Month

Snow leopard

Red fox

Tibetan fox

Pallasrsquos cat

0

01

02

03

04

(a)

0 2 4 6 8 10 12 14 16 18 20 22 24

Act

ivit

y in

dex

Time (h)

Snow leopard

Red fox

Tibetan fox

Pallasrsquos cat

0

01

02

03

04

(b)


0

01

02

03

04

05

06

07

1 2 3 4 5 6 7 8 9 10 11 12

Act

ivit

y in

dex

Month

Snow leopard

Blue sheep

Domestic yak

(a)

0

01

02

03

04

0 2 4 6 8 10 12 14 16 18 20 22 24

Act

ivit

y in

dex

Time (h)

Snow leopard

Blue sheep

Domestic yak

(b)






Liv

esto

ck

Blu

e sh

eep

Bro

wn

bea

r

Sno

w l

eop

ard

Red

fo

x

Tib

etan

fo

x

Pal

lasrsquo

s ca

t

Gra

y w

olf

Do

mes

tic

do

g

05

06

07

08

09

Cluster dendrogram

Hei

ght




Large carnivores



Small carnivores











5 Conclusions


Conict of nterest


Acknowledgments


References








































Volume 2013


ISRN Biotechnology




Volume 2013




Advances in

Virolog y

ISRN Microbiology






ISRN Zoology




ISRN Cell Biology







Enzyme Research








05

06

07

1 2 3 4 5 6 7 8 9 10 11 12

Act

ivit

y in

dex

Month

Snow leopard

Red fox

Tibetan fox

Pallasrsquos cat

0

01

02

03

04

(a)

0 2 4 6 8 10 12 14 16 18 20 22 24

Act

ivit

y in

dex

Time (h)

Snow leopard

Red fox

Tibetan fox

Pallasrsquos cat

0

01

02

03

04

(b)


0

01

02

03

04

05

06

07

1 2 3 4 5 6 7 8 9 10 11 12

Act

ivit

y in

dex

Month

Snow leopard

Blue sheep

Domestic yak

(a)

0

01

02

03

04

0 2 4 6 8 10 12 14 16 18 20 22 24

Act

ivit

y in

dex

Time (h)

Snow leopard

Blue sheep

Domestic yak

(b)






Liv

esto

ck

Blu

e sh

eep

Bro

wn

bea

r

Sno

w l

eop

ard

Red

fo

x

Tib

etan

fo

x

Pal

lasrsquo

s ca

t

Gra

y w

olf

Do

mes

tic

do

g

05

06

07

08

09

Cluster dendrogram

Hei

ght




Large carnivores



Small carnivores











5 Conclusions


Conict of nterest


Acknowledgments


References








































Volume 2013


ISRN Biotechnology




Volume 2013




Advances in

Virolog y

ISRN Microbiology






ISRN Zoology




ISRN Cell Biology







Enzyme Research








Liv

esto

ck

Blu

e sh

eep

Bro

wn

bea

r

Sno

w l

eop

ard

Red

fo

x

Tib

etan

fo

x

Pal

lasrsquo

s ca

t

Gra

y w

olf

Do

mes

tic

do

g

05

06

07

08

09

Cluster dendrogram

Hei

ght




Large carnivores



Small carnivores











5 Conclusions


Conict of nterest


Acknowledgments


References








































Volume 2013


ISRN Biotechnology




Volume 2013




Advances in

Virolog y

ISRN Microbiology






ISRN Zoology




ISRN Cell Biology







Enzyme Research









5 Conclusions


Conict of nterest


Acknowledgments


References








































Volume 2013


ISRN Biotechnology




Volume 2013




Advances in

Virolog y

ISRN Microbiology






ISRN Zoology




ISRN Cell Biology







Enzyme Research























Volume 2013


ISRN Biotechnology




Volume 2013




Advances in

Virolog y

ISRN Microbiology






ISRN Zoology




ISRN Cell Biology







Enzyme Research







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