Spatiotemporal Patterns of Amur Leopards in Northeast China

Home , Amur leopard, Asian badger

Mammalian Biology 92 (2018) 120–128

Contents lists available at ScienceDirect

Mammalian Biology

jou rnal homepage: www.elsevier.com/locate/mambio

Original investigation

Spatiotemporal patterns of Amur leopards in northeast China:

Inﬂuence of tigers, prey, and humans

∗

Haitao Yang, Xiaodan Zhao, Boyu Han, Tianming Wang, Pu Mou, Jianping Ge, Limin Feng

Monitoring and Research Center for Amur tiger and Amur leopard, State Forestry Administration, State Key Laboratory of Earth Surface and Resource

Ecology, Ministry of Education Key for Biodiversity Science and Engineering, College of Life sciences, Beijing Normal University, Beijing, 100875, China

r t i c l e i n f o a b s t r a c t

Article history: The Amur leopard Panthera pardus orientalis is one of the most endangered cat subspecies in the world.

Received 5 September 2017

The rare leopard is sympatric with Amur tiger Panthera tigris altaica and their prey in human dominated

Accepted 20 March 2018

landscape. To conserve the felid species, it is important to understand the activity patterns of Amur

Available online 22 March 2018

leopards, including its interactions with Amur tigers, prey, and human activities. We used a data set

from 163 camera traps to quantify the spatial-temporal overlap between Amur leopards, Amur tigers,

Handled by Francesco Ferretti

prey species, and human disturbances (e.g., humans presence on foot, vehicles, domestic dogs, and cattle

Keywords: grazing) from January to December 2013 in the Hunchun Nature Reserve, NE China. Our results indicated

that leopards were more active in daytime and twilight; the seasonal spatial-temporal overlaps between

Activity patterns

Amur leopard leopards and tigers were lower than that between leopards and their prey species. Human activities and

camera trap cattle grazing could inﬂuence the spatial distribution and activity patterns of the leopards, and therefore,

human disturbance the conservation actions should focus on reduction of human disturbances to minimize the impacts to

spatial overlap

Amur leopard activity patterns.

Introduction For several years, Amur leopards have been studied using

remote camera-traps in China (Feng et al., 2017, 2011; Wang et al.,

The Amur leopard Panthera pardus orientalis, one of the nine 2016, 2017; Xiao et al., 2014) to estimate population size and spatial

leopard subspecies, is the rarest cat in the world (Nowell and habitat selection across the landscape. Additionally, other studies

Jackson, 1996; Uphyrkina et al., 2001, 2002). Since 1996, it has have focused on the feeding habits of the leopards (Sugimoto et al.,

been classiﬁed as Critically Endangered (CR) by the International 2016). However, basic information about the interactions of the

Union for Conservation of Nature (IUCN) (Stein et al., 2017). The cur- Amur leopard with the Amur tiger, their prey, and human dis-

rent population of the Amur leopard is at least 87 individuals (Feng turbances are still lacking, and such information is important for

et al., 2017) and its distribution is conﬁned to approximately 4,000 continued persistence of Amur leopard.

km in southwestern Primorsky Krai and adjacent habitats in Jilin We focused on the spatial and temporal dimensions of the eco-

and Heilongjiang Provinces, China (Feng et al., 2017; Hebblewhite logical overlap when investigating the interactions of the leopards

et al., 2011). In this area, there are also >38 Amur tigers Panthera with the Amur tiger, their prey, and human disturbances, given

tigris altaica (Feng et al., 2017) existing in the same habitat of the these factors may change leopard behavior. High spatial overlap

leopards. Habitat isolation, inbreeding, environmental stochastic- between leopards and prey may increase leopard encounter rates

ity, and infectious diseases have increased the stress on the leopards with prey species, while high temporal overlap between leopards

(Sugimoto et al., 2014; Uphyrkina et al., 2002). More knowledge of and human disturbances and/or tigers may change activity patterns

basic ecology and behavior are needed for conservation efforts to of the leopards (Linkie and Ridout, 2011). O’Brien et al. (2003) found

combat the trend towards extinction of the Amur leopard. a signiﬁcant spatial relationship between the Sumatran tiger (Pan-

thera tigris sumatrae) and wild pig (Sus sp.), suggesting that tigers

preferred areas where the wild pigs are more abundant. In Thailand,

leopards (Panthera pardus) exhibited reduced diurnal activity in

∗ more heavily used areas compared to the areas less used by peo-

Corresponding author at: College of life Sciences, No. 19, Xin Jie Kou Outer Street,

Haidian District, Beijing 100875, China. ple (Ngoprasert et al., 2007). Tigas et al. (2002) found that bobcat

E-mail address: [email protected] (L. Feng).

https://doi.org/10.1016/j.mambio.2018.03.009

H. Yang et al. / Mammalian Biology 92 (2018) 120–128 121

(Lynx rufus) activity was higher during the diurnal period than in farms), animal husbandry (cattle grazing and frog farming), and

a fragmented study area, suggesting certain degree of avoidance poaching.

of humans. In this study, we used remote camera-trap data from

the Hunchun Nature Reserve in NE China to investigate the sea-

Study design and data collection

sonal spatial-temporal overlap of leopard-tiger, leopard-prey, and

leopard-human disturbances. The two main hypotheses were: (1)

We established 163 camera traps in the gridded study area to

the leopards will have a high spatial or temporal overlap with prey

monitor the Amur leopard, the Amur tiger, and their prey (Fig. 1).

species; and (2) the leopards will avoid human disturbances and

In each grid (3.6 * 3.6 km), mostly 2 camera traps were placed along

tigers spatially or temporally.

road, trail or ridge, which were natural routes for leopards, tigers,

and prey species. The cameras were fastened to trees, 40 - 80 cm

above the ground, and were programmed to shoot 15-sec videos

with a 1-min interval between consecutive events. The camera

Material and methods

traps operated 24-hours per day throughout the year. We visited

each camera monthly to download videos and check batteries.

Study area

We analysed only videos taken at a minimum time interval of

30 minutes (O’Brien et al., 2003). Only videos from the 163 stations

The Hunchun National Reserve (HNR) was located in the east-

were used for analysis. Based on local climate characteristics, we

ern part of Jilin Province, China, bordering Russia and North Korea

◦ ◦ ◦ ◦ deﬁned the seasons as the snow period (winter: Jan-Apr and Nov-

(E 130 14 08 -131 14 44 , N 42 32 40 -43 28 00 ) (Fig. 1). This

Dec) and the snow-free period (summer: May-Oct).

region serves as core habitat for both the Amur tiger and the

Amur leopard in China, tigers and leopards can transfer through the

fences on the Sino-Russia border. The 1,087-km HNR was in the Spatial overlap

northern portion of the Changbai Mountains. The major vegetation

types included deciduous birch (Betula linn.) and oak (Quercus mon- To investigate spatial overlap (Pianka, 1973), we calculated the

golica) forests, most of which were secondary deciduous forests, Relative Abundance Index (RAI) at each trap site as the number of

as well as some coniferous forests distributed in the northeastern detections per 100 camera-trap days of every species for the two

region (Tian et al., 2011). The HNR has been exposed to human seasons (O’Brien et al., 2003). Each camera trap was considered an

disturbance for decades, including plantations (crops and ginseng independent spatial point, and the RAI of each site was examined for

Fig. 1. Study area showing locations of remote camera traps in the Hunchun Nature Reserve, northeast China, 2013. Data about the Amur leopard current extant area derived

from Feng et al. (2017).

122 H. Yang et al. / Mammalian Biology 92 (2018) 120–128

Table 1

correlations among the leopards, tigers, prey species, and human

Number of events and Relative Abundance Index (RAI) for the Amur leopard, Amur

disturbances (grazing, domestic dog, human activity (humans pres-

tiger, prey, and various human disturbances (grazing, domestic dog, human activity

ence on foot) and vehicles) using the Spearman Rank Correlation

(humans presence on foot) and vehicles) during summer and winter, NE China, 2013.

Index (Ramesh et al., 2012) and Pianka’s index (Pianka, 1973) which

Species Events (RAI)

can reﬂect the spatial overlap of leopard-tiger, leopard-prey and

leopard-human disturbances (Ramesh et al., 2012). The Spearman Winter (RAI) Summer (RAI)

rank correlation index and Pianka’s index were calculated using R

Amur leopard 42 (0.23) 79 (0.35)

software (v. 3.1.2)(Team, 2014). Amur tiger 101 (0.53) 152 (0.67)

Wild boar 116 (0.63) 562 (2.46)

Roe deer 213 (1.16) 469 (2.05)

Temporal overlap

Sika deer 362 (1.97) 846 (3.70)

Red fox 158 (0.85) 295 (1.29)

Events were selected, including the date and time of animal Asian badger 49 (0.27) 604 (2.64)

Raccoon dog 19 (0.10) 176 (0.77)

activity, to assess the temporal patterns of leopard-tiger, leopard-

Musk deer 9 (0.05) 14 (0.06)

prey, and leopard-human disturbance. Random samples from the

Manchurian hare 221 (1.21) 343 (1.50)

continuous temporal distribution could reﬂect the probability of

Human activity 985 (5.31) 4876 (21.35)

the events being recorded in any particular interval during the day Grazing 16 (0.09) 1406 (6.16)

Domestic dog 348 (1.90) 639 (2.80)

(Monterroso et al., 2013; Ridout and Linkie, 2009). We followed the

Vehicle 837 (4.52) 3700 (16.20)

procedures of Ridout and Linkie (2009) to quantify the overlap of

the activity patterns of the leopards with tigers, prey species and

human disturbances. The ﬁrst step included separately estimat-

Results

ing the probability density function based on the non-parametric

kernel density. We used the distribution function for pairwise com-

Abundance

parisons of the activity patterns of the leopards, tigers, prey species,

and human disturbances. For the second step, the coefﬁcient of

From January 2013 to December 2013, we used 163 camera traps

overlap, , which ranges from 0 (no overlap) to 1 (complete over-

for 41,122 trap-nights. We collected 121 events for leopards, 253

lap), was used to measure the overlap between the two probability

for tigers, 678 for wild boars, 682 for roe deer, 1,208 for sika deer,

distributions of two species (Linkie and Ridout, 2011). The coefﬁ-

12,807 for human disturbances (humans on foot, vehicles, domestic

cient was obtained from the area under the curve formed by taking

dog and grazing), and 1,888 for small- and medium-sized mammals

the minimum of two density functions at each time point (Linkie

(453 for red fox, 653 for Asian badger, 195 for raccoon dog,23 for

and Ridout, 2011). Ridout and Linkie (2009) developed three ways

musk deer, and 564 for Manchurian hare)(Table 1).

of estimating ; we used 1 for small sample sizes (<75) and 4

The RAI for leopards in the summer was higher than the RAI in

for larger sample sizes (≥75). The 95% conﬁdence interval were

winter; the RAI for tigers was similar to leopard (Table 1). Among

obtained by using 10000 bootstrap samples. Statistical analyses

the three main prey species, the RAI was highest for sika deer in

were completed using the “overlap” package (Meredith and Ridout,

both seasons (Table 1). The RAI of human disturbances in summer

2013) in R software (version v.3.1.2)(Team, 2014).

was higher than winter, and the RAI for cattle were very rare in

The actual time of sunrise and sunset varied in each sample

the winter (Table 1). For small-medium size mammals, the RAI was

period. According to the exact time of sunrise and sunset, the

higher in summer, but only 19 events of raccoon dog were recorded

diurnal cycle was divided into three phases: day, night, and crepus-

in winter (Table 1). For musk deer, we got 23 events during the

cular (1 h before sunrise to 1 h after sunrise and 1 h before sunset

study period. Due to the low detections of raccoon dog and musk

to 1 h after sunset)(Lucherini et al., 2009). The activities of the

deer, we excluded the winter data of raccoon dog and the all data

leopards and their prey species were then classiﬁed into the fol-

of musk deer in the next analysis (Table 1).

lowing three categories: diurnal (activity predominantly between

1 h after sunrise and 1 h before sunset), nocturnal (activity predomi-

Spatial overlap

nantly between 1 h after the sunset and 1 h before the sunrise) and

twilight (activity predominantly between ± 1 h from sunrise and

The seasonal spatial overlap between leopards and tigers was

sunset)(Foster et al., 2013). The selection ratios of each species was

low and Spearman’s rank correlation coefﬁcients of spatial pattern

used to determine whether a species’ activity was predominantly

indicated that overlap was not signiﬁcant (p>0.05) (Table 2). For

classiﬁed as twilight, diurnal, or nocturnal (Bu et al., 2016; Manly

three main prey species (wild boar, roe deer, sika deer), spatial over-

et al., 2007):

lap between leopards and wild boars was highest in summer, while

spatial overlap between leopards and sika deer was highest in win-

wi = oi/eˆi

ter (Table 2). However, only the seasonal Spearman rank correlation

w o

where i is the selection of the period i; i is proportion of detec- coefﬁcients of spatial pattern between leopards and wild boars

tions in period i; ˆi is the proportion of the length of the period to were signiﬁcantly positive (p<0.01) (Table 2). Pianka’s index values

the length of all periods. When i >1, the time period is highly between leopards and small-medium size mammals, except rac-

preferred; when i < 1, the time period is avoided (Bu et al., 2016; coon dog, were relatively higher than the three main prey species

Gerber et al., 2012). and the Spearman rank correlation coefﬁcients of spatial patterns

The synchrony of the times of peak activities for a pair of species were signiﬁcantly positive (p<0.01) in seasonal periods (Table 2).

can also be an indicator of the activity pattern of the two species The low spatial overlap between leopards and human disturbances

(Ramesh et al., 2012; Ridout and Linkie, 2009). We divided the 24 (Table 2) and correlation coefﬁcients of spatial patterns between

hr of the day into 512 equal intervals (approximately 2.8 min per leopards and human disturbances varied seasonally.

interval)(Ridout and Linkie, 2009; Schmid and Schmidt, 2006), and

the probability density of each time point was estimated via kernel

Temporal overlap

density estimation. Spearman’s rank correlation was used to esti-

mate the degree of synchronization of the temporal peak activities

Leopards were more active in daytime and twilight (Table 3),

among the leopards, tigers, prey species, and human disturbances.

and they exhibited a peak of activity at approximately 9:00 dur-

H. Yang et al. / Mammalian Biology 92 (2018) 120–128 123

Fig. 2. Probability density distribution and activity pattern overlap of Amur leopards and Amur tigers and three main prey species throughout the day for summer and winter.

Note: The solid line represents the activities of the Amur leopard density curve, and the dotted line indicates the activity density curve of the species being compared. The

gray area under the curve represents the degree of overlap between the activity patterns of the two species. The vertical dotted lines indicate the average times of sunrise

and sunset.

124 H. Yang et al. / Mammalian Biology 92 (2018) 120–128

Fig. 3. Probability density distribution and activity pattern overlap of Amur leopards and small-sized animals throughout the day in the summer and winter. Note: The solid

line represents the activities of the Amur leopard density curve, and the dotted line indicates the activity density curve of the species being compared. The gray area under

the curve represents the degree of overlap between the activity patterns of the two species. The vertical dotted lines indicate the average times of sunrise and sunset. There

was no data for raccoon dogs during winter.

H. Yang et al. / Mammalian Biology 92 (2018) 120–128 125

Fig. 4. Probability density distribution and activity pattern overlap of Amur leopards and human disturbances (grazing, domestic dog, human activity (humans presence on

foot) and vehicles) during the day in the summer and winter. Note: The solid line represents the activities of the Amur leopard density curve, and the dotted line indicates

the activity density curve of the disturbance being compared with the Amur leopard. The gray area under the curve represents the degree of overlap between the activity

patterns of the two variables. The vertical dotted lines indicate the average times of sunrise and sunset. There was no grazing during winter.

126 H. Yang et al. / Mammalian Biology 92 (2018) 120–128

Table 2

Spatial overlap index (Pianka’s index (95% conﬁdence interval)) and Spearman rank correlation (SRC) between the Amur leopard and Amur tiger, prey, and various human

disturbances (grazing, domestic dog, human activity (humans presence on foot) and vehicles) during summer and winter, NE China, 2013.

Paired species Spatial overlap

Winter Summer

Pianka’s index (CI) SRC Pianka’s index (CI) SRC

Amur leopard VS Amur tiger 0.081 (0.013-0.189) 0.044 0.109 (0.030-0.230) -0.042

** *

Amur leopard VS Wild boar 0.171 (0.077-0.326) 0.230 0.379 (0.171-0.597) 0.197

Amur leopard VS Roe deer 0.067 (0.021-0.164) -0.055 0.317 (0.171-0.510) 0.04

Amur leopard VS Sika deer 0.208 (0.091-0.402) 0.111 0.301 (0.164-0.453) 0.138

** **

Amur leopard VS Red fox 0.344 (0.208-0.499) 0.329 0.263 (0.130-0.513) 0.285

** **

Amur leopard VS Asian badger 0.441 (0.082-0.680) 0.244 0.372 (0.237-0.537) 0.329

Amur leopard VS Raccoon dog - - 0.094 (0.036-0.198) 0.052

* **

Amur leopard VS Manchurian hare 0.357 (0.108-0.591) 0.201 0.289 (0.142-0.491) 0.272

Amur leopard VS Human activity 0.062 (0.029-0.124) 0.105 0.093 (0.050-0.187) -0.114

Amur leopard VS Grazing - - 0.121 (0.014-0.394) 0.047

Amur leopard VS Domestic dog 0.063 (0.025-0.192) 0.149 0.035 (0.013-0.090) -0.138

Amur leopard VS Vehicle 0.030 (0.003-0.106) 0.002 0.024 (0.008-0.057) -0.122

P < 0.05.

P < 0.01.

Table 3

Number of events n (selection ratio wi) of leopards, tiger, prey, and various human disturbances (grazing, domestic dog, human activity (humans presence on foot) and

vehicles) in a given time period during summer and winter, NE China, 2013.

Species Season

Winter Summer

n (wi) in given time period n (wi) in given time period

Diurnal Nocturnal Twilight Diurnal Nocturnal Twilight

Amur leopard 28 (1.85) 5 (0.25) 9 (1.29) 48 (1.24) 10 (0.37) 21 (1.59)

Amur tiger 18 (0.49) 58 (1.21) 25 (1.49) 32 (0.43) 65 (1.24) 55 (2.17)

Wild boar 46 (1.10) 41 (0.75) 29 (1.50) 270 (0.98) 153 (0.79) 139 (1.48)

Roe deer 92 (1.20) 71 (0.70) 50 (1.41) 194 (0.85) 127 (0.79) 148 (1.89)

Sika deer 171 (1.31) 115 (0.67) 76 (1.26) 411 (0.99) 196 (0.67) 239 (1.70)

Red fox 11 (0.19) 121 (1.62) 26 (0.99) 13 (0.09) 183 (1.80) 99 (2.01)

Asian badger 14 (0.79) 28 (1.21) 7 (0.14) 187 (0.63) 327 (1.57) 90 (0.899)

Raccoon dog - - - 11 (0.13) 115 (1.90) 50 (1.70)

Manchurian hare 2 (0.03) 212 (2.03) 7 (0.19) 15 (0.09) 266 (2.25) 62 (1.01)

Human activity 886 (2.50) 32 (0.07) 67 (0.41) 4517 (1.89) 68 (0.04) 291 (0.36)

Grazing - - - 942 (1.37) 184 (0.38) 280 (1.19)

Domestic dog 286 (2.28) 26 (0.16) 36 (0.62) 560 (1.79) 26 (0.12) 53 (0.50)

Vehicle 680 (2.25) 52 (0.13) 105 (0.75) 3281 (1.81) 94 (0.07) 325 (0.53)

Table 4

Temporal overlap index ( (95% conﬁdence interval)) and Spearman rank correlation (SRC) between the Amur leopard and Amur tiger, prey species, and various human

disturbances (grazing, domestic dog, human activity (humans presence on foot) and vehicles) during summer and winter, NE China, 2013.

Paired species Seasonally temporal overlap

Winter Summer

(CI) SRC (CI) SRC

** **

Amur leopard VS Amur tiger 0.55 (0.38-0.64) -0.51 0.67 (0.55-0.78) -0.64

Amur leopard VS Wild boar 0.51 (0.50-0.76) 0.001 0.84 (0.75-0.92) 0.36

** **

Amur leopard VS Roe deer 0.73 (0.63-0.85) 0.63 0.77 (0.67-0.86) -0.17

** **

Amur leopard VS Sika deer 0.73 (0.58-0.82) 0.57 0.82 (0.73-0.90) 0.39

** **

Amur leopard VS Red fox 0.43 (0.36-0.60) -0.83 0.53 (0.43-0.63) -0.93

** **

Amur leopard VS Asian badger 0.59 (0.49-0.77) -0.64 0.68 (0.59-0.77) -0.75

Amur leopard VS Raccoon dog - - 0.49 (0.38-0.59) -0.81

** **

Amur leopard VS Manchurian hare 0.27 (0.16-0.35) -0.92 0.40 (0.31-0.50) -0.86

** **

Amur leopard VS Human activity 0.75 (0.61-0.84) 0.86 0.70 (0.61-0.79) 0.93

Amur leopard VS Grazing - - 0.88 (0.81-0.94) 0.69

** **

Amur leopard VS Domestic dog 0.81 (0.67-0.90) 0.94 0.75 (0.65-0.84) 0.95

** **

Amur leopard VS Vehicle 0.78 (0.52-0.80) 0.79 0.73 (0.64-0.82) 0.91

P < 0.05.

P < 0.01.

ing both seasons (Figs. 2–4). In contrast, tigers were more active ity patterns of them varied in both seasons. In winter, three prey

in night and twilight in both seasons (Table 3). The temporal over- species preferred daytime and twilight. However, they were only

lap value in winter of both cats was lower than in summer, and active at twilight in summer (Table 3, Fig. 2). The temporal over-

the correlation coefﬁcients of peak activity were also signiﬁcantly lap values in winter between leopards and prey species were lower

negative in both seasons (Table 4). For three prey species, the activ- than in summer (Table 4). The synchrony of the times of peak activ-

H. Yang et al. / Mammalian Biology 92 (2018) 120–128 127

ities for pairs of leopards-prey species also varied in both seasons of leopards-roe deer and leopards-sika deer were high that indicate

(Table 4, Fig. 2). In winter, activity patterns of small-medium size there may be high encounter rate between leopards and sika deer

mammals were more active at night, but they were more active dur- or roe deer, the relatively low spatial overlap of leopards-roe deer

ing the night and twilight in summer (Table 3, Fig. 3). The temporal and leopards-sika deer would balance off the actual encounter rate.

overlap values between leopards and small-medium size mammals We speculated that sika deer and roe deer would avoid the leopards

were higher in summer than in winter, and the synchrony of the spatially in the two seasons. Additionally, most of our camera traps

times of peak activities for pairs of them were signiﬁcantly nega- are mounted on the trails where leopard and tiger frequently used

tive (Table 4). Human disturbances were more prevalent in daytime but prey may avoid (Jia et al., 2014; Zhu et al., 2011).

(Table 3) with the values of temporal overlap between leopards and The spatial-temporal overlap between leopards and wild boars

human disturbances being higher in winter than in summer, and were relatively higher in summer than in winter. We speculated

the synchrony of peak activities for pairs of them were signiﬁcantly that leopards may avoid adult wild boar in winter and preferred

positive (Table 4). smaller wild boar in summer to minimize predation difﬁculties

(Andheria et al., 2007; Bromley and Kucherenko, 1983; Karanth and

Sunquist, 1995). Additionally, small-medium sized mammals were

Discussion nocturnal and their temporal overlaps with leopards were very low

(Table 4). The proportion of small-medium sized mammals con-

Coexistence of sympatric predators is favoured by partition- tributed less than 20% of leopard diet (Sugimoto et al., 2016), and

ing of space, habitat, diet and/or temporal activity patterns (de the spatial-temporal overlaps of leopards small-medium size mam-

Almeida Jácomo et al., 2004; Durant, 1998; Karanth and Sunquist, mals were not found signiﬁcant seasonal variation (Tables 2 and 4;

2000; Palomares et al., 1996; Taber et al., 1997). Dietary parti- Fig. 4), indicating the weak relationships between Amur leopards

tioning may favour the coexistence between tigers and leopards and those species.

(Andheria et al., 2007; Karanth and Sunquist, 2000, 1995). However, We speculated that the avoidance of humans by Amur leop-

Lovari et al. (2015) found a great dietary overlap between tiger and ard may limit their distribution and therefore their abundance. The

leopard in their study area, suggesting that coexistence was locally seasonal variation of the spatial-temporal overlaps between leop-

favoured by other mechanisms rather than prey partitioning, and ards and human disturbances indicated the changes of leopards in

other studies have emphasised the role of spatiotemporal partition- spatial distribution accordingly (Tables 2 and 4; Fig. 4). Our results

ing (Carter et al., 2015; Karanth and Sunquist, 2010; Ramesh et al., support the reports by Carter et al. (2012) that leopards change their

2012). In particular, leopards have been suggested to avoid tigers by spatial distribution or activity patterns to coexist with humans.

changing niche breadth or space use (Harihar et al., 2011; Mondal Wang et al. (2017) indicated that Amur leopards keep away from

et al., 2012; Odden et al., 2010; Schaller, 1967; Seidensticker, 1976; roads and human settlements, and avoided areas where livestock

Steinmetz et al., 2013; Sunarto et al., 2015). Amur tigers were most were abundant. The same type of behaviors of leopards were also

likely to occur in the valley at lower altitudes, which provided easy found in Nepal (Carter et al., 2015) and Thailand (Ngoprasert et al.,

travel corridors (Carroll and Miquelle, 2006). In NE China, Amur 2007).

leopards usually use ridge trails more frequently than tigers (Wang Our results showed there were weak spatial associations and

et al., 2017). Our results revealed spatial overlap between leopards strong temporal overlap between leopards and their main prey.

and tigers was rather low (Table 2) suggesting that leopards avoid There were high temporal overlaps and low spatial overlaps

tigers by spatial separation (Wang et al., 2017, 2018). Temporal between leopards and various human disturbances, indicating the

segregation is a mechanism that species of similar niches could use leopards may adjust their spatial distribution to minimize interac-

to avoid competition (Hayward and Slotow, 2010; Kronfeld-Schor tions with human. It should be noted that the leopard population

and Dayan, 2003). Our results that the activity patterns of leopards survived in our study area and neighbouring Sino-Russian trans-

and tigers vary at different temporal scales support it (Fig. 3). The bourdary area, is the single population of the rare leopard, and its

Amur leopards were more active during daytime in our study area, area limited to the narrow region of approximately 4,000 km (Feng

and their activity peaks were similar in both summer and winter et al., 2017). Obviously, it is threatened by small population size,

(Table 3; Figs. 2–4). In contrast, the Amur tigers showed nocturnal genetic impoverishment and stochastic events (Sugimoto et al.,

and crepuscular activity patterns (Table 3; Fig. 2). In Russia, satellite 2014; Uphyrkina et al., 2002). Now, the Chinese government has

telemetry data showed that Amur tigers were active mostly at twi- been convinced to create a National Park for Amur tigers and Amur

light (Rozhnov et al., 2011). Our results also support that temporal leopards covering about 15,000 km of forested lands (Feng et al.,

partitioning between tiger and leopard may allow the coexistence 2017; McLaughlin, 2016). This may be the last chance to save and

of these sympatric big cats (Steinmetz et al., 2013; Sunarto et al., restore this critically endangered cat.

2015).

The behavioral strategies of big cats are to maximize nutri-

Acknowledgements

ent intake while to minimize energy expenditure (Sunquist and

Sunquist, 1989). Larger predators are inclined to kill larger-bodied

China’s State Forestry Administration approved this study as a

prey to achieve the best trade-off (Hayward and Kerley, 2005).

part of the long-term Tiger Leopard Observation Network (TLON).

Studies in Far Eastern Russia, have conﬁrmed that the food pref-

Jilin Province Bureau approved permits for the work conducted.

erences of the Amur leopard were sika deer and roe deer in winter

Beijing Normal University conducted this study in collaboration

(Kerley et al., 2015; Sugimoto et al., 2016). In this study, we found

with the administrations of the local protected areas. We thank the

that leopards-roe deer and leopards-sika deer temporally over-

Jilin Province Forestry Bureau for kindly providing research per-

lapped more than that to other prey species (Table 4) in winter.

mits and facilitating ﬁeldwork. We thank Tonggang Chen, Shuyun

Contrary to the predating behaviors, the ecology of fear postu-

Peng, Zhanzheng Sun, and Chunze Tan for ﬁeld data collection.

lates that herbivores with natural vigilance would minimize the

This study was granted by the National Key R&D Program of China

encounter rate with predators by changing their activity patterns

(2016YFC0503200), the National Natural Science Foundation of

or their spatial distribution (Brown et al., 1999). High encounter

China (31200410, 31210103911, 31421063, 31270567, 31470566

rates with predators would inﬂuence habitat use, activity patterns

and 31670537) and the National Scientiﬁc and Technical Founda-

and the temporal and spatial distribution patterns of the herbivores

tion Project of China (2012FY112000).

(Hayward and Kerley, 2005). Although the temporal overlap values

128 H. Yang et al. / Mammalian Biology 92 (2018) 120–128

References Monterroso, P., Alves, P.C., Ferreras, P., 2013. Catch me if you can: diel activity

patterns of mammalian prey and predators. Ethology 119, 1044–1056.

Ngoprasert, D., Lynam, A.J., Gale, G.A., 2007. Human disturbance affects habitat use

Andheria, A., Karanth, K., Kumar, N., 2007. Diet and prey proﬁles of three sympatric

and behaviour of Asiatic leopard Panthera pardus in Kaeng Krachan National

large carnivores in Bandipur Tiger Reserve, India. Journal of Zoology 273,

169–175. Park, Thailand. Oryx 41, 343–351.

Nowell, K., Jackson, P., 1996. Wild cats: status survey and conservation action plan.

Bromley, G.F., Kucherenko, S.P., Nauka, Moscow, Russia. (in Russian) 1983.

IUCN Gland.

Ungulates of the southern part of the Far East[M].

O’Brien, T.G., Kinnaird, M.F., Wibisono, H.T., 2003. Crouching tigers, hidden prey:

Brown, J.S., Laundré, J.W., Gurung, M., 1999. The ecology of fear: optimal foraging,

Sumatran tiger and prey populations in a tropical forest landscape. Animal

game theory, and trophic interactions. Journal of Mammalogy 80, 385–399.

Conservation 6, 131–139.

Bu, H., Wang, F., McShea, W.J., Lu, Z., Wang, D., Li, S., 2016. Spatial Co-Occurrence

Odden, M., Wegge, P., Fredriksen, T., 2010. Do tigers displace leopards? If so, why?

and Activity Patterns of Mesocarnivores in the Temperate Forests of Southwest

Ecological Research 25, 875–881.

China. PloS one 11, e0164271.

Palomares, F., Ferreras, P., Fedriani, J.M., Delibes, M., 1996. Spatial relationships

Carroll, C., Miquelle, D.G., 2006. Spatial viability analysis of Amur tiger Panthera

between Iberian lynx and other carnivores in an area of south-western Spain.

tigris altaica in the Russian Far East: the role of protected areas and landscape

Journal of Applied Ecology, 5–13.

matrix in population persistence. Journal of Applied Ecology 43, 1056–1068.

Pianka, E.R., 1973. The structure of lizard communities. Annual review of ecology

Carter, N.H., Shrestha, B.K., Karki, J.B., Pradhan, N.M.B., Liu, J., 2012. Coexistence

and systematics 4, 53–74.

between wildlife and humans at ﬁne spatial scales. Proceedings of the National

Ramesh, T., Kalle, R., Sankar, K., Qureshi, Q., 2012. Spatio-temporal partitioning

Academy of Sciences 109, 15360–15365.

among large carnivores in relation to major prey species in Western Ghats.

Carter, N., Jasny, M., Gurung, B., Liu, J., 2015. Impacts of people and tigers on

Journal of Zoology 287, 269–275.

leopard spatiotemporal activity patterns in a global biodiversity hotspot.

Ridout, M.S., Linkie, M., 2009. Estimating overlap of daily activity patterns from

Global Ecology and Conservation 3, 149–162.

camera trap data. Journal of Agricultural, Biological, and Environmental

de Almeida Jácomo, A.T., Silveira, L., Diniz-Filho, J.A.F., 2004. Niche separation

Statistics 14, 322–337.

between the maned wolf (Chrysocyon brachyurus), the crab-eating fox

Rozhnov, V., Hernandez-Blanco, J., Lukarevskiy, V., Naidenko, S., Sorokin, P.,

(Dusicyon thous) and the hoary fox (Dusicyon vetulus) in central Brazil. Journal

Litvinov, M., Kotlyar, A., Pavlov, D., 2011. Application of satellite collars to the

of Zoology 262, 99–106.

study of home range and activity of the Amur tiger (Panthera tigris altaica).

Durant, S.M., 1998. Competition refuges and coexistence: an example from

Biology Bulletin 38, 834–847.

Serengeti carnivores. Journal of Animal Ecology 67, 370–386.

Schaller, G.B., 1967. The Deer and the Tiger. In: A Study of Wildlife in India.[With

Feng, L., Wang, T., Mou, P., Kou, X., Ge, J., 2011. First image of an Amur leopard

Plates.]. University of Chicago Press.

recorded in China. Cat News 55.

Schmid, F., Schmidt, A., 2006. Nonparametric estimation of the coefﬁcient of

Feng, L., Shevtsova, E., Vitkalova, A., Matyukhina, D., Miquelle, D., Aramilev, V.,

overlapping—theory and empirical application. Computational statistics & data

Wang, T., Mu, P., Xu, R., Ge, J., 2017. Collaboration brings hope for the last Amur

analysis 50, 1583–1596.

leopards. Cat News 65, 20.

Seidensticker, J., 1976. On the ecological separation between tigers and leopards.

Foster, V.C., Sarmento, P., Sollmann, R., Torres, N., Jacomo, A.T.A., Negroes, N.,

Biotropica, 225–234.

Fonseca, C., Silveira, L., 2013. Jaguar and Puma Activity Patterns and

Stein, A., Athreya, V., Gerngross, P., Balme, G., Henschel, P., Karanth, U., Miquelle,

Predator-Prey Interactions in Four Brazilian Biomes. Biotropica 45, 373–379.

D., Rostro-Garcia, S., Kamler, J., Laguardia, A., 2017. Panthera pardus. (errata

Gerber, B.D., Karpanty, S.M., Randrianantenaina, J., 2012. Activity patterns of

version published in 2016) The IUCN Red List of Threatened Species 2016: e.

carnivores in the rain forests of Madagascar: implications for species

T15954A102421779. Downloaded on 14.

coexistence. Journal of Mammalogy 93, 667–676.

Steinmetz, R., Seuaturien, N., Chutipong, W., 2013. Tigers, leopards, and dholes in a

Harihar, A., Pandav, B., Goyal, S.P., 2011. Responses of leopard Panthera pardus to

half-empty forest: Assessing species interactions in a guild of threatened

the recovery of a tiger Panthera tigris population. Journal of Applied Ecology 48,

806–814. carnivores. Biological Conservation 163, 68–78.

Sugimoto, T., Aramilev, V.V., Kerley, L.L., Nagata, J., Miquelle, D.G., McCullough,

Hayward, M.W., Kerley, G.I., 2005. Prey preferences of the lion (Panthera leo).

D.R., 2014. Noninvasive genetic analyses for estimating population size and

Journal of Zoology 267, 309–322.

genetic diversity of the remaining Far Eastern leopard (Panthera pardus

Hayward, M.W., Slotow, R., 2010. Temporal Partitioning of Activity in Large African

orientalis) population. Conservation genetics 15, 521–532.

Carnivores: Tests of Multiple Hypotheses. South African Journal of Wildlife

Sugimoto, T., Aramilev, V.V., Nagata, J., McCullough, D.R., 2016. Winter food habits

Research 39, 109–125.

of sympatric carnivores, Amur tigers and Far Eastern leopards, in the Russian

Hebblewhite, M., Miguelle, D.G., Murzin, A.A., Aramilev, V.V., Pikunov, D.G., 2011.

Far East. Mammalian Biology-Zeitschrift für Säugetierkunde 81, 214–218.

Predicting potential habitat and population size for reintroduction of the Far

Sunarto, S., Kelly, M., Parakkasi, K., Hutajulu, M., 2015. Cat coexistence in central

Eastern leopards in the Russian Far East. Biological Conservation 144,

2403–2413. Sumatra: ecological characteristics, spatial and temporal overlap, and

implications for management. Journal of Zoology 296, 104–115.

Jia, L.I., Yankuo, L.I., Miao, L., Xie, G., Yuan, F., 2014. Impact of Logging upon the

Sunquist, M.E., Sunquist, F.C., 1989. Ecological constraints on predation by large

Habitat Selection of Sika Deer in Winter in Taohongling National Nature

felids. In: Carnivore behavior, ecology, and evolution. Springer, pp. 283–301.

Reserve,China. Sichuan Journal of Zoology.

Taber, A.B., Novaro, A.J., Neris, N., Colman, F.H., 1997. The food habits of sympatric

Karanth, K.U., Sunquist, M.E., 1995. Prey selection by tiger, leopard and dhole in

jaguar and puma in the Paraguayan Chaco. Biotropica 29, 204–213.

tropical forests. Journal of Animal Ecology, 439–450.

Team, R.C., 2014. R: A language and environment for statistical computing. Vienna,

Karanth, K., Sunquist, M., 2000. Behavioral correlates of predation by tiger, leopard

Austria: R Foundation for Statistical Computing; 2014.

and dhole in Nagarhole National Park, India. Journal of Zoology 250, 255–265.

Tian, Y., Wu, J.G., Smith, A.T., Wang, T.M., Kou, X.J., Ge, J.P., 2011. Population

Karanth, K.U., Sunquist, M.E., 2010. Behavioural correlates of predation by tiger

viability of the Siberian tiger in a changing landscape: Going, going and gone?

(Panthera tigris), leopard (Panthera pardus) and dhole (Cuon alpinus) in

Ecological Modelling 222, 3166–3180.

Nagarahole, India. Proceedings of the Zoological Society of London 250,

255–265. Tigas, L.A., Van Vuren, D.H., Sauvajot, R.M., 2002. Behavioral responses of bobcats

and coyotes to habitat fragmentation and corridors in an urban environment.

Kerley, L.L., Mukhacheva, A.S., Matyukhina, D.S., Salmanova, E., Salkina, G.P.,

Biological Conservation 108, 299–306.

Miquelle, D.G., 2015. A comparison of food habits and prey preference of Amur

Uphyrkina, O., Johnson, W.E., Quigley, H., Miquelle, D., Marker, L., Bush, M., O’Brien,

tiger (Panthera tigris altaica) at three sites in the Russian Far East. Integrative

S.J., 2001. Phylogenetics, genome diversity and origin of modern leopard,

zoology 10, 354–364.

Panthera pardus. Molecular ecology 10, 2617–2633.

Kronfeld-Schor, N., Dayan, T., 2003. Partitioning of time as an ecological resource.

Uphyrkina, O., Miquelle, D., Quigley, H., Driscoll, C., O’Brien, S., 2002. Conservation

Annual Review of Ecology. Evolution, and Systematics, 153–181.

genetics of the Far Eastern leopard (Panthera pardus orientalis). Journal of

Linkie, M., Ridout, M., 2011. Assessing tiger–prey interactions in Sumatran

Heredity 93, 303–311.

rainforests. Journal of Zoology 284, 224–229.

Wang, T., Feng, L., Mou, P., Wu, J., Smith, J.L., Xiao, W., Yang, H., Dou, H., Zhao, X.,

Lovari, S., Pokheral, C., Jnawali, S., Fusani, L., Ferretti, F., 2015. Coexistence of the

Cheng, Y., 2016. Amur tigers and leopards returning to China: direct evidence

tiger and the common leopard in a prey-rich area: the role of prey partitioning.

and a landscape conservation plan. Landscape ecology 31, 491–503.

Journal of Zoology 295, 122–131.

Wang, T., Feng, L., Yang, H., Han, B., Zhao, Y., Juan, L., Lü, X., Zou, L., Li, T., Xiao, W.,

Lucherini, M., Reppucci, J.I., Walker, R.S., Villalba, M.L., Wurstten, A., Gallardo, G.,

2017. A science-based approach to guide Amur leopard recovery in China.

Iriarte, A., Villalobos, R., Perovic, P., 2009. Activity Pattern Segregation of

Biological Conservation 210, 47–55.

Carnivores in the High Andes. Journal of Mammalogy 90, 1404–1409.

Wang, T., Royle, J.A., Smith, J.L., Zou, L., Lü, X., Li, T., Yang, H., Li, Z., Feng, R., Bian, Y.,

Manly, B., McDonald, L., Thomas, D., McDonald, T.L., Erickson, W.P., 2007. Springer

2018. Living on the edge: Opportunities for Amur tiger recovery in China.

Science & Business Media. In: Resource selection by animals: statistical design

Biological Conservation 217, 269–279.

and analysis for ﬁeld studies.

Xiao, W.H., Feng, L.M., Zhao, X.D., Yang, H.T., Dou, H.L., Cheng, Y.C., Mou, P., Wang,

McLaughlin, K., 2016. Tiger land. Science 353, 744–745.

T.M., Ge, J.P., 2014. Distribution and abundance of Amur tiger, Amur leopard

Meredith, M., Ridout, M., 2013. overlap: Estimates of Coefﬁcient of Overlapping for

and their ungulate preys in Hunchun National Nature Reserve, Jilin.

Animal Activity Patterns. R package version 0.2. 0. URL: http://CRAN. R-project.

Biodiversity Science 22, 717–724, in Chinese.

org/package= overlap.

Zhu, H.Q., Ge, Z.Y., Chang, S.H., Liu, G., Wu, J.C., Shi, X.J., Xu, J.F., Mao, Z.X., 2011.

Mondal, K., Gupta, S., Bhattacharjee, S., Qureshi, Q., Sankar, K., 2012. Response of

Winter habitat selection of wild boar (sus scrofa ussuricus) in Huangnihe nature

leopards to re-introduced tigers in Sariska Tiger Reserve, Western India.

reserve. Chinese Journal of Ecology 30, 734–738.

International Journal of Biodiversity and Conservation 4, 228–236.