Spatiotemporal patterns of Amur leopards in northeast China: Influence of tigers, prey, and humans

Mammalian Biology 92 (2018) 120–128

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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

a r t i c l e

i n f o

Article history: Received 5 September 2017 Accepted 20 March 2018 Available online 22 March 2018 Handled by Francesco Ferretti Keywords: Activity patterns Amur leopard camera trap human disturbance spatial overlap

a b s t r a c t The Amur leopard Panthera pardus orientalis is one of the most endangered cat subspecies in the world. The rare leopard is sympatric with Amur tiger Panthera tigris altaica and their prey in human dominated landscape. To conserve the felid species, it is important to understand the activity patterns of Amur 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, prey species, and human disturbances (e.g., humans presence on foot, vehicles, domestic dogs, and cattle 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 leopards and tigers were lower than that between leopards and their prey species. Human activities and cattle grazing could influence the spatial distribution and activity patterns of the leopards, and therefore, the conservation actions should focus on reduction of human disturbances to minimize the impacts to Amur leopard activity patterns. ¨ Saugetierkunde. ¨ © 2018 Deutsche Gesellschaft fur Published by Elsevier GmbH. All rights reserved.

Introduction The Amur leopard Panthera pardus orientalis, one of the nine leopard subspecies, is the rarest cat in the world (Nowell and Jackson, 1996; Uphyrkina et al., 2001, 2002). Since 1996, it has been classified as Critically Endangered (CR) by the International Union for Conservation of Nature (IUCN) (Stein et al., 2017). The current population of the Amur leopard is at least 87 individuals (Feng et al., 2017) and its distribution is confined to approximately 4,000 km2 in southwestern Primorsky Krai and adjacent habitats in Jilin and Heilongjiang Provinces, China (Feng et al., 2017; Hebblewhite et al., 2011). In this area, there are also >38 Amur tigers Panthera tigris altaica (Feng et al., 2017) existing in the same habitat of the leopards. Habitat isolation, inbreeding, environmental stochasticity, and infectious diseases have increased the stress on the leopards (Sugimoto et al., 2014; Uphyrkina et al., 2002). More knowledge of basic ecology and behavior are needed for conservation efforts to combat the trend towards extinction of the Amur leopard.

∗ Corresponding author at: College of life Sciences, No. 19, Xin Jie Kou Outer Street, Haidian District, Beijing 100875, China. E-mail address: [email protected] (L. Feng).

For several years, Amur leopards have been studied using remote camera-traps in China (Feng et al., 2017, 2011; Wang et al., 2016, 2017; Xiao et al., 2014) to estimate population size and spatial habitat selection across the landscape. Additionally, other studies have focused on the feeding habits of the leopards (Sugimoto et al., 2016). However, basic information about the interactions of the Amur leopard with the Amur tiger, their prey, and human disturbances are still lacking, and such information is important for continued persistence of Amur leopard. We focused on the spatial and temporal dimensions of the ecological overlap when investigating the interactions of the leopards with the Amur tiger, their prey, and human disturbances, given these factors may change leopard behavior. High spatial overlap between leopards and prey may increase leopard encounter rates with prey species, while high temporal overlap between leopards and human disturbances and/or tigers may change activity patterns of the leopards (Linkie and Ridout, 2011). O’Brien et al. (2003) found a significant spatial relationship between the Sumatran tiger (Panthera 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 people (Ngoprasert et al., 2007). Tigas et al. (2002) found that bobcat

https://doi.org/10.1016/j.mambio.2018.03.009 ¨ Saugetierkunde. ¨ Published by Elsevier GmbH. All rights reserved. 1616-5047/© 2018 Deutsche Gesellschaft fur

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

(Lynx rufus) activity was higher during the diurnal period than in a fragmented study area, suggesting certain degree of avoidance of humans. In this study, we used remote camera-trap data from the Hunchun Nature Reserve in NE China to investigate the seasonal spatial-temporal overlap of leopard-tiger, leopard-prey, and leopard-human disturbances. The two main hypotheses were: (1) the leopards will have a high spatial or temporal overlap with prey species; and (2) the leopards will avoid human disturbances and tigers spatially or temporally.

Material and methods Study area The Hunchun National Reserve (HNR) was located in the eastern part of Jilin Province, China, bordering Russia and North Korea (E 130◦ 14 08 -131◦ 14 44 , N 42◦ 32 40 -43◦ 28 00 ) (Fig. 1). This 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-km2 HNR was in the northern portion of the Changbai Mountains. The major vegetation types included deciduous birch (Betula linn.) and oak (Quercus mongolica) forests, most of which were secondary deciduous forests, as well as some coniferous forests distributed in the northeastern region (Tian et al., 2011). The HNR has been exposed to human disturbance for decades, including plantations (crops and ginseng

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farms), animal husbandry (cattle grazing and frog farming), and poaching. Study design and data collection We established 163 camera traps in the gridded study area to monitor the Amur leopard, the Amur tiger, and their prey (Fig. 1). In each grid (3.6 * 3.6 km), mostly 2 camera traps were placed along 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 traps operated 24-hours per day throughout the year. We visited each camera monthly to download videos and check batteries. We analysed only videos taken at a minimum time interval of 30 minutes (O’Brien et al., 2003). Only videos from the 163 stations were used for analysis. Based on local climate characteristics, we defined the seasons as the snow period (winter: Jan-Apr and NovDec) and the snow-free period (summer: May-Oct). Spatial overlap To investigate spatial overlap (Pianka, 1973), we calculated the Relative Abundance Index (RAI) at each trap site as the number of detections per 100 camera-trap days of every species for the two seasons (O’Brien et al., 2003). Each camera trap was considered an 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).

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correlations among the leopards, tigers, prey species, and human disturbances (grazing, domestic dog, human activity (humans presence on foot) and vehicles) using the Spearman Rank Correlation Index (Ramesh et al., 2012) and Pianka’s index (Pianka, 1973) which can reflect the spatial overlap of leopard-tiger, leopard-prey and leopard-human disturbances (Ramesh et al., 2012). The Spearman rank correlation index and Pianka’s index were calculated using R software (v. 3.1.2)(Team, 2014). Temporal overlap Events were selected, including the date and time of animal activity, to assess the temporal patterns of leopard-tiger, leopardprey, and leopard-human disturbance. Random samples from the continuous temporal distribution could reflect the probability of the events being recorded in any particular interval during the day (Monterroso et al., 2013; Ridout and Linkie, 2009). We followed the 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 estimating the probability density function based on the non-parametric kernel density. We used the distribution function for pairwise comparisons of the activity patterns of the leopards, tigers, prey species, and human disturbances. For the second step, the coefficient of overlap, , which ranges from 0 (no overlap) to 1 (complete overlap), was used to measure the overlap between the two probability distributions of two species (Linkie and Ridout, 2011). The coefficient was obtained from the area under the curve formed by taking the minimum of two density functions at each time point (Linkie and Ridout, 2011). Ridout and Linkie (2009) developed three ways of estimating ; we used 1 for small sample sizes (<75) and 4 for larger sample sizes (≥75). The 95% confidence interval were obtained by using 10000 bootstrap samples. Statistical analyses were completed using the “overlap” package (Meredith and Ridout, 2013) in R software (version v.3.1.2)(Team, 2014). The actual time of sunrise and sunset varied in each sample period. According to the exact time of sunrise and sunset, the diurnal cycle was divided into three phases: day, night, and crepuscular (1 h before sunrise to 1 h after sunrise and 1 h before sunset to 1 h after sunset)(Lucherini et al., 2009). The activities of the leopards and their prey species were then classified into the following three categories: diurnal (activity predominantly between 1 h after sunrise and 1 h before sunset), nocturnal (activity predominantly between 1 h after the sunset and 1 h before the sunrise) and twilight (activity predominantly between ± 1 h from sunrise and sunset)(Foster et al., 2013). The selection ratios of each species was used to determine whether a species’ activity was predominantly classified as twilight, diurnal, or nocturnal (Bu et al., 2016; Manly et al., 2007): wi = oi /eˆi where wi is the selection of the period i; oi is proportion of detections in period i; eˆi is the proportion of the length of the period to the length of all periods. When wi >1, the time period is highly preferred; when wi < 1, the time period is avoided (Bu et al., 2016; Gerber et al., 2012). The synchrony of the times of peak activities for a pair of species can also be an indicator of the activity pattern of the two species (Ramesh et al., 2012; Ridout and Linkie, 2009). We divided the 24 hr of the day into 512 equal intervals (approximately 2.8 min per interval)(Ridout and Linkie, 2009; Schmid and Schmidt, 2006), and the probability density of each time point was estimated via kernel density estimation. Spearman’s rank correlation was used to estimate the degree of synchronization of the temporal peak activities among the leopards, tigers, prey species, and human disturbances.

Table 1 Number of events and Relative Abundance Index (RAI) for the Amur leopard, 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. Species

Amur leopard Amur tiger Wild boar Roe deer Sika deer Red fox Asian badger Raccoon dog Musk deer Manchurian hare Human activity Grazing Domestic dog Vehicle

Events (RAI) Winter (RAI)

Summer (RAI)

42 (0.23) 101 (0.53) 116 (0.63) 213 (1.16) 362 (1.97) 158 (0.85) 49 (0.27) 19 (0.10) 9 (0.05) 221 (1.21) 985 (5.31) 16 (0.09) 348 (1.90) 837 (4.52)

79 (0.35) 152 (0.67) 562 (2.46) 469 (2.05) 846 (3.70) 295 (1.29) 604 (2.64) 176 (0.77) 14 (0.06) 343 (1.50) 4876 (21.35) 1406 (6.16) 639 (2.80) 3700 (16.20)

Results Abundance From January 2013 to December 2013, we used 163 camera traps for 41,122 trap-nights. We collected 121 events for leopards, 253 for tigers, 678 for wild boars, 682 for roe deer, 1,208 for sika deer, 12,807 for human disturbances (humans on foot, vehicles, domestic dog and grazing), and 1,888 for small- and medium-sized mammals (453 for red fox, 653 for Asian badger, 195 for raccoon dog,23 for musk deer, and 564 for Manchurian hare)(Table 1). The RAI for leopards in the summer was higher than the RAI in winter; the RAI for tigers was similar to leopard (Table 1). Among the three main prey species, the RAI was highest for sika deer in both seasons (Table 1). The RAI of human disturbances in summer was higher than winter, and the RAI for cattle were very rare in the winter (Table 1). For small-medium size mammals, the RAI was higher in summer, but only 19 events of raccoon dog were recorded in winter (Table 1). For musk deer, we got 23 events during the study period. Due to the low detections of raccoon dog and musk deer, we excluded the winter data of raccoon dog and the all data of musk deer in the next analysis (Table 1). Spatial overlap The seasonal spatial overlap between leopards and tigers was low and Spearman’s rank correlation coefficients of spatial pattern indicated that overlap was not significant (p>0.05) (Table 2). For three main prey species (wild boar, roe deer, sika deer), spatial overlap between leopards and wild boars was highest in summer, while spatial overlap between leopards and sika deer was highest in winter (Table 2). However, only the seasonal Spearman rank correlation coefficients of spatial pattern between leopards and wild boars were significantly positive (p<0.01) (Table 2). Pianka’s index values between leopards and small-medium size mammals, except raccoon dog, were relatively higher than the three main prey species and the Spearman rank correlation coefficients of spatial patterns were significantly positive (p<0.01) in seasonal periods (Table 2). The low spatial overlap between leopards and human disturbances (Table 2) and correlation coefficients of spatial patterns between leopards and human disturbances varied seasonally. Temporal overlap Leopards were more active in daytime and twilight (Table 3), and they exhibited a peak of activity at approximately 9:00 dur-

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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.

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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.

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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.

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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. Spatial overlap

Paired species

Winter

Amur leopard VS Amur tiger Amur leopard VS Wild boar Amur leopard VS Roe deer Amur leopard VS Sika deer Amur leopard VS Red fox Amur leopard VS Asian badger Amur leopard VS Raccoon dog Amur leopard VS Manchurian hare Amur leopard VS Human activity Amur leopard VS Grazing Amur leopard VS Domestic dog Amur leopard VS Vehicle * **

Summer

Pianka’s index (CI)

SRC

Pianka’s index (CI)

SRC

0.081 (0.013-0.189) 0.171 (0.077-0.326) 0.067 (0.021-0.164) 0.208 (0.091-0.402) 0.344 (0.208-0.499) 0.441 (0.082-0.680) 0.357 (0.108-0.591) 0.062 (0.029-0.124) 0.063 (0.025-0.192) 0.030 (0.003-0.106)

0.044 0.230** -0.055 0.111 0.329** 0.244** 0.201* 0.105 0.149 0.002

0.109 (0.030-0.230) 0.379 (0.171-0.597) 0.317 (0.171-0.510) 0.301 (0.164-0.453) 0.263 (0.130-0.513) 0.372 (0.237-0.537) 0.094 (0.036-0.198) 0.289 (0.142-0.491) 0.093 (0.050-0.187) 0.121 (0.014-0.394) 0.035 (0.013-0.090) 0.024 (0.008-0.057)

-0.042 0.197* 0.04 0.138 0.285** 0.329** 0.052 0.272** -0.114 0.047 -0.138 -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

Amur leopard Amur tiger Wild boar Roe deer Sika deer Red fox Asian badger Raccoon dog Manchurian hare Human activity Grazing Domestic dog Vehicle

Season Winter

Summer

n (wi ) in given time period

n (wi ) in given time period

Diurnal

Nocturnal

Twilight

Diurnal

Nocturnal

Twilight

28 (1.85) 18 (0.49) 46 (1.10) 92 (1.20) 171 (1.31) 11 (0.19) 14 (0.79) 2 (0.03) 886 (2.50) 286 (2.28) 680 (2.25)

5 (0.25) 58 (1.21) 41 (0.75) 71 (0.70) 115 (0.67) 121 (1.62) 28 (1.21) 212 (2.03) 32 (0.07) 26 (0.16) 52 (0.13)

9 (1.29) 25 (1.49) 29 (1.50) 50 (1.41) 76 (1.26) 26 (0.99) 7 (0.14) 7 (0.19) 67 (0.41) 36 (0.62) 105 (0.75)

48 (1.24) 32 (0.43) 270 (0.98) 194 (0.85) 411 (0.99) 13 (0.09) 187 (0.63) 11 (0.13) 15 (0.09) 4517 (1.89) 942 (1.37) 560 (1.79) 3281 (1.81)

10 (0.37) 65 (1.24) 153 (0.79) 127 (0.79) 196 (0.67) 183 (1.80) 327 (1.57) 115 (1.90) 266 (2.25) 68 (0.04) 184 (0.38) 26 (0.12) 94 (0.07)

21 (1.59) 55 (2.17) 139 (1.48) 148 (1.89) 239 (1.70) 99 (2.01) 90 (0.899) 50 (1.70) 62 (1.01) 291 (0.36) 280 (1.19) 53 (0.50) 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

Amur leopard VS Amur tiger Amur leopard VS Wild boar Amur leopard VS Roe deer Amur leopard VS Sika deer Amur leopard VS Red fox Amur leopard VS Asian badger Amur leopard VS Raccoon dog Amur leopard VS Manchurian hare Amur leopard VS Human activity Amur leopard VS Grazing Amur leopard VS Domestic dog Amur leopard VS Vehicle *

Summer

 (CI)

SRC

 (CI)

SRC

0.55 (0.38-0.64) 0.51 (0.50-0.76) 0.73 (0.63-0.85) 0.73 (0.58-0.82) 0.43 (0.36-0.60) 0.59 (0.49-0.77) 0.27 (0.16-0.35) 0.75 (0.61-0.84) 0.81 (0.67-0.90) 0.78 (0.52-0.80)

-0.51** 0.001 0.63** 0.57** -0.83** -0.64** -0.92** 0.86** 0.94** 0.79**

0.67 (0.55-0.78) 0.84 (0.75-0.92) 0.77 (0.67-0.86) 0.82 (0.73-0.90) 0.53 (0.43-0.63) 0.68 (0.59-0.77) 0.49 (0.38-0.59) 0.40 (0.31-0.50) 0.70 (0.61-0.79) 0.88 (0.81-0.94) 0.75 (0.65-0.84) 0.73 (0.64-0.82)

-0.64** 0.36** -0.17** 0.39** -0.93** -0.75** -0.81** -0.86** 0.93** 0.69** 0.95** 0.91**

P < 0.05. ** P < 0.01.

ing both seasons (Figs. 2–4). In contrast, tigers were more active in night and twilight in both seasons (Table 3). The temporal overlap value in winter of both cats was lower than in summer, and the correlation coefficients of peak activity were also significantly negative in both seasons (Table 4). For three prey species, the activ-

ity patterns of them varied in both seasons. In winter, three prey species preferred daytime and twilight. However, they were only active at twilight in summer (Table 3, Fig. 2). The temporal overlap values in winter between leopards and prey species were lower than in summer (Table 4). The synchrony of the times of peak activ-

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ities for pairs of leopards-prey species also varied in both seasons (Table 4, Fig. 2). In winter, activity patterns of small-medium size mammals were more active at night, but they were more active during the night and twilight in summer (Table 3, Fig. 3). The temporal overlap values between leopards and small-medium size mammals were higher in summer than in winter, and the synchrony of the times of peak activities for pairs of them were significantly negative (Table 4). Human disturbances were more prevalent in daytime (Table 3) with the values of temporal overlap between leopards and human disturbances being higher in winter than in summer, and the synchrony of peak activities for pairs of them were significantly positive (Table 4).

Discussion Coexistence of sympatric predators is favoured by partitioning of space, habitat, diet and/or temporal activity patterns (de Almeida Jácomo et al., 2004; Durant, 1998; Karanth and Sunquist, 2000; Palomares et al., 1996; Taber et al., 1997). Dietary partitioning may favour the coexistence between tigers and leopards (Andheria et al., 2007; Karanth and Sunquist, 2000, 1995). However, Lovari et al. (2015) found a great dietary overlap between tiger and leopard in their study area, suggesting that coexistence was locally favoured by other mechanisms rather than prey partitioning, and other studies have emphasised the role of spatiotemporal partitioning (Carter et al., 2015; Karanth and Sunquist, 2010; Ramesh et al., 2012). In particular, leopards have been suggested to avoid tigers by changing niche breadth or space use (Harihar et al., 2011; Mondal et al., 2012; Odden et al., 2010; Schaller, 1967; Seidensticker, 1976; Steinmetz et al., 2013; Sunarto et al., 2015). Amur tigers were most likely to occur in the valley at lower altitudes, which provided easy travel corridors (Carroll and Miquelle, 2006). In NE China, Amur leopards usually use ridge trails more frequently than tigers (Wang et al., 2017). Our results revealed spatial overlap between leopards and tigers was rather low (Table 2) suggesting that leopards avoid tigers by spatial separation (Wang et al., 2017, 2018). Temporal segregation is a mechanism that species of similar niches could use to avoid competition (Hayward and Slotow, 2010; Kronfeld-Schor and Dayan, 2003). Our results that the activity patterns of leopards and tigers vary at different temporal scales support it (Fig. 3). The Amur leopards were more active during daytime in our study area, and their activity peaks were similar in both summer and winter (Table 3; Figs. 2–4). In contrast, the Amur tigers showed nocturnal and crepuscular activity patterns (Table 3; Fig. 2). In Russia, satellite telemetry data showed that Amur tigers were active mostly at twilight (Rozhnov et al., 2011). Our results also support that temporal partitioning between tiger and leopard may allow the coexistence of these sympatric big cats (Steinmetz et al., 2013; Sunarto et al., 2015). The behavioral strategies of big cats are to maximize nutrient intake while to minimize energy expenditure (Sunquist and Sunquist, 1989). Larger predators are inclined to kill larger-bodied prey to achieve the best trade-off (Hayward and Kerley, 2005). Studies in Far Eastern Russia, have confirmed that the food preferences of the Amur leopard were sika deer and roe deer in winter (Kerley et al., 2015; Sugimoto et al., 2016). In this study, we found that leopards-roe deer and leopards-sika deer temporally overlapped more than that to other prey species (Table 4) in winter. Contrary to the predating behaviors, the ecology of fear postulates that herbivores with natural vigilance would minimize the encounter rate with predators by changing their activity patterns or their spatial distribution (Brown et al., 1999). High encounter rates with predators would influence habitat use, activity patterns and the temporal and spatial distribution patterns of the herbivores (Hayward and Kerley, 2005). Although the temporal overlap values

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of leopards-roe deer and leopards-sika deer were high that indicate there may be high encounter rate between leopards and sika deer or roe deer, the relatively low spatial overlap of leopards-roe deer and leopards-sika deer would balance off the actual encounter rate. We speculated that sika deer and roe deer would avoid the leopards spatially in the two seasons. Additionally, most of our camera traps are mounted on the trails where leopard and tiger frequently used but prey may avoid (Jia et al., 2014; Zhu et al., 2011). The spatial-temporal overlap between leopards and wild boars were relatively higher in summer than in winter. We speculated that leopards may avoid adult wild boar in winter and preferred 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 nocturnal and their temporal overlaps with leopards were very low (Table 4). The proportion of small-medium sized mammals contributed less than 20% of leopard diet (Sugimoto et al., 2016), and the spatial-temporal overlaps of leopards small-medium size mammals were not found significant seasonal variation (Tables 2 and 4; Fig. 4), indicating the weak relationships between Amur leopards and those species. We speculated that the avoidance of humans by Amur leopard may limit their distribution and therefore their abundance. The seasonal variation of the spatial-temporal overlaps between leopards and human disturbances indicated the changes of leopards in spatial distribution accordingly (Tables 2 and 4; Fig. 4). Our results support the reports by Carter et al. (2012) that leopards change their spatial distribution or activity patterns to coexist with humans. Wang et al. (2017) indicated that Amur leopards keep away from roads and human settlements, and avoided areas where livestock were abundant. The same type of behaviors of leopards were also found in Nepal (Carter et al., 2015) and Thailand (Ngoprasert et al., 2007). Our results showed there were weak spatial associations and strong temporal overlap between leopards and their main prey. There were high temporal overlaps and low spatial overlaps between leopards and various human disturbances, indicating the leopards may adjust their spatial distribution to minimize interactions with human. It should be noted that the leopard population survived in our study area and neighbouring Sino-Russian transbourdary area, is the single population of the rare leopard, and its area limited to the narrow region of approximately 4,000 km2 (Feng et al., 2017). Obviously, it is threatened by small population size, genetic impoverishment and stochastic events (Sugimoto et al., 2014; Uphyrkina et al., 2002). Now, the Chinese government has been convinced to create a National Park for Amur tigers and Amur leopards covering about 15,000 km2 of forested lands (Feng et al., 2017; McLaughlin, 2016). This may be the last chance to save and restore this critically endangered cat.

Acknowledgements China’s State Forestry Administration approved this study as a part of the long-term Tiger Leopard Observation Network (TLON). Jilin Province Bureau approved permits for the work conducted. Beijing Normal University conducted this study in collaboration with the administrations of the local protected areas. We thank the Jilin Province Forestry Bureau for kindly providing research permits and facilitating fieldwork. We thank Tonggang Chen, Shuyun Peng, Zhanzheng Sun, and Chunze Tan for field data collection. This study was granted by the National Key R&D Program of China (2016YFC0503200), the National Natural Science Foundation of China (31200410, 31210103911, 31421063, 31270567, 31470566 and 31670537) and the National Scientific and Technical Foundation Project of China (2012FY112000).

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References Andheria, A., Karanth, K., Kumar, N., 2007. Diet and prey profiles of three sympatric large carnivores in Bandipur Tiger Reserve, India. Journal of Zoology 273, 169–175. Bromley, G.F., Kucherenko, S.P., Nauka, Moscow, Russia. (in Russian) 1983. Ungulates of the southern part of the Far East[M]. Brown, J.S., Laundré, J.W., Gurung, M., 1999. The ecology of fear: optimal foraging, game theory, and trophic interactions. Journal of Mammalogy 80, 385–399. Bu, H., Wang, F., McShea, W.J., Lu, Z., Wang, D., Li, S., 2016. Spatial Co-Occurrence and Activity Patterns of Mesocarnivores in the Temperate Forests of Southwest China. PloS one 11, e0164271. Carroll, C., Miquelle, D.G., 2006. Spatial viability analysis of Amur tiger Panthera tigris altaica in the Russian Far East: the role of protected areas and landscape matrix in population persistence. Journal of Applied Ecology 43, 1056–1068. Carter, N.H., Shrestha, B.K., Karki, J.B., Pradhan, N.M.B., Liu, J., 2012. Coexistence between wildlife and humans at fine spatial scales. Proceedings of the National Academy of Sciences 109, 15360–15365. Carter, N., Jasny, M., Gurung, B., Liu, J., 2015. Impacts of people and tigers on leopard spatiotemporal activity patterns in a global biodiversity hotspot. Global Ecology and Conservation 3, 149–162. de Almeida Jácomo, A.T., Silveira, L., Diniz-Filho, J.A.F., 2004. Niche separation between the maned wolf (Chrysocyon brachyurus), the crab-eating fox (Dusicyon thous) and the hoary fox (Dusicyon vetulus) in central Brazil. Journal of Zoology 262, 99–106. Durant, S.M., 1998. Competition refuges and coexistence: an example from Serengeti carnivores. Journal of Animal Ecology 67, 370–386. Feng, L., Wang, T., Mou, P., Kou, X., Ge, J., 2011. First image of an Amur leopard recorded in China. Cat News 55. Feng, L., Shevtsova, E., Vitkalova, A., Matyukhina, D., Miquelle, D., Aramilev, V., Wang, T., Mu, P., Xu, R., Ge, J., 2017. Collaboration brings hope for the last Amur leopards. Cat News 65, 20. Foster, V.C., Sarmento, P., Sollmann, R., Torres, N., Jacomo, A.T.A., Negroes, N., Fonseca, C., Silveira, L., 2013. Jaguar and Puma Activity Patterns and Predator-Prey Interactions in Four Brazilian Biomes. Biotropica 45, 373–379. Gerber, B.D., Karpanty, S.M., Randrianantenaina, J., 2012. Activity patterns of carnivores in the rain forests of Madagascar: implications for species coexistence. Journal of Mammalogy 93, 667–676. Harihar, A., Pandav, B., Goyal, S.P., 2011. Responses of leopard Panthera pardus to the recovery of a tiger Panthera tigris population. Journal of Applied Ecology 48, 806–814. Hayward, M.W., Kerley, G.I., 2005. Prey preferences of the lion (Panthera leo). Journal of Zoology 267, 309–322. Hayward, M.W., Slotow, R., 2010. Temporal Partitioning of Activity in Large African Carnivores: Tests of Multiple Hypotheses. South African Journal of Wildlife Research 39, 109–125. Hebblewhite, M., Miguelle, D.G., Murzin, A.A., Aramilev, V.V., Pikunov, D.G., 2011. Predicting potential habitat and population size for reintroduction of the Far Eastern leopards in the Russian Far East. Biological Conservation 144, 2403–2413. Jia, L.I., Yankuo, L.I., Miao, L., Xie, G., Yuan, F., 2014. Impact of Logging upon the Habitat Selection of Sika Deer in Winter in Taohongling National Nature Reserve,China. Sichuan Journal of Zoology. Karanth, K.U., Sunquist, M.E., 1995. Prey selection by tiger, leopard and dhole in tropical forests. Journal of Animal Ecology, 439–450. Karanth, K., Sunquist, M., 2000. Behavioral correlates of predation by tiger, leopard and dhole in Nagarhole National Park, India. Journal of Zoology 250, 255–265. Karanth, K.U., Sunquist, M.E., 2010. Behavioural correlates of predation by tiger (Panthera tigris), leopard (Panthera pardus) and dhole (Cuon alpinus) in Nagarahole, India. Proceedings of the Zoological Society of London 250, 255–265. Kerley, L.L., Mukhacheva, A.S., Matyukhina, D.S., Salmanova, E., Salkina, G.P., Miquelle, D.G., 2015. A comparison of food habits and prey preference of Amur tiger (Panthera tigris altaica) at three sites in the Russian Far East. Integrative zoology 10, 354–364. Kronfeld-Schor, N., Dayan, T., 2003. Partitioning of time as an ecological resource. Annual Review of Ecology. Evolution, and Systematics, 153–181. Linkie, M., Ridout, M., 2011. Assessing tiger–prey interactions in Sumatran rainforests. Journal of Zoology 284, 224–229. Lovari, S., Pokheral, C., Jnawali, S., Fusani, L., Ferretti, F., 2015. Coexistence of the tiger and the common leopard in a prey-rich area: the role of prey partitioning. Journal of Zoology 295, 122–131. Lucherini, M., Reppucci, J.I., Walker, R.S., Villalba, M.L., Wurstten, A., Gallardo, G., Iriarte, A., Villalobos, R., Perovic, P., 2009. Activity Pattern Segregation of Carnivores in the High Andes. Journal of Mammalogy 90, 1404–1409. Manly, B., McDonald, L., Thomas, D., McDonald, T.L., Erickson, W.P., 2007. Springer Science & Business Media. In: Resource selection by animals: statistical design and analysis for field studies. McLaughlin, K., 2016. Tiger land. Science 353, 744–745. Meredith, M., Ridout, M., 2013. overlap: Estimates of Coefficient of Overlapping for Animal Activity Patterns. R package version 0.2. 0. URL: http://CRAN. R-project. org/package= overlap. Mondal, K., Gupta, S., Bhattacharjee, S., Qureshi, Q., Sankar, K., 2012. Response of leopards to re-introduced tigers in Sariska Tiger Reserve, Western India. International Journal of Biodiversity and Conservation 4, 228–236.

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 and behaviour of Asiatic leopard Panthera pardus in Kaeng Krachan National Park, Thailand. Oryx 41, 343–351. Nowell, K., Jackson, P., 1996. Wild cats: status survey and conservation action plan. IUCN Gland. O’Brien, T.G., Kinnaird, M.F., Wibisono, H.T., 2003. Crouching tigers, hidden prey: Sumatran tiger and prey populations in a tropical forest landscape. Animal Conservation 6, 131–139. Odden, M., Wegge, P., Fredriksen, T., 2010. Do tigers displace leopards? If so, why? Ecological Research 25, 875–881. Palomares, F., Ferreras, P., Fedriani, J.M., Delibes, M., 1996. Spatial relationships between Iberian lynx and other carnivores in an area of south-western Spain. Journal of Applied Ecology, 5–13. Pianka, E.R., 1973. The structure of lizard communities. Annual review of ecology and systematics 4, 53–74. Ramesh, T., Kalle, R., Sankar, K., Qureshi, Q., 2012. Spatio-temporal partitioning among large carnivores in relation to major prey species in Western Ghats. Journal of Zoology 287, 269–275. Ridout, M.S., Linkie, M., 2009. Estimating overlap of daily activity patterns from camera trap data. Journal of Agricultural, Biological, and Environmental Statistics 14, 322–337. Rozhnov, V., Hernandez-Blanco, J., Lukarevskiy, V., Naidenko, S., Sorokin, P., Litvinov, M., Kotlyar, A., Pavlov, D., 2011. Application of satellite collars to the study of home range and activity of the Amur tiger (Panthera tigris altaica). Biology Bulletin 38, 834–847. Schaller, G.B., 1967. The Deer and the Tiger. In: A Study of Wildlife in India.[With Plates.]. University of Chicago Press. Schmid, F., Schmidt, A., 2006. Nonparametric estimation of the coefficient of overlapping—theory and empirical application. Computational statistics & data analysis 50, 1583–1596. Seidensticker, J., 1976. On the ecological separation between tigers and leopards. Biotropica, 225–234. Stein, A., Athreya, V., Gerngross, P., Balme, G., Henschel, P., Karanth, U., Miquelle, D., Rostro-Garcia, S., Kamler, J., Laguardia, A., 2017. Panthera pardus. (errata version published in 2016) The IUCN Red List of Threatened Species 2016: e. T15954A102421779. Downloaded on 14. Steinmetz, R., Seuaturien, N., Chutipong, W., 2013. Tigers, leopards, and dholes in a half-empty forest: Assessing species interactions in a guild of threatened carnivores. Biological Conservation 163, 68–78. Sugimoto, T., Aramilev, V.V., Kerley, L.L., Nagata, J., Miquelle, D.G., McCullough, D.R., 2014. Noninvasive genetic analyses for estimating population size and genetic diversity of the remaining Far Eastern leopard (Panthera pardus orientalis) population. Conservation genetics 15, 521–532. Sugimoto, T., Aramilev, V.V., Nagata, J., McCullough, D.R., 2016. Winter food habits of sympatric carnivores, Amur tigers and Far Eastern leopards, in the Russian Far East. Mammalian Biology-Zeitschrift für Säugetierkunde 81, 214–218. Sunarto, S., Kelly, M., Parakkasi, K., Hutajulu, M., 2015. Cat coexistence in central Sumatra: ecological characteristics, spatial and temporal overlap, and implications for management. Journal of Zoology 296, 104–115. Sunquist, M.E., Sunquist, F.C., 1989. Ecological constraints on predation by large felids. In: Carnivore behavior, ecology, and evolution. Springer, pp. 283–301. Taber, A.B., Novaro, A.J., Neris, N., Colman, F.H., 1997. The food habits of sympatric jaguar and puma in the Paraguayan Chaco. Biotropica 29, 204–213. Team, R.C., 2014. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2014. Tian, Y., Wu, J.G., Smith, A.T., Wang, T.M., Kou, X.J., Ge, J.P., 2011. Population viability of the Siberian tiger in a changing landscape: Going, going and gone? Ecological Modelling 222, 3166–3180. 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. Biological Conservation 108, 299–306. Uphyrkina, O., Johnson, W.E., Quigley, H., Miquelle, D., Marker, L., Bush, M., O’Brien, S.J., 2001. Phylogenetics, genome diversity and origin of modern leopard, Panthera pardus. Molecular ecology 10, 2617–2633. Uphyrkina, O., Miquelle, D., Quigley, H., Driscoll, C., O’Brien, S., 2002. Conservation genetics of the Far Eastern leopard (Panthera pardus orientalis). Journal of Heredity 93, 303–311. Wang, T., Feng, L., Mou, P., Wu, J., Smith, J.L., Xiao, W., Yang, H., Dou, H., Zhao, X., Cheng, Y., 2016. Amur tigers and leopards returning to China: direct evidence and a landscape conservation plan. Landscape ecology 31, 491–503. Wang, T., Feng, L., Yang, H., Han, B., Zhao, Y., Juan, L., Lü, X., Zou, L., Li, T., Xiao, W., 2017. A science-based approach to guide Amur leopard recovery in China. Biological Conservation 210, 47–55. Wang, T., Royle, J.A., Smith, J.L., Zou, L., Lü, X., Li, T., Yang, H., Li, Z., Feng, R., Bian, Y., 2018. Living on the edge: Opportunities for Amur tiger recovery in China. Biological Conservation 217, 269–279. Xiao, W.H., Feng, L.M., Zhao, X.D., Yang, H.T., Dou, H.L., Cheng, Y.C., Mou, P., Wang, T.M., Ge, J.P., 2014. Distribution and abundance of Amur tiger, Amur leopard and their ungulate preys in Hunchun National Nature Reserve, Jilin. Biodiversity Science 22, 717–724, in Chinese. Zhu, H.Q., Ge, Z.Y., Chang, S.H., Liu, G., Wu, J.C., Shi, X.J., Xu, J.F., Mao, Z.X., 2011. Winter habitat selection of wild boar (sus scrofa ussuricus) in Huangnihe nature reserve. Chinese Journal of Ecology 30, 734–738.