Spatiotemporal Patterns of Amur Leopards in Northeast China
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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 a 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. © 2018 Deutsche Gesellschaft fur¨ Saugetierkunde.¨ Published by Elsevier GmbH. All rights reserved. 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. 2 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 1616-5047/© 2018 Deutsche Gesellschaft fur¨ Saugetierkunde.¨ Published by Elsevier GmbH. All rights reserved. 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 2 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.