sign in sign up
<<
Home , Asian badger, Leopard cat, Masked palm civet, Mesocarnivore, Siberian weasel

Global and Conservation 21 (2020) e00897

Contents lists available at ScienceDirect

Global Ecology and Conservation

journal homepage: http://www.elsevier.com/locate/gecco

Original Research Article Spatio-temporal coexistence of sympatric with a single apex in a fine-scale landscape

Guojing Zhao a, b, c, d, e, 1, Haitao Yang a, b, c, d, e, 1, Bing Xie a, b, c, d, e, * Yinan Gong a, b, c, d, e, Jianping Ge a, b, c, d, e, Limin Feng a, b, c, d, e, a Northeast and Biodiversity National Observation and Research Station, Normal University, Beijing, 100875, b National Forestry and Administration Key Laboratory for Conservation Ecology of Northeast Tiger and Leopard National Park, Beijing Normal University, Beijing, 100875, China c National Forestry and Grassland Administration Amur Tiger and Monitoring and Research Center, Beijing Normal University, Beijing, 100875, China d Ministry of Education Key Laboratory for Biodiversity Science and Engineering, Beijing Normal University, Beijing, 100875, China e College of Life Sciences, Beijing Normal University, Beijing, 100875, China article info abstract

Article history: Mesocarnivores uniquely and profoundly impact ecosystem function, structure, and dy- Received 23 July 2019 namics. Sympatric tend to spatially and temporally partition limited resources to Received in revised form 22 December 2019 facilitate coexistence. We investigated the seasonal spatial and temporal cooccurrences Accepted 22 December 2019 among six mesocarnivores, the leopard ( bengalensis), red ( vulpes), Asian ( leucurus), Siberian (Mustela sibirica), masked palm Keywords: (Paguma larvata) and yellow-throated (Martes flavigula), as well as a single Camera trap (Northern Chinese leopard, pardus japonensis). We used a camera Sympatric species coexistence trapping dataset collected from June 2016 to May 2017 (16,636 camera trapping days, 52 Activity pattern camera locations). The activity patterns varied among seasons and species. Most species Spatial overlap were most active during summer. were most active in winter. Siberian and yellow-throated were mainly diurnal, tended to spatially avoid each other, and were temporally segregated from the other mesocarnivores. Leopard , Asian , red and masked palm were nocturnal and showed high overlap in every season, but their highest peaks of activity were staggered. Mesocarnivores may be affected by the threat of the apex carnivore; they mainly avoided leopards spatially, showing low spatial overlap with leopards in all seasons. Interestingly, we found that the may engage in temporal-spatial coordination to facilitate coexistence, as increased temporal overlap in a given season was associated with decreased spatial overlap. Our results provide new insight into the carnivore community of terrestrial in northern China and will facilitate future studies on the mechanisms determining the coexistence of species within the trophic cascade. © 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

* Corresponding author. Beijing Normal University, No.19, Xinjiekou Outer Street, Haidian District, Beijing, China. E-mail address: [email protected] (L. Feng). 1 Guojing Zhao and Haitao Yang contributed equally to this work and share first authorship. https://doi.org/10.1016/j.gecco.2019.e00897 2351-9894/© 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/). 2 G. Zhao et al. / Global Ecology and Conservation 21 (2020) e00897

1. Introduction

The coexistence of sympatric species is an important aspect of ecological research, and studies of this type of coexistence are crucial for understanding community diversity (Chesson, 2000; Jonathan Davies et al., 2007; Kondrashov and Kondrashov, 1999; Schoener, 1983; Wisz et al., 2013). The competitive exclusion principle states that two ecologically similar species cannot coexist; consequently, some degree of partitioning may occur in the realized niche of coexisting species (Arias-Del Razo et al., 2011; Davies et al., 2007; Gause, 1934). Ecological character displacement plays an important role of competi- tion in structuring ecological communities (Brown and Wilson, 1956). Due to the niche differentiation that occurs among sympatric species, understanding the coexistence mechanisms of species will contribute to the conservation and manage- ment of ecological communities (Davis et al., 2018; Friedemann et al., 2016; HilleRisLambers et al., 2012; Macarthur and Levins, 1967; Schoener, 1974; Sergio et al., 2003). The temporal niche axis plays an important role in facilitating the coexistence of sympatric species (Carothers and Jaksic, 1984; Di Bitetti et al., 2009; Hayward and Slotow, 2009; Lesmeister et al., 2015; Wang and , 2012; Yang et al., 2018b). Mesocarnivore species at intermediate trophic levels (Prugh et al., 2009) generally show high species richness and diverse resource and habitat use (Roemer et al., 2009). The aggressive interactions among mesocarnivores normally influence their activity patterns and are expected to be stronger for species with high dietary overlap, such as species that usually eat vertebrate prey; for species more prone to interspecific killing; and for species whose relative body size falls within a specific range between 2 and 5.4 (Donadio and Buskirk, 2006; Ritchie and Johnson, 2009; Schoener, 1974). Additionally, lethal encounters are more frequent between species of the same family than between those of different families, which makes important to understand the predisposition of to attack each other (Donadio and Buskirk, 2006; De Oliveira and Pereira, 2014). The activity peaks of most species are asyn- chronous, especially in communities with high diversity (Monterroso et al., 2014; Sunarto et al., 2015). Activity patterns of species are highly variable among regions and across seasons (Noor et al., 2017; Torretta et al., 2015). Daily activity patterns are also internally regulated by the endogenous clocks of species, temperature (Kronfeld-Schor and Dayan, 2003; Zielinski, 2000), light availability and biotic factors (Broekhuis et al., 2013; Yang et al., 2018b); for instance, risk (Yang et al., 2018c)cansignificantly alter the activity of mesocarnivores under pressure from higher trophic levels (Farías et al., 2012; Friedemann et al., 2016; Linkie and Ridout, 2011). Several studies have indicated that the relative abundances of apex and meso-predators are negatively correlated (Berger et al., 2008; Fedriani et al., 1999; Palomares and Caro, 1999; Pasanen-Mortensen et al., 2013). Apex predators are always dominant over and can directly influence mesocarnivores (De Oliveira and Pereira, 2014; Roemer et al., 2009). Mesocarnivores under the influence of apex predators can change their behaviour to avoid negative interactions or be absent from areas where larger predators occur. In such situations, temporal segregation among species is a behavioural adaptation allowing coexistence (Brown et al., 1999; Di Bitetti et al., 2010). Spatial separation is also an important factor that could influence the coexistence of species (Afan et al., 2013; Friedemann et al., 2016; Noor et al., 2017; Robertson et al., 2014). To some extent, the spatial overlap of sympatric species reflects the relationships of the species’ spatial distributions. For instance, microhabitat differences in species distribution allow the coexistence of species with seemingly similar activities and diets (Noor et al., 2017). Animals can modify their spatial under increased competitive interactions with other species, resulting in successful cooccurrence (Kajtoch et al., 2016; Yang et al., 2018c). To determine how different carnivore species coexist under natural conditions, we need to provide evidence for fine-scale temporal and spatial avoidance mechanisms. Research on the coexistence of mesocarnivores is very scarce in China, with only one study conducted in the southwest area of the country (Bu et al., 2016). The Ziwuling Mountains in northwest China harbour abundant terrestrial communities with high species richness. Currently, various mesocarnivores with a single apex predator (Northern Chinese leopard, Panthera pardus japonensis) survive in the landscape (Xie et al., 2018). However, the ecological and behavioural characteristics of these species in this region are completely unknown, which is detrimental to wildlife protection and management. Thus, the main goal of this study was to define the spatial-temporal behaviour of carnivores in northern China to understand their cooccurrence status. We hypothesized that among these mesocarnivores was high; in particular, we expected high segregation between taxonomically related species (such as the and yellow- throated marten). We speculated that mesocarnivores would coexist through spatial and/or temporal separation and fluc- tuate in different seasons. Moreover, we hypothesized that mesocarnivores would make spatial and temporal adjustments in response to apex predators to minimize the probability of encounters with leopards.

2. Study area

We conducted the study in Ziwuling National Nature Reserve (ZNR) (35450-36010 N, 108300-108410 E) and Qiaoshan Provincial Nature Reserve (QNR) (35300-3546 N, 108310-108490 E). This region is located at the junction of the and provinces (Fig. 1). The elevation of this area ranges from 1100 to 1750 m (Zhang, 2014). The zonal vegetation type belongs to the warm temperate broad-leaved of northern China, which is windy in spring and cold and prone to drought in winter (Liu, 2004; Zhang, 2014). Based on the local climate characteristics, we divided the year into four seasons (winter: DeceFeb; spring: MareMay; summer: JuneAug; autumn: SepeNov). The ZNR is in the northern part of the study area; here, human activity is very rare, and forestry workers frequently patrol the area. In contrast, the QNR is in the south of G. Zhao et al. / Global Ecology and Conservation 21 (2020) e00897 3

Fig. 1. Study areas and survey locations in the Ziwuling National Nature Reserve and Qiaoshan Provincial Nature Reserve, China.

the study area; here, human activity and oil operations are common, while livestock is uncommon (Gao et al., 2014). The area harbours various mesocarnivores, including the , , , ( pro- cyonoides), Siberian weasel, and yellow-throated marten, as well as a large carnivore, the Northern Chinese leopard (Xie et al., 2018).

3. Data collection

We established 52 camera traps in the gridded study area to monitor the leopard and mesocarnivores (Fig. 1). Generally, in each grid cell (4 * 4 km), 2 camera traps were placed along a road, trail or ridge, which are natural routes for animals. The cameras were fastened to trees 40e80 cm above the ground and programmed to shoot 15-sec videos with a 1-min interval between consecutive events (Yang et al., 2018c). The camera traps were implemented 24 h per day throughout the year. We visited each camera monthly to download the videos and check the batteries. We counted the number of species- independent events per 100 camera-days, that is, the relative abundance index number (RAI), to measure the abundance of each species. The independent event judgement criteria were as follows: (1) different individuals; (2) videos of the same individual taken at a minimum time interval of 30 min; (3) discontinuous videos of the same individual. A video meeting any of these criteria was considered an independent event (O’Brien et al., 2003). 4 G. Zhao et al. / Global Ecology and Conservation 21 (2020) e00897

4. Data analysis

4.1. Daily activity patterns and overlaps

Camera traps can record temporal information associated with species activity, so we were able to further analyse the activity patterns of species. We used Moonrise 3.5 software to determine the exact sunrise and sunset times. Each day was divided into three main periods: diurnal, nocturnal and crepuscular (1 h before sunrise and 1 h after sunset) (Foster and Silveira, 2013). We followed the procedures of (Ridout and Linkie, 2009) to quantify the overlap of carnivore activity pat- terns. The first step included the separate estimation of the probability density function based on the nonparametric kernel density. We used the distribution function for pairwise comparisons of the carnivores’ activity patterns. In the second step, the coefficient of overlap (D, which ranges from 0 (no overlap) to 1 (complete overlap)) 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 estimation methods; we used D1 for small sample sizes (D < 75) and D4 for larger sample sizes (D 75). The 95% confidence intervals were obtained using 10,000 bootstrap samples. Statistical analyses were completed using the “overlap” package (Meredith and Ridout, 2014) in R (version 3.1.2) (Team, 2014).

4.2. Spatial distribution overlap

To investigate the spatial overlap (Pianka, 1973), we calculated the relative abundance index (RAI) for each trap site as the number of detections per 100 camera-trap days for every species in the four seasons (O’Brien et al., 2003). We considered each camera site as spatially independent and used the RAI for each camera site to calculate the spatial overlap index (Pianka’sO index). Pairwise species spatial overlap analysis was performed in R (Team, 2014) using the “spaa” package (Zhang et al., 2013).

5. Results

We collected 4021 independent videos and recorded one apex predator (leopard) and seven mesocarnivores in our study area during 16,636 trap days (spring: 4088; summer: 4354; autumn: 3782; winter: 4412) (Table 1). The dataset of raccoon was too small for further analysis. Most of the mesocarnivores in our study were most active during the summer, except for the red fox, which was most active in autumn (Fig. 2). In winter, the RAI of the Asian badger and Siberian weasel were near zero, and we did not detect the masked palm civet. In contrast, the activity of leopards was highest in winter and lowest in summer (Fig. 2).

5.1. Daily activity patterns and temporal overlap

Across the different seasons, the trends in the daily activity patterns of the seven animal species were roughly the same, but there were differences in the appearance of the highest activity peak. Leopards were mainly diurnal and crepuscular. Leopard cats and red foxes were both more active during night than during daytime. The Asian badger and masked palm civet were nocturnal and had one peak of activity in each of the three seasons. The Siberian weasel was diurnal. The yellow- throated marten was mainly active during the day and crepuscular (Fig. 3). To further observe the differences in the four nocturnal animals (leopard cats, Asian badgers, red foxes and masked palm civets), we compared their activities in the same season (Fig. 4). The highest activity peak was staggered across the four different species and varied with the seasons. In the pairwise analysis of species, we found that the leopard cat, Asian badger, red fox and masked palm civet all showed high overlap in every season, with the leopard cat and red fox showing the highest level of overlap (Fig. 5). These four species exhibited low overlap with the Siberian weasel and yellow-throated marten, but the Siberian weasel and yellow-throated marten showed high overlap. Overall, leopards showed low temporal overlap with leopard cats and masked palm civets and high temporal overlap with the other four mesocarnivores. Excluding winter, leopard cats, Asian badgers, red foxes and masked palm civets all had the

Table 1 Numbers of independent detections of leopards and mesocarnivores in four seasons during June 2016eMay 2017 in Ziwuling National Nature Reserve and Qiaoshan Provincial Nature Reserve, China.

Spring Summer Autumn Winter Total Leopard 94 66 80 106 346 Leopard cat 81 151 140 46 418 Asian Badger 798 755 542 9 2104 0 6 3 0 9 Red Fox 169 189 350 181 889 Siberian Weasel 16 48 29 3 96 Masked Palm Civet 28 32 21 0 81 Yellow-Throated Marten 10 29 25 14 78 G. Zhao et al. / Global Ecology and Conservation 21 (2020) e00897 5

Fig. 2. Relative abundance index (RAI, the number of species-independent events per 100 camera-days) values of seven animals in different seasons during June 2016eMay 2017 in Ziwuling National Nature Reserve and Qiaoshan Provincial Nature Reserve, China. (The animal pictures in the text all represent the same species as those shown in this figure (a~g)).

Fig. 3. Daily activity patterns of seven animals in different seasons during June 2016eMay 2017 in Ziwuling National Nature Reserve and Qiaoshan Provincial Nature Reserve, China (the vertical lines indicate the times of sunrise and sunset).

highest temporal overlap with leopards in spring and the lowest overlap with leopards in summer. Siberian weasels and yellow-throated martens had the highest overlap with leopards in summer and the lowest overlap with leopards in spring (Fig. 5, Table 4).

5.2. Spatial distribution overlap

The Siberian weasel and the other five mesocarnivores had low spatial overlap. However, the spatial overlap of pairs of four mesocarnivores (leopard cat, Asian badger, red fox and masked palm civet) were relatively high, with the exception of the Asian badger and masked palm civet (Table 2). 6 G. Zhao et al. / Global Ecology and Conservation 21 (2020) e00897

Fig. 4. Daily activity patterns of four nocturnal mesocarnivores (LC - leopard cat; HB - Asian badger; RF - red fox; MPC - masked palm civet) in four seasons during June 2016eMay 2017 in Ziwuling National Nature Reserve and Qiaoshan Provincial Nature Reserve. The vertical lines indicate the times of sunrise and sunset. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

Of the different seasons, the spatial overlap of all six mesocarnivores with leopards was highest in autumn. Leopards had the lowest spatial overlap with leopard cats and Asian badgers in spring and the lowest spatial overlap with the other four mesocarnivores in summer (Table 2, Table 4). We picked species pairs with high spatial and temporal overlaps and then compared their temporal and spatial overlaps in different seasons. When the temporal (spatial) overlap was the highest, the spatial (temporal) overlap was the lowest. Like the leopard cats and Asian badgers, leopard cats and red foxes had the highest temporal overlap and the lowest spatial overlap in summer and the lowest temporal overlap and the highest spatial overlap in autumn (Table 3).

6. Discussion

This study provides the first information on the coexistence of the mesocarnivore community in northern China, which will be meaningful for the conservation of local species. The coexistence of sympatric species could be affected by many factors. We investigated basic information at temporal and spatial scales, but other aspects of mesocarnivore coexistence will require further discussion. RAI and spatial overlap index values were used to show the spatial relationships among species, but these metrics have limitations that must be improved in the future. The RAI values of the species varied among seasons, and we recorded the highest detectability of all mesocarnivores, except for the red fox, during summer. This result was likely due to the diversity of food resources in summer (Goszczynski et al., 2005; Hartova-Nentvichov a et al., 2010; Kowalczyk et al., 2003). Red foxes were most active in autumn, which may be linked to the dispersal of red foxes during this season. Small red foxes begin to actively search for food independently (Smith and Xie, 2010). The low detection of the Asian badger, Siberian weasel and masked palm civet during winter may be due to G. Zhao et al. / Global Ecology and Conservation 21 (2020) e00897 7

Fig. 5. Values of temporal overlap for species pairs between seven animals in four seasons (spring - green row; summer - orange row; autumn - yellow row; winter - white row) during June 2016eMay 2017 in the Ziwuling National Nature Reserve and Qiaoshan Provincial Nature Reserve, China. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

their biorhythms, behavioural adaptations that reduce activity or cause hibernation at low temperatures, which has also been observed in other areas (Goszczynski et al., 2005; Kowalczyk et al., 2003; Maurel and Boissin, 2008; Torretta et al., 2015). In contrast, leopards showed the lowest activity in summer and the highest activity in winter. This may be because it is easy to obtain food with a small amount of activity in summer, while in the winter, food is scarce, making it necessary for leopards to increase their time and frequency of foraging. The daily activity patterns of carnivores differ and may depend on their endogenous clock (Kronfeld-Schor and Dayan, 2003) and other factors. In our study area, we observed that leopard cats, Asian badgers and red foxes were all nocturnal, the activity of masked palm civets started after sunset and stopped before sunrise, yellow-throated martens showed active diurnal and some crepuscular activity, and Siberian weasels were diurnal, which was consistent with some previous reports (Barrull et al., 2014; Bu et al., 2016; Chen et al., 2009; Goszczynski et al., 2005; Grassman et al., 2005; Johnson et al., 2009; Kowalczyk et al., 2003; Monterroso et al., 2014; Noor et al., 2017; Prater, 1980; Torretta et al., 2015) but differed from some others, as masked palm civets were observed to have a peak in activity between 08:00 and 12:00 (Zhou et al., 2014), yellow- throated martens can hunt completely during the daytime (Bu et al., 2016; Chiang et al., 2012; Noor et al., 2017), and Siberian weasels were found to lack a distinct daily activity pattern in the warm season but became nocturnal in the winter (Bu et al., 2016) or were nocturnal and active during the daytime in regions where flourish (Smith and Xie, 2010). These dif- ferences in results may be due to geographical differences and the influence of climates, as some species may be active longer in warm regions than in cold regions (Goszczynski et al., 2005; Kowalczyk et al., 2003). Additionally, carnivore activity patterns may be affected by the daytime temperature (Zielinski et al., 1983). We also observed that the leopard cat, Asian 8 G. Zhao et al. / Global Ecology and Conservation 21 (2020) e00897

Table 2 Spatial overlap index values for species pairs in four seasons (Pianka’s O index (mean (range))) during June 2016eMay 2017 in Ziwuling National Nature Reserve and Qiaoshan Provincial Nature Reserve, China.

Pairwise species Spring Summer Autumn Winter

Pianka’s O Pianka’s O Pianka’s O Pianka’sO L-LC 0.17 (0.08e0.328) 0.266 (0.163e0.589) 0.533 (0.283e0.722) 0.178 (0.049e0.412) L-HB 0.225 (0.122e0.423) 0.242 (0.152e0.494) 0.345 (0.162e0.693) e L-RF 0.375 (0.24e0.604) 0.17 (0.024e0.624) 0.553 (0.327e0.716) 0.415 (0.187e0.666) L-SW 0.249 (0.116e0.497) 0.108 (0.032e0.438) 0.304 (0.102e0.62) e L-MPC 0.167 (0.045e0.365) 0.074 (0.009e0.435) 0.326 (0.071e0.584) e L-YTM 0.189 (0.016e0.392) 0.064 (0.007e0.349) 0.406 (0.127e0.673) 0.049 (0e0.193) LC-HB 0.461 (0.214e0.707) 0.366 (0.281e0.55) 0.528 (0.397e0.725) e LC-RF 0.54 (0.142e0.84) 0.153 (0.068e0.372) 0.764 (0.377e0.908) 0.379 (0.212e0.587) LC-SW 0.269 (0.038e0.551) 0.358 (0.108e0.685) 0.229 (0.07e0.527) e LC-MPC 0.496 (0.157e0.773) 0.147 (0.047e0.521) 0.411 (0.157e0.704) e LC-YTM 0.342 (0e0.674) 0.129 (0.025e0.394) 0.569 (0.162e0.787) 0.022 (0e0.126) HB-RF 0.22 (0.135e0.39) 0.493 (0.154e0.764) 0.338 (0.173e0.688) 0.293 (0.013e0.642) HB-SW 0.133 (0.057e0.328) 0.417 (0.23e0.653) 0.37 (0.194e0.61) e HB-MPC 0.315 (0.076e0.639) 0.281 (0.065e0.751) 0.35 (0.146e0.634) e HB-YTM 0.188 (0.04e0.4) 0.323 (0.107e0.609) 0.236 (0.09e0.605) e RF-SW 0.068 (0.002e0.275) 0.083 (0.01e0.326) 0.227 (0.09e0.529) e RF-MPC 0.506 (0.225e0.816) 0.411 (0.047e0.938) 0.296 (0.121e0.555) e RF-YTM 0.506 (0.04e0.813) 0.384 (0.003e0.835) 0.767 (0.471e0.882) 0.464 (0.199e0.861) SW-MPC 0.032 (0e0.158) 0.151 (0.028e0.634) 0.359 (0.167e0.687) e SW-YTM 0 (0e0) 0.173 (0e0.568) 0.268 (0.038e0.514) e MPC-YTM 0.501 (0.291e0.762) 0.229 (0.012e0.827) 0.451 (0.232e0.671) e

Note: L e leopard; LC - leopard cat; HB - Asian badger; RF - red fox; SW - Siberian weasel; MPC - masked palm civet; YTM - yellow-throated marten.

Table 3 Temporal overlap and spatial overlap for species pairs in three seasons during June 2016eMay 2017 in Ziwuling National Nature Reserve and Qiaoshan Provincial Nature Reserve, China.

Temporal overlap (from high to low) Spatial overlap (from high to low) LC-HB summer; spring; autumn autumn; spring; summer LC-RF summer; spring; autumn autumn; spring; summer HB-RF spring; autumn; summer summer; autumn; spring LC-MPC summer; spring; autumn spring; autumn; sunnmer RF-MPC summer; antumn; spring spring; summer; autumn HB-MPC antumn; summer; spring autumn; spring; summer SW-YTM summer; spring; autumn autumn; summer; spring

Note: LC-leopard cat; HB-Asian badger; RF-red fox; SW-Siberian weasel; MPC-masked palm civet; YTM-yellow-throated marten.

Table 4 Temporal overlap and spatial overlap for each mesocarnivore and leopard pair in three seasons during June 2016eMay 2017 in Ziwuling National Nature Reserve and Qiaoshan Provincial Nature Reserve, China.

Temporal overlap (from high to low) Spatial overlap (from high to low) L-LC spring; autumn; summer autumn; summer; spring L-HB spring; autumu; summer autumn; summer; spring L-RF spring; autumu; summer autumn; spring; summer L-MPC spring; autumu; summer autumn; spring; summer L-YTM summer; autumn; spring autumn; spring; summer L-SW summer; autumn; spring autumn; spring; summer

Note: L-leopard; LC-leopard cat; HB-Asian badger; RF-red fox; SW-Siberian weasel; MPC-masked palm civet; YTM-yellow-throated marten.

badger and red fox increased their time of activity at noon or in the afternoon during autumn or winter. This might occur because the air is cold during autumn and winter, so the animals increased their activity during periods of the day with the highest temperatures. The variation in activity patterns across different sites may be attributed to the broad flexibility and adaptability of animals. Sympatric mesocarnivores can promote coexistence through temporal and spatial separation or coordination among species (Monterroso et al., 2013). St. Pierre et al. (2006) indicated that sympatric Siberian weasels and yellow-throated martens had a high degree of diet overlap (i.e., small mammals). The smaller Siberian weasel may avoid the larger, diurnal yellow-throated marten by being more active at night (Chiang et al., 2012). In contrast, these two species may avoid each other spatially, with low spatial overlap in our study area, as they were both diurnal and had high temporal overlap. Siberian weasels and yellow-throated martens may show temporal separation from the other four nocturnal species. Moreover, due to G. Zhao et al. / Global Ecology and Conservation 21 (2020) e00897 9 its relatively small body size, the Siberian weasel may have avoided the other animals, as the temporal and spatial overlap between them were both low; the Siberian weasel can be 2e4 times smaller than the other animals, which increases interference competition. The other four nocturnal mesocarnivores had high temporal overlap, and their spatial overlap was not low (expect for the overlap between the Asian badger and masked palm civet). Additionally, the leopard cat, Asian badger and red fox may experience greater competition, since they have similar food resources (Zhang et al., 2011). The masked palm civet primarily consumes fruits (Bu et al., 2016), and food differentiation may facilitate its coexistence with other meso- carnivores. In addition, the activity peaks of the mesocarnivores were staggered, even though they were all active at night. The leopard cat and red fox had one more activity peak than the Asian badger. The activity peak of leopard cats was approximately 1.5 h later than that of Asian badgers in three seasons. This variation in the activity peak times may facilitate the coexistence of these species. Furthermore, we found that animals may engage in temporal-spatial coordination to reduce their overall niche overlap (Table 3), and when the temporal overlap increases in a given season, the spatial overlap decreases, especially for the leopard cat, Asian badger and red fox, which had different temporal and spatial overlaps over the three seasons. For these species, there is no season in which the temporal and spatial overlap are both at their highest value. This trend further promotes their coexistence. In addition, there may be other niche-scale dimensions that need further research. Mesocarnivores may be affected by the threat of an apex predator, and they may reduce this risk by avoiding large predators at spatial and/or temporal scales. The spatial overlap of all six mesocarnivores and leopards was highest in autumn. Scavenging may provide alternative resources for carnivores during seasons with a food shortage (Yang et al., 2018a), under stressful environmental conditions or during other critical periods (Selva et al., 2005; Wikenros et al., 2014) and hence may result in an increase in spatial overlap. As indicated by the “ecology of fear”, prey modify their behaviour by striking a balance between their need to forage and their need to avoid large predators (Brown et al., 1999). Consequently, this trade-off may result in the avoidance of food-rich habitat patches, either spatially or temporally, which remain unoccupied by prey species when these patches are also associated with significantly high predation risks (Linkie and Ridout, 2011). The mesocarnivores in our study may mainly avoid large predators spatially because they all had low spatial overlap with leopards in all seasons; in contrast, all mesocarnivores, especially Asian badgers, red foxes, Siberian weasels and yellow-throated martens, had high temporal overlap with leopards. In addition, relative temporal-spatial coordination may reduce their predation risk. Some species exhibited the lowest spatial overlap and the highest temporal overlap in one season (Leopard cat, spring; Asian badger, spring; Siberian weasel, summer; yellow-throated marten; summer). The seasonal temporal and/or spatial transition may represent behavioural adaptations of mesocarnivores to reduce their risk of being prey and competition. Overall, our study showed that mesocarnivores may benefit from seasonal temporal-spatial coordination among species. Promoting coexistence and reducing aggressive interactions may be achieved by adjustments along one or more niche di- mensions, reducing the overall potential ecological risk of each competing species within biodiverse communities (Linnell and Strand, 2000; Chesson, 2000; Barrull et al., 2014).

Funding information

National Natural Science Foundation of China (31670537, 31200410, 31800452); National Scientific and Technical Foun- dation Project of China (2012FY112000); Cyrus Tang Foundation (2016) and Doctoral Fund of Ministry of Education of China (2019M653714).

Declaration of competing interest

The authors declare no conflict of interest.

Acknowledgments

We sincerely thank the National Forestry and Grassland Administration, Shaanxi Forestry Administration, Yan’an Forestry Administration and Ziwuling National Nature Reserve Administration for kindly providing research permits and facilitating fieldwork. We also thank Jinlong Gao, Min Gu, Shengping Jia, Zhiqi Gao, Chenghao Wu, Yazhou Wang, Xiangzhong Liu, Wei Wang and Hui Liu for data collection in the field. This work was supported by grant from the National Natural Science Foundation of China (31670537, 31200410, 31800452); National Scientific and Technical Foundation Project of China (2012FY112000); Cyrus Tang Foundation (2016) and Doctoral Fund of Ministry of Education of China (2019M653714).

References

Afan, I., Navarro, J., Cardador, L., Ramírez, F., Kato, A., Rodríguez, B., Ropert-Coudert, Y., Forero, M.G., 2013. Foraging movements and habitat niche of two closely related seabirds breeding in sympatry. Mar. Biol. 161 (3), 657e668. https://doi:10.1007/s00227-013-2368-4. Arias-Del Razo, I., Hernandez, L., Laundre, J.W., Myers, O., 2011. Do predator and prey foraging activity patterns match? A study of ( latrans), and lagomorphs (Lepus californicus and Sylvilagus audobonii). J. Arid Environ. 75 (2), 112e118. https://doi:10.1016/j.jaridenv.2010.09.008. Barrull, J., Mate, I., Ruiz-Olmo, J., Casanovas, J.G., Gosalbez, J., Salicrú, M., 2014. Factors and mechanisms that explain coexistence in a Mediterranean carnivore assemblage: an integrated study based on camera trapping and diet. Mamm. Biol. 79 (2), 123e131. https://doi:10.1016/j.mambio.2013.11.004. Berger, K.M., Gese, E.M., Berger, J., 2008. Indirect effects and traditional trophic cascades: a test involving , coyotes, and pronghorn, 89, pp. 818e828, 3. https://doi:10.1890/07-0193.1. 10 G. Zhao et al. / Global Ecology and Conservation 21 (2020) e00897

Broekhuis, F., Cozzi, G., Valeix, M., McNutt, J.W., Macdonald, D.W., 2013. Risk avoidance in sympatric large carnivores: reactive or predictive? J. Anim. Ecol. 82 (5), 1098e1105. https://doi:10.1111/1365-2656.12077. Brown, J.S., Laundre, J.W., Gurung, M., 1999. The ecology of fear: optimal foraging, game theory, and trophic interactions. J. Mammal. 80 (2), 385e399. https://doi:10.2307/1383287. Brown, W.L., Wilson, E.O.J., 1956. Character displacement. Syst. Zool. 5 (2), 49e64. http://doi:10.2307/2411924. 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 of southwest China. PLoS One 11 (10), e0164271. https://doi:10.1371/journal.pone.0164271. Carothers, J.H., Jaksic, F.M., 1984. Time as a niche difference: the role of interference competition. Oikos 42 (3), 403e406. https://doi:10.2307/3544413. Chen, M.T., Tewes, M.E., Pei, K.J., Grassman, L.I., 2009. Activity patterns and habitat use of sympatric small carnivores in southern . Mammalia 73 (1), 20e26. https://doi:10.1515/mamm.2009.006. Chesson, P., 2000. Mechanisms of Maintenance of Species Diversity 31 (1), 343e366. https://doi:10.1146/annurev.ecolsys.31.1.343. Chiang, P.J., Pei, K.J.C., Vaughan, M.R., Li, C.F., 2012. Niche relationships of carnivores in a subtropical primary forest in southern Taiwan. Zool. Stud. 51 (4), 500e511. Davies, T.J., Meiri, S., Barraclough, T.G., Gittleman, J.L., 2007. Species co-existence and character divergence across carnivores. Ecol. Lett. 10 (2), 146e152. https://doi:10.1111/j.1461-0248.2006.01005.x. Davis, C.L., Rich, Lindsey N., Farris, Z.J., Kelly, M.J., Di Bitetti, M.S., Blanco, Y.D., Albanesi, S., Farhadinia, Mohammad S., Gholikhani, N., Hamel, S., Harmsen, B.J., Wultsch, C., Kane, M.D., Martins, Q., Murphy, A.J., Steenweg, R., Sunarto, S., Taktehrani, A., Thapa, K., Tucker, J.M., Whittington, J., Widodo, F.A., Yoccoz, N. G., Miller, D.A.W., 2018. Ecological correlates of the spatial co-occurrence of sympatric mammalian carnivores worldwide, 21, pp. 1401e1412, 9. https:// doi:10.1111/ele.13124. De Oliveira, T.G., Pereira, J.A., 2014. and interspecific killing as structuring forces of carnivoran communities in south America. J. Mamm. Evol. 21 (4), 427e436. https://doi:10.1007/s10914-013-9251-4. Di Bitetti, M.S., De Angelo, C.D., Di Blanco, Y.E., Paviolo, A., 2010. Niche partitioning and species coexistence in a Neotropical felid assemblage. Acta Oecol. 36 (4), 403e412. https://doi:10.1016/j.actao.2010.04.001. Di Bitetti, M.S., Di Blanco, Y.E., Pereira, J.A., Paviolo, A., Perez, I.J., 2009. Time partitioning favors the coexistence of sympatric crab- foxes (Cerdocyon thous) and pampas foxes (Lycalopex gymnocercus). J. Mammal. 90 (2), 479e490. https://doi:10.1644/08-MAMM-A-113.1. Donadio, E., Buskirk, S.W., 2006. Diet, morphology, and interspecific killing in . Am. Nat. 167 (4), 524e536. https://doi:10.1086/501033. Farías, V., Fuller, T.K., Sauvajot, R.M., 2012. Activity and distribution of gray foxes ( cinereoargenteus) in southern California. Southwest. Nat. 57 (2), 176e181. https://doi:10.1894/0038-4909-57.2.176. Fedriani, J.M., Palomares, F., Delibes, M., 1999. Niche relations among three sympatric Mediterranean carnivores. Oecologia 121 (1), 138e148. https://doi:10. 1007/s004420050915. Foster, V.C., Silveira, L., 2013. and activity patterns and predator-prey interactions in four Brazilian biomes. Biotropica 45 (3), 373e379. https:// doi:10.1111/btp.12021. Friedemann, G., Leshem, Y., Kerem, L., Shacham, B., Bar-Massada, A., McClain, K.M., Bohrer, G., Izhaki, I., 2016. Multidimensional differentiation in foraging resource use during breeding of two sympatric top predators. Sci. Rep. 6, 35031. https://doi:10.1038/srep35031. Gao, Y., Dang, K., Fu, X., 2014. The range and function adjustment of Qiaoshan Nature Reserve (in Chinese with English abstract). Shaanxi Forest Science and Technology (5), 51e54. Gause, G.F., 1934. Experimental analysis of Vito Volterra’s mathematical theory of the struggle for existence. Science 79 (2036), 16e17. Goszczynski, J., Juszko, S., Pacia, A., Skoczynska, J., 2005. Activity of badgers (Meles meles) in Central Poland. Mamm. Biol. 70 (1), 1e11. https://doi:10.1078/ 1616-5047-00171. Grassman, L.I., Tewes, M.E., Silvy, N.J., 2005. Ranging, habitat use and activity patterns of Arctictis binturong and yellow-throated marten Martes flavigula in north-central . Wildl. Biol. 11 (1), 49e57. https://doi:10.2981/0909-6396(2005)11[49:RHUAAP]2.0.CO;2. Hartova-Nentvichov a, M., Salek, M., Cervený, J., Koubek, P., 2010. Variation in the diet of the red fox (Vulpes vulpes) in mountain habitats: effects of altitude and season. Mamm. Biol. 75 (4), 334e340. https://doi:10.1016/j.mambio.2009.09.003. Hayward, M.W., Slotow, R., 2009. Temporal partitioning of activity in large African carnivores: tests of multiple hypotheses. S. Afr. J. Wildl. Res. 39 (2), 109e125. https://doi:10.3957/056.039.0207. HilleRisLambers, J., Adler, P.B., Harpole, W.S., Levine, J.M., Mayfield, M.M., 2012. Rethinking community assembly through the lens of coexistence theory. Annu. Rev. Ecol. Evol. Syst. 43 (1), 227e248. https://doi:10.1146/annurev-ecolsys-110411-160411. Johnson, A., Vongkhamheng, C., Saithongdam, T., 2009. The diversity, status and conservation of small carnivores in a montane tropical forest in northern . Oryx 43, 04. https://doi:10.1017/s0030605309990238. Jonathan Davies, T., Meiri, S., Barraclough, T.G., Gittleman, J.L., 2007. Species co-existence and character divergence across carnivores, 10, pp.146e152, 2. https://doi:10.1111/j.1461-0248.2006.01005.x. Kajtoch, Ł., Matysek, M., Figarski, T., 2016. Spatio-temporal patterns of owl territories in fragmented forests are affected by a top predator (). Ann. Zool. Fenn. 53 (3e4), 165e174. https://doi:10.5735/086.053.0405. Kondrashov, A.S., Kondrashov, F.A., 1999. Interactions among quantitative traits in the course of sympatric speciation. Nature 400 (6742), 351e354. https:// doi:10.1038/22514. Kowalczyk, R., Je¸ drzejewska, B., Zalewski, A., 2003. Annual and circadian activity patterns of badgers (Meles meles) in Białowieza_ Primeval Forest (eastern Poland) compared with other Palaearctic populations. J. Biogeogr. 30 (3), 463e472. https://doi:10.1046/j.1365-2699.2003.00804.x. Kronfeld-Schor, N., Dayan, T., 2003. Partitioning of time as an ecological resource. Annu. Rev. Ecol. Evol. Syst. 34 (1), 153e181. https://doi:10.1146/annurev. ecolsys.34.011802.132435. Lesmeister, D.B., Nielsen, C.K., Schauber, E.M., Hellgren, E.C., 2015. Spatial and temporal structure of a mesocarnivore guild in midwestern . Wildl. Monogr. 191 (1), 1e61. https://doi:10.1002/wmon.1015. Linkie, M., Ridout, M.S., 2011. Assessing tiger-prey interactions in Sumatran rainforests. J. Zool. 284 (3), 224e229. https://doi:10.1111/j.1469-7998.2011. 00801.x. Linnell, J.D., Strand, O., 2000. Interference interactions, coyexistence and conservation of mammalian carnivores. Divers. Distrib. 6 (4), 169e176. http://doi: 10.1046/j.1472-4642.2000.00069.x. Liu, S.M., 2004. Climate characteristics of ziwuling nature Reserve in Shaanxi province (in Chinese with English abstract). Arid Zone Res. 21 (4), 466e469. https://doi:10.13866/j.azr.2004.04.035. Macarthur, R., Levins, R., 1967. The limiting similarity, convergence, and divergence of coexisting species. Am. Nat. 101 (921), 377e385. https://doi:10.1086/ 282505. Maurel, D., Boissin, J., 2008. Seasonal rhythms of locomotor activity and thyroid function in male badgers(Meles melesL.). J. Interdiscip. Cycle Res. 14 (4), 285e303. https://doi:10.1080/09291018309359823. Meredith, M., Ridout, M., 2014. Overlap: Estimates of Coefficient of Overlapping for Animal Activity Patterns. R Package Version 0.2. 4. Monterroso, P., Alves, P.C., Ferreras, P., 2014. Plasticity in circadian activity patterns of mesocarnivores in Southwestern : implications for species coexistence. Behav. Ecol. Sociobiol. 68 (9), 1403e1417. https://doi:10.1007/s00265-014-1748-1. Monterroso, P., Alves, P.C., Ferreras, P., Fusani, L., 2013. Catch me if you can: diel activity patterns of mammalian prey and predators. Ethology 119 (12), 1044e1056. https://doi:10.1111/eth.12156. Noor, A., Mir, Z.R., Veeraswami, G.G., Habib, B., 2017. Activity patterns and spatial co-occurrence of sympatric mammals in the moist temperate forest of the Himalaya, . Folia Zoologica 66 (4), 231e241. https://doi:10.25225/fozo.v66.i4.a4.2017. G. Zhao et al. / Global Ecology and Conservation 21 (2020) e00897 11

O’Brien, T.G., Kinnaird, M.F., Wibisono, H.T., 2003. Crouching , hidden prey: sumatran tiger and prey populations in a tropical forest landscape. Anim. Conserv. 6 (2), 131e139. https://doi:10.1017/S1367943003003172. Palomares, F., Caro, T.M., 1999. Interspecific killing among mammalian carnivores. Am. Nat. 153 (5), 492e508. https://doi:10.1086/303189. Pasanen-Mortensen, M., Pyykonen,€ M., Elmhagen, B., 2013. Where prevail, foxes will fail - limitation of a in Eurasia. Glob. Ecol. Biogeogr. 22 (7), 868e877. https://doi:10.1111/geb.12051. Pianka, E.R., 1973. The structure of lizard communities. Annu. Rev. Ecol. Systemat. 4 (1), 53e74. https://doi:10.1146/annurev.es.04.110173.000413. Prater, S., 1980. The Book of Indian Animals bombay Natural History Society and Oxford University Press (Mumbai). Prugh, L.R., Stoner, C.J., Epps, C.W., Bean, W.T., Ripple, W.J., Laliberte, A.S., Brashares, J.S., 2009. The rise of the mesopredator. Bioscience 59 (9), 779e791. Ridout, M.S., Linkie, M., 2009. Estimating overlap of daily activity patterns from camera trap data. J. Agric. Biol. Environ. Stat. 14 (3), 322e337. https://doi:10. 1198/jabes.2009.08038. Ritchie, E.G., Johnson, C.N., 2009. Predator interactions, mesopredator release and biodiversity conservation 12 (9), 982e998. https://doi:10.1111/j.1461- 0248.2009.01347.x. Robertson, G.S., Bolton, M., Grecian, W.J., Wilson, L.J., Davies, W., Monaghan, P., 2014. Resource partitioning in three congeneric sympatrically breeding seabirds: foraging areas and prey utilization. Auk 131 (3), 434e446. https://doi:10.1642/AUK-13-243.1. Roemer, G.W., Gompper, M.E., Van Valkenburgh, B., 2009. The ecological role of the mammalian mesocarnivore. Bioscience 59 (2), 165e173. https://doi:10. 1525/bio.2009.59.2.9. Schoener, T.W., 1974. Resource partitioning in ecological communities. Science 185 (4145), 27e39. https://doi:10.1126/science.185.4145.27. Schoener, T.W., 1983. Field experiments on interspecific competition. Am. Nat. 122 (2), 240e285. https://doi:10.1086/284133. Selva, N., Je˛drzejewska, B., Je˛drzejewski, W., Wajrak, A., 2005. Factors affecting carcass use by a guild of in European temperate woodland. Can. J. Zool. 83 (12), 1590e1601. https://doi:10.1139/z05-158. Sergio, F., Marchesi, L., Pedrini, P., 2003. Spatial refugia and the coexistence of a diurnal raptor with its intraguild owl predator. J. Anim. Ecol. 72 (2), 232e245. https://doi:10.1046/j.1365-2656.2003.00693.x. Smith, A.T., Xie, Y., 2010. A Guide to the Mammals of China. Princeton University Press. St-Pierre, C., Ouellet, J.P., Crete,^ M., 2006. Do competitive intraguild interactions affect space and habitat use by small carnivores in a forested landscape? Ecography 29 (4), 487e496. https://doi:10.1111/j.0906-7590.2006.04395.x. Sunarto, S., Kelly, M.J., Parakkasi, K., Hutajulu, M.B., 2015. Cat coexistence in central Sumatra: ecological characteristics, spatial and temporal overlap, and implications for management, 296, pp. 104e115, 2. https://doi:10.1111/jzo.12218. Team, R.C., 2014. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Torretta, E., Serafini, M., Puopolo, F., Schenone, L., 2015. Spatial and temporal adjustments allowing the coexistence among carnivores in Liguria (N-W Italy). Acta Ethol. 19 (2), 123e132. https://doi:10.1007/s10211-015-0231-y. Wang, Y., Fisher, D.O., 2012. Dingoes affect activity of feral cats, but do not exclude them from the habitat of an endangered macropod. Wildl. Res. 39 (7), 611e620. https://doi:10.1071/wr11210. Wikenros, C., Ståhlberg, S., Sand, H., 2014. Feeding under high risk of intraguild predation: vigilance patterns of two medium-sized generalist predators. J. Mammal. 95 (4), 862e870. https://doi:10.1644/13-mamm-a-125. Wisz, M.S., Pottier, J., Kissling, W.D., Pellissier, L., Lenoir, J., Damgaard, C.F., Dormann, C.F., Forchhammer, M.C., Grytnes, J.A., Guisan, A., Heikkinen, R.K., Hoye, T.T., Kuhn, I., Luoto, M., Maiorano, L., Nilsson, M.C., Normand, S., Ockinger, E., Schmidt, N.M., Termansen, M., Timmermann, A., Wardle, D.A., Aastrup, P., Svenning, J.C., 2013. The role of biotic interactions in shaping distributions and realised assemblages of species: implications for species distribution modelling. Biol. Rev. Camb. Philos. Soc. 88 (1), 15e30. https://doi:10.1111/j.1469-185X.2012.00235.x. Xie, B., Han, S.Y., Wang, Y.Z., Zhao, G.J., Gao, Z.Q., Wu, C.H., Liu, Z.Z., Bai, J.B., Liu, M., Gao, J.L., Feng, L.M., Yang, H.T., 2018. Camera trap survey of mammals and in ziwuling national nature Reserve and qiaoshan provincial nature Reserve, Shaanxi (in Chinese with English abstract). Biodivers. Sci. 26 (3), 283e285. https://doi:10.17520/biods.2017241. Yang, H.T., Dou, H.L., Baniya, R.K., Han, S.Y., Guan, Y., Xie, B., Zhao, G.J., Wang, T.M., Mou, P., Feng, L.M., Ge, J.P., 2018a. Seasonal food habits and prey selection of Amur tigers and Amur leopards in Northeast China. Sci. Rep. 8 (1), 6930. https://doi:10.1038/s41598-018-25275-1. Yang, H.T., Han, S.Y., Xie, B., Mou, P., Kou, X., Wang, T.M., Ge, J.P., Feng, L.M., 2018b. Do prey availability, human disturbance and habitat structure drive the daily activity patterns of Amur tigers (Panthera tigris altaica)? J. Zool. 307 (2), 131e140. https://doi:10.1111/jzo.12622. Yang, H.T., Zhao, X.D., Han, B.Y., Wang, T.M., Mou, P., Ge, J.P., Feng, L.M., 2018c. Spatiotemporal patterns of Amur leopards in northeast China: influence of tigers, prey, and humans. Mamm. Biol. 92, 120e128. https://doi:10.1016/j.mambio.2018.03.009. Zhang, J.L., Ding, Q., Huang, J.H., 2013. Spaa: Species Association Analysis. R Package Version 0.2.1. Zhang, L.J., Wang, A.M., Yuan, L., Bao, W.D., Yang, Y.X., Baterr, 2011. Preliminary comparison of diet composition of four small sized carnivores at Saihanwula Nature Reserve, Inner (in Chinese with English abstract). Acta Theriol. Sin. 31 (1), 55e61. https://doi:10.16829/j.slxb.2011.01.009. Zhang, X., 2014. China Forestry-National Nature Reserve. China forestry press. Zhou, Y., Newman, C., Palomares, F., Zhang, S., Xie, Z., Macdonald, D.W., 2014. Spatial organization and activity patterns of the masked palm civet (Paguma larvata) in central-south China. J. Mammal. 95 (3), 534e542. https://doi:10.1644/13-mamm-a-185. Zielinski, W.J., 2000. Weasels and Martens d Carnivores in Northern Latitudes. Springer, Berlin, Heidelberg. Zielinski, W.J., Spencer, W.D., Barrett, R.H., 1983. Relationship between food habits and activity patterns of pine martens. J. Mammal. 64 (3), 387e396. https://doi:10.2307/1380351.