Global Ecology 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 mesocarnivores with a single apex carnivore 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 Tiger and Leopard Biodiversity National Observation and Research Station, Beijing Normal University, Beijing, 100875, China b National Forestry and Grassland 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 Amur Leopard 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 species 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 cat (Prionailurus bengalensis), red fox (Vulpes vulpes), Asian badger (Meles leucurus), Siberian weasel (Mustela sibirica), masked palm Keywords: civet (Paguma larvata) and yellow-throated marten (Martes flavigula), as well as a single Camera trap apex predator (Northern Chinese leopard, Panthera pardus japonensis). We used a camera Sympatric species Mesocarnivore 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. Leopards were most active in winter. Siberian weasels and yellow-throated martens were mainly diurnal, tended to spatially avoid each other, and were temporally segregated from the other mesocarnivores. Leopard cats, Asian badgers, red foxes and masked palm civets 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 animals 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 mammals in northern China and will facilitate future studies on the mechanisms determining the coexistence of animal 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 Fisher, 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 taxonomy important to understand the predisposition of carnivores 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, predation 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 territory 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 mammal 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 competition among these mesocarnivores was high; in particular, we expected high segregation between taxonomically related species (such as the Siberian weasel 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