The competitive exclusion principle states that two ecologically similar species cannot coexist1. Thus, multiple sympatric species can partition their niche according to four major factors: food resources, natural enemies, space, and time2. Elucidating the mechanisms of species coexistence based on their niche partitioning is important for understanding community diversity and for implementing effective community conservation and management strategies3–6.
It is widely known that interspecific competition can often occur among sympatric carnivores7–10. The extent of their interspecific competition is influenced by taxonomic similarity, dietary overlap, and intermediate body-size differences11. For example, larger coyotes (Canis latrans) can exclude smaller swift foxes (Vulpes velox) from their home ranges and territories9. Similarly, Tsunoda et al.12 suggested that interspecific competition can increase between larger golden jackals (Canis aureus) and smaller red foxes (Vulpes vulpes) because of their dietary overlaps. To avoid such competition, carnivores coexist sympatrically by shifting their activity time and spaces (e.g.,13–15). In particular, temporal niche partitioning is one of the most important strategies to ensure their coexistence5,16,17.
Currently, temporal niche partitioning among sympatric carnivores is often assessed using camera-trap data5, and several studies have demonstrated that temporal niche partitioning is key for their successful sympatry (e.g.,18–21). For example, European badgers (Meles meles) and stone martens (Martes foina) shifted their diel activity patterns to avoid antagonistic encounters with larger golden jackals in Bulgaria20. Stone martens also tended to be active at different times than larger red foxes and European wildcats (Felis sylvestris)21. Typically, temporal niche partitioning among carnivores is assessed using time data (i.e., 0:00–23:59) (e.g.,18–23). Among them, the coefficient of temporal overlap of activity patterns based on the kernel density estimation24,25 has been widely used (e.g.,5,26−31). Frey et al.5 argued that the kernel density estimation has greatly improved the level of knowledge available from camera-trap data.
Furthermore, recent studies have assessed the influence of effective sample size for the accuracy and the statistical power when estimating the temporal overlap32,33. However, measuring the temporal overlap may sometimes be insufficient to assess species interactions correctly, as this method evaluates the overlaps/differences in diel activity patterns between a focal species pair throughout the day, from 0:00 to 23:59, from a dataset pooled during a sampled period. For example, if two species are both nocturnal, a subordinate (i.e., smaller) species may coexist with a dominant species by avoiding direct encounters with the larger competitor at fine time scale (e.g., dozens of minutes or several hours), even if the coefficient of temporal overlap shows a high value34. Nowadays, the spatio-temporal niche partitioning has been measured to assess behavioral avoidance by focusing on the time-to-encounter between individuals of different species (e.g.,34–40). Indeed, Karanth et al.34 found a large overlap in diel activity patterns between tigers (Panthera tigris) and leopards (Panthera pardus), while demonstrating their behavioral avoidance by using the time-to-encounter analysis. Similarly, Paúl et al.39 also found a large overlap in diel activity patterns between side-striped jackals (Canis adustus) and African wolves (Canis lupaster), while indicating the occurrence of some behavioral avoidance using the time-to-encounter analysis, with side-striped jackals taking longer than expected to be detected after the occurrence of African wolves. These results suggest that the evaluation of behavioral avoidance at fine time scales using the time-to-encounter analysis may provide an understanding of the mechanisms of species coexistence that cannot be detected by only estimating the temporal overlap. When different analytical approaches detect different niche partitioning results, the mechanisms of species coexistence may be misinterpreted. To avoid this, it is important to evaluate temporal niche partitioning using multiple analytical approaches. Although a previous study evaluated the detection power of the temporal overlap and the time-to-encounter analysis separately33, comparative evaluations of multiple analytical methods have not been conducted yet.
To address this methodological issue, we compared multiple analytical methods to accurately evaluate the temporal partitioning among three sympatric mesocarnivores. We used the temporal overlap, temporal co-occurrence analysis, and the time-to-encounter analysis (Fig. 1). Our focal species were red foxes, raccoon dogs (Nyctereutes procyonoides), and Japanese martens (Martes melampus). Red foxes and genus Martes individuals are widespread in the Northern Hemisphere41,42, and raccoon dogs are widely distributed in East Asia and Russian Far East and have also been introduced in Europe43. In addition, the red foxes and raccoon dogs belong to the same family (i.e., Canidae), and differ in body size from the Japanese martens42, indicating their potential competitive interactions, according to Donadio & Buskirk11. Therefore, our focal species are ideal to assess the role of temporal partitioning in mesocarnivores sympatry. In this study, we proposed the temporal co-occurrence analysis (Fig. 1b), adapted from the spatial co-occurrence analysis44,45, which is a method used to assess the spatial co-occurrence of multiple species by using presence-absence data (e.g.,46–49). Furthermore, we also performed the time-to-encounter analysis (Fig. 1c) based on the concept of multi-response permutation procedures, according to Karanth et al.34. We performed this analysis in two ways: using multiple time scales which ranged from several minutes to several days or weeks, according to the previous study34, and only using nighttime unit scale to address diel activities of the focal species (for more details see ‘Methods’).