To the best of our knowledge, this is the first study of the temporal activity pattern of multiple carnivores other than felids in several study sites in Borneo. We find that six species (three civets, one skunk, one felid, one linsang) are nocturnal, two species (one felid, one mustelid) and mongoose spp. are diurnal, and one species (bear) is cathemeral. We successfully obtain substantial sample sizes of the three civet species (banded civets, common palm civets, Malay civets) and sun bears, and we confirm that their activity patterns do not differ among the three sites. Therefore, this study would be a thorough reference for the primary activity patterns of these four species. The results of the activity patterns for the other five species (leopard cats, marbled cats, Sunda stink badgers, yellow-throated martens, and banded linsangs) should be interpreted with caution because we could not distinguish individuals and pooled data from the three study sites, which may have introduced some pseudo-replications18. However, given the limited amount of data available on some of these species in general, our data would still contribute to understanding their activity patterns.
Temporal niche partitioning among some species with morphological and/or ecological similarities is observed in this study. First, we find a clear separation of activity patterns between two felid species; leopard cats are strongly nocturnal, while similar-sized marbled cats present diurnal behavior (Table 3, Fig. 3). These results corroborate the previous study in Sabah8. Second, yellow-throated martens and common palm civets on Borneo also have several similarities such as body sizes, diets, and semi-arboreal habits19, suggesting that they could be potential competitors, although they belong to different families. However, yellow-throated martens are diurnal and common palm civets are nocturnal, therefore, their temporal activity overlap was low (Table 3), indicating their temporal niche segregation, mitigating negative interactions by avoidance of direct encounters. Contrary to the felids and martens, three civet species of the same family exhibit the most extensive activity overlaps among the observed species (Table 3, Fig. 3). The three civet species have similar diet and body size19, and they occur in quite similar spatial and temporal spaces. Although there is no evidence of temporal niche partitioning among the three civet species, there appear to be minor differences in spatial activity patterns among them. Banded civets and common palm civets prefer interior forests, open-canopy habitats such as roadside, respectively, while Malay civets are found in both forest types20. These subtle ecological differences would be significant to maintain their coexistence in complex forest structures in Borneo.
Based on our results, yellow-throated martens and mongoose spp. are strictly diurnal, but the other species have nocturnal activity patterns in varying degrees (Table 2, Fig. 2). All three civets, leopard cats, Sunda stink badgers, and banded linsangs are nocturnal, and most of them exhibit high overlaps (0.7 < ∆, Table 3) in their temporal activity patterns, except for banded linsangs. Overall, activity overlaps between banded linsangs and the other nocturnal carnivores are not high (∆1 < 0.7, Table 3) compared to the others. During the nighttime, differences in activity peaks may relate to the low activity overlaps of banded linsangs. Banded linsangs show clear bimodal peaks during the night and twilight periods (Fig. 2), and they are most active in the last half of the night (Table 2). Whereas, the other five nocturnal species are active throughout the night, especially in the first half of the night (Table 2). Thus, even among species with the same temporal activity patterns, some species differentiate activity peaks. However, temporal niche overlap among the other five nocturnal species is still quite extensive. A possible reason for their coexistence is dietary niche partitioning. In Borneo, only felids and linsangs are supposed to be hyper-carnivores19,21, while the other species are highly omnivorous: feeding on mammals, birds, invertebrates, plant matters19. Although information regarding the diets of most Bornean carnivore species is still scarce, such broad dietary breadth may compensate for the high temporal niche overlaps among the nocturnal carnivores.
In this study, we find that six out of the 10 studied species, including mongoose spp., are nocturnal, and temporal activity overlaps are high among these species. Some species possessing either one or both morphological and ecological similarities exhibit clear temporal niche segregation, but some species, that is, civets, do not. Most of the studied carnivore species are small to medium (< 10 kg19) except for the sun bears. In a guild of five African sympatric small-medium carnivores (< 10 kg), they are separated into two temporal groups: three nocturnal and two diurnal species22. In Madagascar carnivores, comprising a single-family Eupleridae have three nocturnal, one diurnal, and one cathemeral species23. In a Neotropical small-medium felid guild, there are two are nocturnal, one diurnal, and one cathemeral species6. Thus, it is suggested that the number of nocturnal small-medium carnivore species is extensive across the continent most likely, due to phylogenetic constraints24, but that of the Bornean community overwhelms the others. We find no cathemeral small-medium species from the studied species. Due to data deficiency, it remains unclear whether the occurrence of these sympatric carnivore species during the same periods generates negative effects such as intra-guild killing and interference competitions. Given that temporal niche segregation is one of the most effective mechanisms that diminishes competition4, the studied carnivore species may not compete intensively, or have relatively small ecological differences that have not yet been investigated.
Currently, camera-trapping is one of the most basic but effective tools for community ecology and conservation planning in mammals3. The temporal activity pattern is one of the main data obtained from camera trapping. Indeed, our data on temporal activity patterns of common palm civets and Malay civets successfully show results similar to radio-tracking in DVCA and TWR15,25, where both are predominantly nocturnal, but also show crepuscular behavior. For sun bears, the results are contradictory in an intensive study using both individual radio-tracking and camera trapping conducted in the DVFC for two years26: diurnal by radio-tracking, crepuscular and nocturnal by camera-trapping. However, our relatively robust dataset showed that sun bears are cathemeral. Considering that their activity patterns vary at the individual level26, the overall activity patterns of several individuals in a certain area may become cathemeral as indicated by this study. The lack of long-term empirical data in any taxa would hinder our understanding of its temporal activity pattern, which could consequently divert conservationists from effective protection measures. Therefore, we propose that at least three years of long-term study is necessary to understand an animals’ temporal activity patterns by camera trapping.
All the three study sites are protected areas, but evidence of poaching have been reported, including sun bears in some of these areas27. Our results do not show statistical differences in temporal activity patterns of sun bears and the three civet species among the study sites, but this may change depending on the threat status given that some animals change temporal activity patterns because of hunting disturbances28. Non-lethal tourism activities may also affect animal activity. Tourism activity was conducted at all study sites during the study period. The potential benefits gained from ecotourism may frequently counteract the risks of exposure to changes in animal activity patterns29. In LKWS, community-based ecotourism is common and can bring significant benefits such as alternative income that incentivizes local communities and policy makers to protect the species in areas of interest. Spotlighting activities along the Menanggul River were often conducted by several motor boats during early morning, late afternoon, and night in LKWS. However, no nocturnal tourism activities were conducted around the camera stations in DVCA and TWR. Common palm civets show at least two clear peaks of temporal activity levels in the latter two sites, whereas those in LKWS are unclear and delayed (Fig. 1). Given that common palm civets prefer open-canopy areas including riverine forests30, they might be directly affected by tourism activity, especially during nighttime in LKWS. Thus, there may be a need for evaluating the effect of tourism activity on animal behavior in future studies, even though it is non-lethal ecotourism.
Lastly, many studies are using camera-trapping data, including remote areas with relatively poor accessibility. Thus, it is the time to accumulate the information on rare species to determine their basic ecology, including temporal activity patterns and habitat selection, and to reassess the propriety of current conservation management strategies.