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Temporal partitioning by felids, dholes and their potential prey in northern Laos

Temporal partitioning by felids, dholes and their potential prey in northern Laos Temporal partitioning can allow sympatric carnivores to coexist, especially if overlap of other resources is high. Using camera trap data from 2013 to 2017, we investigated the temporal partitioning of a community of wild felids and a canid in Nam Et–Phou Louey National Protected Area, Laos, to determine the extent to which temporal avoidance might be facilitating coexistence of similarly sized carnivores. We also investigated temporal overlap of these carnivore species and their presumed main prey, to determine if their activity is likely most influenced by their prey or potential competitors. The dhole (Cuon alpinus) and clouded leopard (Neofelis nebulosa), the two largest carnivores, had low temporal overlap, and activity appeared to be synchronized with the main prey for dhole, but not clouded leopard. Thus, it was possible that clouded leopard used temporal partitioning to coexist with dhole. The temporal overlap of Asian golden cat (Catopuma temminckii) was high with clouded leopard and moderate with dhole, and overall appeared to be influenced most by its presumed prey species, rather than by its potential competitors. The two small felids had the least temporal overlap between any species, as the marbled cat (Pardofelis marmorata) was primarily diurnal whereas the leopard cat (Prionailurus bengalensis) was primarily nocturnal. Given that the two small felids reportedly have similar diets consisting of small rodents and birds, their temporal partitioning is likely to help facilitate their coexistence. For carnivore species in northern Laos that are most similar in body size and diet, temporal partitioning is likely to be an important mechanism of coexistence. Otherwise, temporal patterns appear to be synchronized with their main prey. . . . . . . Keywords Activity pattern Asian golden cat Clouded leopard Dhole Lao PDR Leopard cat Marbled cat Introduction which include space, time and food (Case and Gilpin 1974; Schoener 1974). In particular, dietary overlap often drives Species coexistence is one of the most complex topics in ecol- interference competition within carnivore guilds; therefore, ogy (Gordon 2000). In principle, species that are ecologically food niche differences can be key to successful sympatry similar cannot coexist in the same area (Hardin 1960). For (Tsunoda et al. 2017). If dietary partitioning between such species to coexist, theory anticipates some degree of similarly-sized carnivores is low, then partitioning of other niche differentiation whereby interspecific competition is re- resources is necessary to reduce intraguild predation and fa- duced (Schoener 1974). Niche differentiation of ecologically cilitate coexistence (Case and Gilpin 1974;Schoener 1974; similar species may occur in one or more niche dimensions Holt and Polis 1997). Temporal partitioning has been shown to reduce interference competition and facilitate coexistence Communicated by: Krzysztof Schmidt among species (Kronfeld-Schor and Dayan 2003;Hayward and Slotow 2009). Additionally, small felids and small canids Electronic supplementary material The online version of this article (https://doi.org/10.1007/s13364-020-00524-9) contains supplementary have been shown to use temporal partitioning to coexist with material, which is available to authorized users. larger members of their guilds (Kamler et al. 2012b, 2013; Lynam et al. 2013; McCarthy et al. 2015b; Hearn et al. * Akchousanh Rasphone 2018; Santos et al. 2019), especially those with high dietary akchousanhr@yahoo.com overlap (Lucherini et al. 2009; Nagy-Reis et al. 2019). However, activity patterns are determined by numerous fac- Wildlife Conservation Research Unit, Department of Zoology, tors, and often activity patterns of carnivores are driven by the Recanati-Kaplan Centre, University of Oxford, Tubney House, activity of their main prey (Lucherini et al. 2009; Nagy-Reis Abingdon Road, Tubney, Abingdon OX13 5QL, UK 680 Mamm Res (2020) 65:679–689 et al. 2019). Understanding the factors that drive the activity felids, such as leopards (Panthera pardus) and pumas (Puma patterns of carnivorous species can be important for under- concolor), during encounters due to their numerical advantage standing their ecological niche, especially in regard to their (Venkataraman 1995; Ruth et al. 2019). Therefore, dholes relationships with other carnivores and their main prey. likely behaviourally dominate clouded leopards as well. Nam Et–Phou Louey National Protected Area (hereafter Based on body size, the next most dominant carnivore should NEPL) in northern Laos is known for its diverse carnivore be the Asian golden cat, followed by leopard cats and marbled community (Johnson et al. 2009), yet little is known regarding cats (Table 1). Although the activity patterns of these species the ecology of those carnivore species and their ecological have been determined in previous studies (Table 1), activity interactions. Large carnivores, tiger Panthera tigris and leop- patterns of a species can vary across sites due to differences in ard P. pardus, were part of the NEPL community, but they numbers of competitors, prey and humans (Valeix et al. 2007; recently became extirpated (Rasphone et al. 2019). Currently, Lucherini et al. 2009;Kamleretal. 2013;Ngoprasert etal. the canid and felid communities of the NEPL consist of large 2017). Regardless, it is not known if the activities of these (> 15 kg; dhole Cuon alpinus, clouded leopard Neofelis carnivores are driven by competition within their guild or by nebulosa), medium (5–15 kg; Asian golden cat Catopuma their main prey. Better knowledge of the ecological relation- temminckii), and small-sized (< 5 kg; marbled cat Pardofelis ships of this carnivore community in NEPL could assist con- marmorata, leopard cat Prionailurus bengalensis) species servation efforts for them, especially given that the IUCN has (Table 1). To date, the understanding of the coexistence of classified most of these carnivores as threatened or near threat- this diverse carnivore community is poorly known ened (Table 1). For example, increased human activities in (Grassman et al. 2005a;Ngoprasert etal. 2012; Lynam et al. parks, including tourism, can cause shifts in carnivore activity 2013; McCarthy et al. 2015b; Hearn et al. 2018; Can et al. patterns, which can reduce the health, reproduction and sur- 2020). Clearly, more data would better elucidate their mecha- vival of carnivores (Ngoprasert et al. 2017). nisms of coexistence, especially after the extirpation of the We used camera-trap surveys to determine the activity pat- largest carnivores, which might have changed the interactions terns of felid species and dholes in NEPL. Our primary objec- between the remaining carnivores and their prey (Estes et al. tives were to determine the temporal overlap between the carni- 2011;Ripple etal. 2014). vores, as well as between the carnivores and their potential prey. Because competition among carnivores often is driven by Based on the body size of these species and their reported diets diet and body size (Donadio and Buskirk 2006), we assumed and activity patterns (Table 1), we made the following predic- that the two most dominant carnivores remaining in NEPL tions: (1) temporal overlap between dholes and clouded leopards were the dhole and the clouded leopard, which are similar in will be low, owing to their similarity in diets; (2) temporal over- body size and consume the largest prey (Table 1). Large ca- lap between dholes and Asian golden cats will be high, owing to nids, including dholes and wolves (Canis lupus), live in large their different dietary niches; (3) temporal overlap between packs (Kamler et al. 2015) and behaviourally dominate large clouded leopards and Asian golden cats will be low, owing to Table 1 Summary of the reported ecology of the felid and canid community inhabiting the Nam Et–Phou Louey National Protected Area, Laos. The current IUCN status is given after each species (EN = endangered, VU = vulnerable, NT = near threatened, LC = least concern) 1 1 Species Body size (kg) Lifestyle Activity Primary prey species 2 3 4,5 Dhole (EN) 15–21 Terrestrial Diurnal Small, medium and large ungulate 6 6 6 Clouded leopard (VU) 15–23 Semi-arboreal Nocturnal, crepuscular Small ungulate, primate, porcupine, sciurid, bird 7 7 8 Asian golden cat (NT) 12–15 Terrestrial Cathemeral, crepuscular Small ungulate, murid, sciurid, bird 9 9 8 Leopard cat (LC) 3–5 Terrestrial Nocturnal, crepuscular Murid, sciurid, bird 10 10 10 Marbled cat (NT) 2–4 Semi-arboreal Diurnal, crepuscular Murid, sciurid, bird Francis (2019) Kamler et al. (2015) Kamler et al. (2012a) Kamler et al. (2020a) Thinley et al. (2011) Grassman et al. (2016) McCarthy et al. (2015a) Kamler et al. (2020b) Ross et al. (2015) Ross et al. (2016) Mamm Res (2020) 65:679–689 681 similarities in their body size and diet; (4) temporal overlap be- rainfall ranges from 1400 to 1800 mm (Johnson 2012). The tween Asian golden cats and marbled cats will be higher than the NEPL is divided into two protected zones; a totally protected overlap between Asian golden cats and leopard cats, based on zone where human activity (except for protected area manage- results from previous studies; and (5) temporal overlap between ment) is prohibited and a peripheral managed use zone where leopard cats and marbled cats will be low, owing to their simi- specified livelihood activities are permitted following park larity in diets. regulations (Fig. 1). Materials and methods Camera trapping Study area Systematic camera trap surveys, with clouded leopards as the focal species, were carried out from 2013 to 2017 within the The NEPL is located in the northern highlands of Laos (be- NEPL core zone, in four ~ 200 km blocks (Fig. 1), for a total tween latitude 19° 50′–20° 50′ N and longitude 103° 00′–103° of 32,027 trap days (Supplementary Data S1). These four 53′ E), bordering Vietnam along its northern boundary sampling blocks are known as Nam Poung–Na Vaen (Fig. 1). It covers an area of 5969 km with rugged topography (NPNV), Pha Daeng (PD), Phoupha–Siphou (PS) and across seven districts and three provinces (Houaphan, Luang Nam Neun (NN; Fig. 1). For each block, camera traps Prabang and Xiengkhuang) and elevation ranging from 400 to were set in pairs at 80 locations, except for block NN 2257 m, of which > 60% is above 1000 m and 91% with where cameras were set at only 60 locations, with 1– slopes > 12% (Johnson 2012). Vegetation is dominated by 1.5 km spacing between stations based on the home- dry evergreen and semi-evergreen forests. However, around range size of clouded leopards (Hearn et al. 2019). one third of the park is degraded forest with a canopy cover of We used a mixture of three infrared camera trap less than 20%. The climate in Laos is tropical monsoonal with models: CuddeBack Ambush IR - Model 1187, a rainy season lasting from May to October, followed by a Reconyx Hyperfire HC500, and MAGINON – WK 3 distinct dry season for the remainder of the year. Annual HD (Supra Foto-Elektronik-Vertriebs-GmbH). Fig. 1 The Nam Et–Phou Louey National Protected Area (NEPL), Laos, showing locations of the four survey blocks from 2013 to 2017 (NPNV = Nam Poung–Na Vaen; PD = Pha Daeng; PS = Phoupha–Siphou; NN = Nam Neun). The inset map shows the location of the NEPL in Laos 682 Mamm Res (2020) 65:679–689 Traps sites were from 629 to 2185 m altitude time of detection t is the proportion of hours and minutes in (Supplementary Data S1) where 16% of the sites were below 1 day. A measure of overlap under this approach was calcu- 1000 m, 16% were between 1000 and 1500 m, and 68% were lated by fitting non-parametric kernel density functions to the above 1500 m. About 63% of the sites were in closed forest, species’ diel activity data (Ridout and Linkie 2009;Linkieand which comprised evergreen and high density semi-evergreen Ridout 2011) and was performed using the package over- forests. The camera traps were placed mostly along ridge lines lap_0.3.0 in R (Meredith and Ridout 2014). The coefficient and animal trails, and at intersections where trails meet of overlap (Δ) is calculated as the proportion of overlap be- streams. Each camera was mounted onto a tree trunk with its tween the two species’ diel activity curves (Ridout and Linkie motion beam set at ca. 35 cm height from the ground at the 2009). We calculated the coefficients of overlap as a spectrum centre of the trail (approx. shoulder height of an adult clouded of proportional values, with 1 indicating complete overlap and leopard). Each survey period lasted for a minimum of 50 days 0 indicatingnooverlap.Schmid and Schmidt(2006)proposed (Supplementary Data S1). Each camera-trap photo of an ani- five estimators of Δ, and we used the non-parametric estima- mal was identified and organised using the CamtrapR tor Δ because of its superiority for sample sizes that are (Niedballa et al. 2016). Notionally independent events were greater than 50 (Ridout and Linkie 2009; Meredith and considered if they were > 30 min apart (O’Brien et al. 2003). Ridout 2014). Following Lynam et al. (2013), values of Δ ≥ 0.70 and Δ < 0.35 were defined as a high overlap and a low Circadian activity and overlap analysis overlap in diel activity, respectively. In addition to modelling activity overlap for the selected Quantitatively investigating activity patterns is challenging be- species pairs, an activity overlap of each selected carnivore cause time is a wrapped distribution with an arbitrary zero point; species with each of its presumed principle prey species was thus, traditional statistical methods cannot be applied (Frey et al. also modelled. Five ungulate species have been identified as 2017). To solve this, activity patterns can be examined using prey species for dhole in NEPL (Kamler et al. 2020a): small circular statistics which derive descriptive statistics of temporal dark muntjac (M. rooseveltorum complex), northern red munt- data using trigonometric functions (Zar 1996;Freyet al. 2017). jac (Muntiacus vaginalis), sambar (Cervus unicolor), main- Therefore, we used circular statistics to describe activity patterns land serow (Capricornis milneedwardsii) and Eurasian wild of carnivores and potential prey in NEPL. Percentage of detec- pig (Sus scrofa). For the clouded leopard, a wide range of tions recorded for each hour over a 24-h period was used in the species have been considered as its potential prey (Table 1), modelling following Ross et al. (2013). Diel activity patterns including, in a Lao context, small- and medium-sized ungu- models were fitted as a function of continuous trigonometric lates, four species of macaque, two porcupine species, squir- predictors describing one (cosΘ, sinΘ)and two(cos2Θ, sin2Θ) rels, ground-dwelling birds and other small birds (Ross et al. complete cycles in a 24-h period with Θ =πt/24,where t is time 2013;Grassman et al. 2016). For the Asian golden cat, poten- in hours (Ross et al. 2013). For sinΘ, a species is considered tial prey in NEPL included muntjacs, porcupines, squirrels, crepuscular with a single activity peak either at dawn (if positive ground-dwelling birds, other small birds and rats/mice coefficient) or dusk (if negative coefficient). For cosΘ, a species (Kamler et al. 2020b). The potential prey of the leopard cat is considered nocturnal with a positive coefficient or diurnal with and marbled cat are squirrels, birds and rats/mice (Ross et al. a negative coefficient. For the bimodal sin2Θ, positive values 2016; Kamler et al. 2020b). Although the camera-trap survey indicate a species’ peak at pre-dawn and pre-dusk whereas neg- was designed for the clouded leopard, we assumed that it ative values indicate activity peaks at post-dawn and post-dusk. would accurately record the activity patterns of sympatric car- For the bimodal cos2Θ, a species is considered crepuscular and nivores and their potential prey. Although some prey species active at both dawn and dusk (if negative coefficient) or at both (e.g. primates) were mostly arboreal, we assumed their midday and midnight (if positive coefficient). With this ap- ground-level activity detected by the cameras were consistent proach, activity overlap between paired species was also tested with their overall activity patterns. through the construction of models representing the full 24- hcycles(SinΘ, CosΘ, Sin2Θ, Cos2Θ). An ANOVA test was then conducted for each model to test for significant difference Results between the activity of each pair of species, and the model with the highest adjusted R was selected. This analysis was carried Of the five carnivore species, the leopard cat had the highest out in the R program (R Core Team 2017). number of notionally independent photographs followed by In addition, the kernel density method was implemented to the Asian golden cat, whereas the marbled cat had the lowest examine the difference in activity pattern between each pair of number of independent events (Table 2). Out of the three species (Ridout and Linkie 2009). In the kernel density ap- survey blocks where camera trapping was repeated three proach, observed capture times are regarded as random sam- times, PD yielded the most notionally independent records ples from continuous underlying distributions, and a species’ for all felids but the fewest for dhole (Table 2). Among the Mamm Res (2020) 65:679–689 683 Table 2 The number of Survey block notionally independent records of felids and dhole, and presumed Species NN NPNV PD PS prey species from each survey block (NPNV = Nam Poung–Na Asian golden cat (Catopuma temminckii) 8 53 73 38 Vaen; PD = Pha Daeng; PS = Phoupha – Siphou; NN = Nam Clouded leopard (Neofelis nebulosa) 5 34 56 52 Neun) in Nam Et–Phou Louey Dhole (Cuon alpinus) 3 67 30 57 National Protected Area, Laos, Leopard cat (Prionailurus bengalensis) 3 61 79 60 2013–2017 Marbled cat (Pardofelis marmorata) 2 45 47 31 Asiatic brush-tailed porcupine (Atherurus macrourus) 3 93 119 42 Assamese macaque (Macaca assamensis) 5 18 11 13 Small dark muntjac(s) (M. rooseveltorum complex.) 2 206 210 36 East Asian porcupine (Hystrix brachyura)17 136 167 70 Eurasian wild pig (Sus scrofa)21 120 147 62 Grey peacock pheasant (Polyplectron bicalcaratum) 8 40 187 22 Indochinese serow (Capricornis milneedwardsii) 7 128 107 32 Northern pig-tailed macaque (Macaca leonina) – 31 10 Red junglefowl (Gallus gallus) 7 18 105 17 Northern red muntjac (Muntiacus vaginalis) 83 489 629 292 Red-cheeked squirrel (Dremomys rufigenis) – 526 28 Rhesus macaque (Macaca mulatta)5 6 13 15 Sambar (Cervus unicolor) 4 98 29 45 Silver pheasant (Lophura nycthemera)12 81 74 59 Stump-tailed macaque (Macaca arctoides)81 385 457 37 Birds spp. 3 66 73 49 Rat/mouse spp. (Muridae) 8 78 134 191 Squirrels spp. (Sciuridae) 2 26 108 46 presumed prey species, the northern red muntjac had the most Diel activity overlap between carnivores records in all blocks, followed by the stump-tailed macaque Macaca arctoides. Three out of four species of macaques The results from the wave analysis showed that there detected during the study had fewer than 50 notionally inde- was a difference in activity within each pair of pendent records, which were relatively low compared with species (best models of most pairs were P < 0.05; those of all other prey species (Table 2), presumably because Table 4). The activity overlap between dhole and of the greater arboreality of the macaque species. clouded leopard (0.51 Δ ;Fig. 2a) was slightly lower than that between dhole and Asian golden cat (0.66 Δ ;Fig. 2b). Although our wave analysis suggested sig- Circadian activity nificant difference in Cos2Θ (P = 0.038) between clouded leopard and Asian golden cat, the SinΘ was There was strong evidence that activity patterns differed not significant (P =0.753; Table 4). This indicated a high among the five carnivore species (CosΘ*Species: F = level of overlap between the clouded leopard and the 14.78, P <0.001; SinΘ*Species: F =3.22, P =0.01). Asian golden cat, a result consistent with the kernel den- The dhole showed a strongly diurnal and crepuscular (both sity analysis which also indicated a strong overlap in dawn and dusk) pattern of activity, with the highest peak of activity between them (0.80 Δ ;Fig. 2c). We found that activity at dusk (Table 3;Fig. 2a). The clouded leopard was activity overlap between the Asian golden cat and the strongly crepuscular, but most active at dawn (Table 3;Fig. marbled cat was much higher than the overlap between 2a). The Asian golden cat was active both by day and by night the Asian golden cat and the leopard cat (0.74 Δ and (Fig. 2b) but with a peak of activity at dawn (Table 3). The 0.55 Δ ;Fig. 2e, d). Notably, the leopard cat and the leopard cat was clearly nocturnal while the marbled cat was marbled cat had the lowest overlap in activity between strongly diurnal with some activity at dawn and dusk (Table 3; any two carnivore species (0.31 Δ ;Fig. 2f). Fig. 2f). 684 Mamm Res (2020) 65:679–689 Table 3 Estimates of coefficients (± SE) of diel activity models and best marbled cat) in Nam Et–Phou Louey National Protected Area, Laos, models with adjusted R values for five carnivore species (D = dhole; 2013–2017. Significant values are designated with *P <0.05, CL = clouded leopard; AC = Asian golden cat; LC = leopard cat; MC = **P < 0.01, and ***P <0.001 1 2 3 4 2 SinΘ CosΘ Sin2Θ Cos2Θ Best model Adjusted R D 0.009 ± 0.005 − 0.023 ± 0.005*** 0.006 ± 0.005 − 0.017 ± 0.005** CosΘ + Cos2Θ 0.533 CL 0.035 ± 0.005*** 0.006 ± 0.005 − 0.004 ± 0.005 − 0.021 ± 0.005*** SinΘ + Cos2Θ 0.737 AC 0.025 ± 0.006*** − 0.002 ± 0.006 − 0.003 ± 0.006 − 0.002 ± 0.006 SinΘ 0.413 LC 0.008 ± 0.006 0.031 ± 0.006*** 0.002 ± 0.006 − 0.002 ± 0.006 CosΘ 0.495 MC 0.019 ± 0.008* − 0.030 ± 0.008*** − 0.009 ± 0.008 − 0.020 ± 0.008* SinΘ + CosΘ + Cos2Θ 0.506 1 2 For sinΘ, a species is considered crepuscular with a single activity peak either at dawn (if positive coefficient) or dusk (if negative coefficient). For cosΘ, a species is considered nocturnal with a positive coefficient or diurnal with a negative coefficient For the bimodal sin2Θ, positive values indicate a species’ peak at pre-dawn and pre-dusk whereas negative values indicate activity peaks at post-dawn and post-dusk For the bimodal cos2Θ, a species is considered crepuscular and active at both dawn and dusk (if negative coefficient) or at both midday and midnight (if positive coefficient) Diel activity overlap between carnivores and their appeared to be synchronized with that of their main prey. prey Thus, our research supports previous studies that showed tem- poral partitioning can reduce interference competition and fa- Dhole activity overlapped most strongly with the dark munt- cilitate coexistence among carnivores, especially those with jac (0.85 Δ ) and the Eurasian wild pig (0.80 Δ ). While both high dietary overlap (Kronfeld-Schor and Dayan 2003; 4 4 prey species were strongly diurnal, there was a peak of activity Hayward and Slotow 2009; Lucherini et al. 2009;Nagy- of the dark muntjac at dusk, closely corresponding to the Reis et al. 2019). For example, the temporal overlap was activity of the dhole (Supplementary Data S2.1a). Overall, low between dholes and clouded leopards, which supported the overlap coefficients between the clouded leopard and their our prediction, indicating temporal partitioning occurred be- candidate prey species were greater than 0.40 Δ tween these species. Dholes were mostly diurnal with a peak (Supplementary Data S2.2). The strongest overlaps were be- of activity at dusk, which is consistent with findings elsewhere tween the clouded leopard and (i) sambar and (ii) Indochinese (Grassman et al. 2005b; Kawanishi and Sunquist 2008; serow (0.79 Δ and 0.75 Δ , respectively). Clouded leopard Kamler et al. 2012a;Bashiret al. 2014). Dhole activity over- 4 4 overlapped most with the prey species that had an activity lapped moderately to strongly with both muntjac species. peak at dawn. Previous research in NEPL and elsewhere in Southeast Asia The Asian golden cat’s activity overlapped strongly with showed that muntjacs were the most preferred prey of dholes that of both types of muntjacs, squirrels and all listed bird regardless of ungulate diversity and densities (Kamler et al. species (with overlap coefficients > 0.70 Δ ; Supplementary 2020a), indicating that the activity of dholes was driven by the Data S2.3); these overlaps were more strongly congruent than activity of their most preferred prey. Clouded leopard activity those revealed for clouded leopard and their candidate prey was crepuscular with a peak at dawn, similar to that observed species. Asian golden cat overlapped most with prey that were in some areas (Azlan and Sharma 2006; Lynam et al. 2013; active by day, and it overlapped little with porcupines (0.45 McCarthy et al. 2015b), but not others (Singh and Macdonald Δ ) and rats/mice (0.42 Δ ). Insofar as rats/mice were strong- 2017; Hearn et al. 2018; Mukherjee et al. 2019; Can et al. 4 4 ly nocturnal, these prey species overlapped strongly with leop- 2020). Although clouded leopard activity synchronised with ard cat (0.84 Δ ; Supplementary Data S2.4f). The marbled cat that of the Indochinese serow and sambar, it is doubtful that overlapped most strongly with candidate prey that were more these two species are preferred prey of clouded leopards, giv- diurnal such as squirrels and birds (with overlap coefficients > en the large body size of these ungulates relative to that of 0.70; Supplementary Data S2.5a - e). clouded leopards. Instead, the preferred prey of clouded Fig. 2 Overlap in temporal activity between (a) dhole and clouded Discussion „ leopard, (b) dhole and Asian golden cat, (c) clouded leopard and Asian golden cat, (d) Asian golden cat and leopard cat, (e) Asian golden cat and Temporal partitioning among carnivores in NEPL was exhib- marbled cat, and (f) leopard cat and marbled cat in Nam Et–Phou Louey ited only between species that were similar in body size, and National Protected Area, Laos (2013–2017), as measured by the kernel density across the 24-h period likely had similar diets. Otherwise, the activity of carnivores Mamm Res (2020) 65:679–689 685 (a) Dhole vs. Clouded leopard (Δ4=0.51; CI=0.39-0.57) (b) Dhole vs. Asian golden cat (Δ4=0.66; CI=0.55-0.74) (c) Clouded leopard vs. Asian golden cat (Δ4=0.80; CI=0.68-0.86) (d) Asian golden cat vs Leopard cat (Δ4=0.55; CI=0.43-0.60) (e) Asian golden cat vs. Marbled cat (Δ4=0.74; CI=0.65-0.81) (f) Leopard cat vs. Marbled cat (Δ4=0.31; CI=0.20-0.33) 686 Mamm Res (2020) 65:679–689 Table 4 Overlap estimates Species pairing Kernel density (Δ ) Wave Adjusted R P(t) between carnivore species 4 calculated from the kernel density Dhole–clouded leopard 0.51 SinΘ 0.525 0.009 (− 2.919) (correlation coefficient Δ ), and significant wave(s) of best models CosΘ 0.046 (− 2.145) for the interactions, from camera- Dhole–Asian golden cat 0.66 SinΘ 0.604 0.010 (− 2.874) trap data collected in Nam Et– CosΘ 0.046 (− 2.144) Phou Louey National Protected Area, Laos, 2013–2017. The P(t) Clouded leopard–Asian golden cat 0.80 SinΘ 0.682 0.753 (− 0.319) represents the P value with the Cos2Θ 0.038 (− 2.233) associated test statistic (t)inpa- Asian golden cat–leopard cat 0.55 SinΘ 0.722 0.044 (− 2.161) rentheses; P < 0.05 indicate that CosΘ < 0.001 (4.992) species differ in the correspond- ing wave Asian golden cat–marbled cat 0.74 SinΘ 0.475 0.278 (− 1.117) CosΘ 0.076 (− 1.883) Leopard cat–marbled cat 0.31 CosΘ 0.366 0.002 (− 3.540) Cos2Θ 0.372 (− 0.915) leopards is most likely smaller prey species such as muntjacs Clouded leopards and Asian golden cats had similar activ- and primates (Table 1), although activity overlap with these ity patterns, which did not support our prediction that they prey species was low. Therefore, we conclude that activity of should exhibit temporal partitioning. Our results were similar clouded leopards was most influenced by avoidance of dholes, to that found in Sumatra, where Sunda clouded leopards rather than prey, likely because the pack-living dholes are (Neofelis diardi) and Asian golden cats had high temporal behaviorally dominant over clouded leopards. overlap (McCarthy et al. 2015b). McCarthy et al. (2015b) The activity pattern of the only meso-carnivore in NEPL, speculated that differences in resource exploitation due to the Asian golden cat, was crepuscular with activity intensified the clouded leopard’s greater arboreality facilitated their co- from dawn until midmorning. Based on the kernel density existence with Asian golden cats. Additionally, the signifi- activity plot, the species seemed to be active both day and cantly greater canine length in clouded leopards suggests that night, which is consistent with previous studies (Kawanishi they have a vastly different predatory niche (Nowell and and Sunquist 2008; Johnson et al. 2009; Lynam et al. 2013; Jackson 1996; Sunquist and Sunquist 2002), with clouded Singh and Macdonald 2017;Haidiretal. 2018; Mukherjee leopards feeding primarily on primates and small ungulates et al. 2019). Its temporal overlap with the dhole was moderate, and Asian golden cat feeding primarily on small rodents and which did not support our prediction that these two species some small ungulates. We conclude that the differences in should have high activity overlap. In NEPL, the Asian golden lifestyle and canine length result in significantly different di- cat was found to have a high dietary niche breadth and broad etary niches between clouded leopards and Asian golden cats, diet, which consisted mostly of muntjacs, murids and other which facilitated their coexistence without the need for tem- rodents (Kamler et al. 2020b). The activity of Asian golden poral partitioning. cats had moderate overlap with both muntjac species, squirrels The activity patterns of the Asian golden cat overlapped more and birds, indicating that the activity of this species was driven with those of the marbled cat than with those of the leopard cat, by prey rather than avoidance of dholes. Indeed, the which supported our prediction. We found that the marbled cat cathemeral activity of Asian golden cats may have been due was primarily diurnal which is consistent with that reported in to the diversity of their prey, which includes some species that previous studies (Johnson et al. 2009; Lynam et al. 2013;Sunarto were active during the day (e.g. muntjacs, squirrels, birds) and et al. 2015;Mukherjeeetal. 2019; Singh and Macdonald 2017; other prey species that were active at night (e.g. murids). Hearn et al. 2018). In NEPL, the activity of marbled cats coin- Although both dholes and Asian golden cats consumed munt- cided with the activity of avian and arboreal prey, indicating their jac in NEPL (Kamler et al. 2020a, b), the Asian golden cat activity pattern was driven by that of their main prey. The mar- consumed less muntjac and much larger quantities of smaller bled cat and Asian golden cat likely have different dietary niches, prey compared to dholes, indicating that there was little com- especially given that the Asian golden cat is about 3 times larger petition for food resources. Therefore, the diversity of both in body size than the marbled cat, and that the marbled cat is small and large prey, and both diurnal and nocturnal prey, in more arboreal than the Asian golden cat. Consequently, temporal the diet of Asian golden cats likely facilitated their coexistence partitioning apparently is not necessary to facilitate their coexis- with dholes without the need for temporal partitioning. tence. The Asian golden cat and leopard cat had low activity Overall, cathemerality and diversity in diet may enable overlap, primarily because the leopard cat was strongly noctur- the Asian golden cat to fit flexibly into the Southeast nal, similar to that reported in previous studies (Johnson et al. Asian felid and canid guild. 2009; Lynam et al. 2013; Sunarto et al. 2015; Singh and Mamm Res (2020) 65:679–689 687 Funding information This study was supported by an Exploration Grant Macdonald 2017;Hearnetal. 2018; Mukherjee et al. 2019;Can to AR from the National Geographic and a grant to DWM from the et al. 2020). The nocturnal activity of the leopard cat is likely Robertson Foundation. adapted to coincide with their main prey, which is predominantly murids (Kamler et al. 2020b). Thus, although leopard cats and Asian golden cats in NEPL were found to have moderate overlap Open Access This article is licensed under a Creative Commons in diets because of the consumption of small rodents (Kamler Attribution 4.0 International License, which permits use, sharing, et al. 2020b), temporal partitioning likely helped to facilitate their adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the coexistence. source, provide a link to the Creative Commons licence, and indicate if Leopard cats and marbled cats had low activity overlap, changes were made. The images or other third party material in this article which supported our prediction that they should exhibit temporal are included in the article's Creative Commons licence, unless indicated partitioning. It is likely that two felid species so similar in body otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not size likely partition other resources as well, such as diets. For permitted by statutory regulation or exceeds the permitted use, you will example, marbled cats are more arboreal than leopard cats; thus, need to obtain permission directly from the copyright holder. To view a the former likely feeds more on arboreal species, such squirrels copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. and birds, which are diurnal. In contrast, leopard cats prey pri- marily on nocturnal murids (Kamler et al. 2020b), which would facilitate dietary partitioning. We conclude that activity patterns of leopard cats and marbled cats are driven by their main prey, References rather than competition, and that differences in the activity of their presumed main prey facilitates temporal partitioning and Azlan JM, Sharma DSK (2006) The diversity and activity patterns of wild felids in a secondary forest in Peninsular Malaysia. Oryx 40:36–41. coexistence between these two small felids. https://doi.org/10.1017/s0030605306000147 Our camera trapping study was large-scale, repeated and Bashir T, Bhattacharya T, Poudyal K, Roy M, Sathyakumar S (2014) robust, but we lacked spatial and complete dietary data to Precarious status of the endangered dhole Cuon alpinus in the high frame the interpretation of our results. Additionally, our data elevation Eastern Himalayan habitats of Khangchendzonga Biosphere Reserve, Sikkim, India. 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Temporal partitioning by felids, dholes and their potential prey in northern Laos

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Abstract

Temporal partitioning can allow sympatric carnivores to coexist, especially if overlap of other resources is high. Using camera trap data from 2013 to 2017, we investigated the temporal partitioning of a community of wild felids and a canid in Nam Et–Phou Louey National Protected Area, Laos, to determine the extent to which temporal avoidance might be facilitating coexistence of similarly sized carnivores. We also investigated temporal overlap of these carnivore species and their presumed main prey, to determine if their activity is likely most influenced by their prey or potential competitors. The dhole (Cuon alpinus) and clouded leopard (Neofelis nebulosa), the two largest carnivores, had low temporal overlap, and activity appeared to be synchronized with the main prey for dhole, but not clouded leopard. Thus, it was possible that clouded leopard used temporal partitioning to coexist with dhole. The temporal overlap of Asian golden cat (Catopuma temminckii) was high with clouded leopard and moderate with dhole, and overall appeared to be influenced most by its presumed prey species, rather than by its potential competitors. The two small felids had the least temporal overlap between any species, as the marbled cat (Pardofelis marmorata) was primarily diurnal whereas the leopard cat (Prionailurus bengalensis) was primarily nocturnal. Given that the two small felids reportedly have similar diets consisting of small rodents and birds, their temporal partitioning is likely to help facilitate their coexistence. For carnivore species in northern Laos that are most similar in body size and diet, temporal partitioning is likely to be an important mechanism of coexistence. Otherwise, temporal patterns appear to be synchronized with their main prey. . . . . . . Keywords Activity pattern Asian golden cat Clouded leopard Dhole Lao PDR Leopard cat Marbled cat Introduction which include space, time and food (Case and Gilpin 1974; Schoener 1974). In particular, dietary overlap often drives Species coexistence is one of the most complex topics in ecol- interference competition within carnivore guilds; therefore, ogy (Gordon 2000). In principle, species that are ecologically food niche differences can be key to successful sympatry similar cannot coexist in the same area (Hardin 1960). For (Tsunoda et al. 2017). If dietary partitioning between such species to coexist, theory anticipates some degree of similarly-sized carnivores is low, then partitioning of other niche differentiation whereby interspecific competition is re- resources is necessary to reduce intraguild predation and fa- duced (Schoener 1974). Niche differentiation of ecologically cilitate coexistence (Case and Gilpin 1974;Schoener 1974; similar species may occur in one or more niche dimensions Holt and Polis 1997). Temporal partitioning has been shown to reduce interference competition and facilitate coexistence Communicated by: Krzysztof Schmidt among species (Kronfeld-Schor and Dayan 2003;Hayward and Slotow 2009). Additionally, small felids and small canids Electronic supplementary material The online version of this article (https://doi.org/10.1007/s13364-020-00524-9) contains supplementary have been shown to use temporal partitioning to coexist with material, which is available to authorized users. larger members of their guilds (Kamler et al. 2012b, 2013; Lynam et al. 2013; McCarthy et al. 2015b; Hearn et al. * Akchousanh Rasphone 2018; Santos et al. 2019), especially those with high dietary akchousanhr@yahoo.com overlap (Lucherini et al. 2009; Nagy-Reis et al. 2019). However, activity patterns are determined by numerous fac- Wildlife Conservation Research Unit, Department of Zoology, tors, and often activity patterns of carnivores are driven by the Recanati-Kaplan Centre, University of Oxford, Tubney House, activity of their main prey (Lucherini et al. 2009; Nagy-Reis Abingdon Road, Tubney, Abingdon OX13 5QL, UK 680 Mamm Res (2020) 65:679–689 et al. 2019). Understanding the factors that drive the activity felids, such as leopards (Panthera pardus) and pumas (Puma patterns of carnivorous species can be important for under- concolor), during encounters due to their numerical advantage standing their ecological niche, especially in regard to their (Venkataraman 1995; Ruth et al. 2019). Therefore, dholes relationships with other carnivores and their main prey. likely behaviourally dominate clouded leopards as well. Nam Et–Phou Louey National Protected Area (hereafter Based on body size, the next most dominant carnivore should NEPL) in northern Laos is known for its diverse carnivore be the Asian golden cat, followed by leopard cats and marbled community (Johnson et al. 2009), yet little is known regarding cats (Table 1). Although the activity patterns of these species the ecology of those carnivore species and their ecological have been determined in previous studies (Table 1), activity interactions. Large carnivores, tiger Panthera tigris and leop- patterns of a species can vary across sites due to differences in ard P. pardus, were part of the NEPL community, but they numbers of competitors, prey and humans (Valeix et al. 2007; recently became extirpated (Rasphone et al. 2019). Currently, Lucherini et al. 2009;Kamleretal. 2013;Ngoprasert etal. the canid and felid communities of the NEPL consist of large 2017). Regardless, it is not known if the activities of these (> 15 kg; dhole Cuon alpinus, clouded leopard Neofelis carnivores are driven by competition within their guild or by nebulosa), medium (5–15 kg; Asian golden cat Catopuma their main prey. Better knowledge of the ecological relation- temminckii), and small-sized (< 5 kg; marbled cat Pardofelis ships of this carnivore community in NEPL could assist con- marmorata, leopard cat Prionailurus bengalensis) species servation efforts for them, especially given that the IUCN has (Table 1). To date, the understanding of the coexistence of classified most of these carnivores as threatened or near threat- this diverse carnivore community is poorly known ened (Table 1). For example, increased human activities in (Grassman et al. 2005a;Ngoprasert etal. 2012; Lynam et al. parks, including tourism, can cause shifts in carnivore activity 2013; McCarthy et al. 2015b; Hearn et al. 2018; Can et al. patterns, which can reduce the health, reproduction and sur- 2020). Clearly, more data would better elucidate their mecha- vival of carnivores (Ngoprasert et al. 2017). nisms of coexistence, especially after the extirpation of the We used camera-trap surveys to determine the activity pat- largest carnivores, which might have changed the interactions terns of felid species and dholes in NEPL. Our primary objec- between the remaining carnivores and their prey (Estes et al. tives were to determine the temporal overlap between the carni- 2011;Ripple etal. 2014). vores, as well as between the carnivores and their potential prey. Because competition among carnivores often is driven by Based on the body size of these species and their reported diets diet and body size (Donadio and Buskirk 2006), we assumed and activity patterns (Table 1), we made the following predic- that the two most dominant carnivores remaining in NEPL tions: (1) temporal overlap between dholes and clouded leopards were the dhole and the clouded leopard, which are similar in will be low, owing to their similarity in diets; (2) temporal over- body size and consume the largest prey (Table 1). Large ca- lap between dholes and Asian golden cats will be high, owing to nids, including dholes and wolves (Canis lupus), live in large their different dietary niches; (3) temporal overlap between packs (Kamler et al. 2015) and behaviourally dominate large clouded leopards and Asian golden cats will be low, owing to Table 1 Summary of the reported ecology of the felid and canid community inhabiting the Nam Et–Phou Louey National Protected Area, Laos. The current IUCN status is given after each species (EN = endangered, VU = vulnerable, NT = near threatened, LC = least concern) 1 1 Species Body size (kg) Lifestyle Activity Primary prey species 2 3 4,5 Dhole (EN) 15–21 Terrestrial Diurnal Small, medium and large ungulate 6 6 6 Clouded leopard (VU) 15–23 Semi-arboreal Nocturnal, crepuscular Small ungulate, primate, porcupine, sciurid, bird 7 7 8 Asian golden cat (NT) 12–15 Terrestrial Cathemeral, crepuscular Small ungulate, murid, sciurid, bird 9 9 8 Leopard cat (LC) 3–5 Terrestrial Nocturnal, crepuscular Murid, sciurid, bird 10 10 10 Marbled cat (NT) 2–4 Semi-arboreal Diurnal, crepuscular Murid, sciurid, bird Francis (2019) Kamler et al. (2015) Kamler et al. (2012a) Kamler et al. (2020a) Thinley et al. (2011) Grassman et al. (2016) McCarthy et al. (2015a) Kamler et al. (2020b) Ross et al. (2015) Ross et al. (2016) Mamm Res (2020) 65:679–689 681 similarities in their body size and diet; (4) temporal overlap be- rainfall ranges from 1400 to 1800 mm (Johnson 2012). The tween Asian golden cats and marbled cats will be higher than the NEPL is divided into two protected zones; a totally protected overlap between Asian golden cats and leopard cats, based on zone where human activity (except for protected area manage- results from previous studies; and (5) temporal overlap between ment) is prohibited and a peripheral managed use zone where leopard cats and marbled cats will be low, owing to their simi- specified livelihood activities are permitted following park larity in diets. regulations (Fig. 1). Materials and methods Camera trapping Study area Systematic camera trap surveys, with clouded leopards as the focal species, were carried out from 2013 to 2017 within the The NEPL is located in the northern highlands of Laos (be- NEPL core zone, in four ~ 200 km blocks (Fig. 1), for a total tween latitude 19° 50′–20° 50′ N and longitude 103° 00′–103° of 32,027 trap days (Supplementary Data S1). These four 53′ E), bordering Vietnam along its northern boundary sampling blocks are known as Nam Poung–Na Vaen (Fig. 1). It covers an area of 5969 km with rugged topography (NPNV), Pha Daeng (PD), Phoupha–Siphou (PS) and across seven districts and three provinces (Houaphan, Luang Nam Neun (NN; Fig. 1). For each block, camera traps Prabang and Xiengkhuang) and elevation ranging from 400 to were set in pairs at 80 locations, except for block NN 2257 m, of which > 60% is above 1000 m and 91% with where cameras were set at only 60 locations, with 1– slopes > 12% (Johnson 2012). Vegetation is dominated by 1.5 km spacing between stations based on the home- dry evergreen and semi-evergreen forests. However, around range size of clouded leopards (Hearn et al. 2019). one third of the park is degraded forest with a canopy cover of We used a mixture of three infrared camera trap less than 20%. The climate in Laos is tropical monsoonal with models: CuddeBack Ambush IR - Model 1187, a rainy season lasting from May to October, followed by a Reconyx Hyperfire HC500, and MAGINON – WK 3 distinct dry season for the remainder of the year. Annual HD (Supra Foto-Elektronik-Vertriebs-GmbH). Fig. 1 The Nam Et–Phou Louey National Protected Area (NEPL), Laos, showing locations of the four survey blocks from 2013 to 2017 (NPNV = Nam Poung–Na Vaen; PD = Pha Daeng; PS = Phoupha–Siphou; NN = Nam Neun). The inset map shows the location of the NEPL in Laos 682 Mamm Res (2020) 65:679–689 Traps sites were from 629 to 2185 m altitude time of detection t is the proportion of hours and minutes in (Supplementary Data S1) where 16% of the sites were below 1 day. A measure of overlap under this approach was calcu- 1000 m, 16% were between 1000 and 1500 m, and 68% were lated by fitting non-parametric kernel density functions to the above 1500 m. About 63% of the sites were in closed forest, species’ diel activity data (Ridout and Linkie 2009;Linkieand which comprised evergreen and high density semi-evergreen Ridout 2011) and was performed using the package over- forests. The camera traps were placed mostly along ridge lines lap_0.3.0 in R (Meredith and Ridout 2014). The coefficient and animal trails, and at intersections where trails meet of overlap (Δ) is calculated as the proportion of overlap be- streams. Each camera was mounted onto a tree trunk with its tween the two species’ diel activity curves (Ridout and Linkie motion beam set at ca. 35 cm height from the ground at the 2009). We calculated the coefficients of overlap as a spectrum centre of the trail (approx. shoulder height of an adult clouded of proportional values, with 1 indicating complete overlap and leopard). Each survey period lasted for a minimum of 50 days 0 indicatingnooverlap.Schmid and Schmidt(2006)proposed (Supplementary Data S1). Each camera-trap photo of an ani- five estimators of Δ, and we used the non-parametric estima- mal was identified and organised using the CamtrapR tor Δ because of its superiority for sample sizes that are (Niedballa et al. 2016). Notionally independent events were greater than 50 (Ridout and Linkie 2009; Meredith and considered if they were > 30 min apart (O’Brien et al. 2003). Ridout 2014). Following Lynam et al. (2013), values of Δ ≥ 0.70 and Δ < 0.35 were defined as a high overlap and a low Circadian activity and overlap analysis overlap in diel activity, respectively. In addition to modelling activity overlap for the selected Quantitatively investigating activity patterns is challenging be- species pairs, an activity overlap of each selected carnivore cause time is a wrapped distribution with an arbitrary zero point; species with each of its presumed principle prey species was thus, traditional statistical methods cannot be applied (Frey et al. also modelled. Five ungulate species have been identified as 2017). To solve this, activity patterns can be examined using prey species for dhole in NEPL (Kamler et al. 2020a): small circular statistics which derive descriptive statistics of temporal dark muntjac (M. rooseveltorum complex), northern red munt- data using trigonometric functions (Zar 1996;Freyet al. 2017). jac (Muntiacus vaginalis), sambar (Cervus unicolor), main- Therefore, we used circular statistics to describe activity patterns land serow (Capricornis milneedwardsii) and Eurasian wild of carnivores and potential prey in NEPL. Percentage of detec- pig (Sus scrofa). For the clouded leopard, a wide range of tions recorded for each hour over a 24-h period was used in the species have been considered as its potential prey (Table 1), modelling following Ross et al. (2013). Diel activity patterns including, in a Lao context, small- and medium-sized ungu- models were fitted as a function of continuous trigonometric lates, four species of macaque, two porcupine species, squir- predictors describing one (cosΘ, sinΘ)and two(cos2Θ, sin2Θ) rels, ground-dwelling birds and other small birds (Ross et al. complete cycles in a 24-h period with Θ =πt/24,where t is time 2013;Grassman et al. 2016). For the Asian golden cat, poten- in hours (Ross et al. 2013). For sinΘ, a species is considered tial prey in NEPL included muntjacs, porcupines, squirrels, crepuscular with a single activity peak either at dawn (if positive ground-dwelling birds, other small birds and rats/mice coefficient) or dusk (if negative coefficient). For cosΘ, a species (Kamler et al. 2020b). The potential prey of the leopard cat is considered nocturnal with a positive coefficient or diurnal with and marbled cat are squirrels, birds and rats/mice (Ross et al. a negative coefficient. For the bimodal sin2Θ, positive values 2016; Kamler et al. 2020b). Although the camera-trap survey indicate a species’ peak at pre-dawn and pre-dusk whereas neg- was designed for the clouded leopard, we assumed that it ative values indicate activity peaks at post-dawn and post-dusk. would accurately record the activity patterns of sympatric car- For the bimodal cos2Θ, a species is considered crepuscular and nivores and their potential prey. Although some prey species active at both dawn and dusk (if negative coefficient) or at both (e.g. primates) were mostly arboreal, we assumed their midday and midnight (if positive coefficient). With this ap- ground-level activity detected by the cameras were consistent proach, activity overlap between paired species was also tested with their overall activity patterns. through the construction of models representing the full 24- hcycles(SinΘ, CosΘ, Sin2Θ, Cos2Θ). An ANOVA test was then conducted for each model to test for significant difference Results between the activity of each pair of species, and the model with the highest adjusted R was selected. This analysis was carried Of the five carnivore species, the leopard cat had the highest out in the R program (R Core Team 2017). number of notionally independent photographs followed by In addition, the kernel density method was implemented to the Asian golden cat, whereas the marbled cat had the lowest examine the difference in activity pattern between each pair of number of independent events (Table 2). Out of the three species (Ridout and Linkie 2009). In the kernel density ap- survey blocks where camera trapping was repeated three proach, observed capture times are regarded as random sam- times, PD yielded the most notionally independent records ples from continuous underlying distributions, and a species’ for all felids but the fewest for dhole (Table 2). Among the Mamm Res (2020) 65:679–689 683 Table 2 The number of Survey block notionally independent records of felids and dhole, and presumed Species NN NPNV PD PS prey species from each survey block (NPNV = Nam Poung–Na Asian golden cat (Catopuma temminckii) 8 53 73 38 Vaen; PD = Pha Daeng; PS = Phoupha – Siphou; NN = Nam Clouded leopard (Neofelis nebulosa) 5 34 56 52 Neun) in Nam Et–Phou Louey Dhole (Cuon alpinus) 3 67 30 57 National Protected Area, Laos, Leopard cat (Prionailurus bengalensis) 3 61 79 60 2013–2017 Marbled cat (Pardofelis marmorata) 2 45 47 31 Asiatic brush-tailed porcupine (Atherurus macrourus) 3 93 119 42 Assamese macaque (Macaca assamensis) 5 18 11 13 Small dark muntjac(s) (M. rooseveltorum complex.) 2 206 210 36 East Asian porcupine (Hystrix brachyura)17 136 167 70 Eurasian wild pig (Sus scrofa)21 120 147 62 Grey peacock pheasant (Polyplectron bicalcaratum) 8 40 187 22 Indochinese serow (Capricornis milneedwardsii) 7 128 107 32 Northern pig-tailed macaque (Macaca leonina) – 31 10 Red junglefowl (Gallus gallus) 7 18 105 17 Northern red muntjac (Muntiacus vaginalis) 83 489 629 292 Red-cheeked squirrel (Dremomys rufigenis) – 526 28 Rhesus macaque (Macaca mulatta)5 6 13 15 Sambar (Cervus unicolor) 4 98 29 45 Silver pheasant (Lophura nycthemera)12 81 74 59 Stump-tailed macaque (Macaca arctoides)81 385 457 37 Birds spp. 3 66 73 49 Rat/mouse spp. (Muridae) 8 78 134 191 Squirrels spp. (Sciuridae) 2 26 108 46 presumed prey species, the northern red muntjac had the most Diel activity overlap between carnivores records in all blocks, followed by the stump-tailed macaque Macaca arctoides. Three out of four species of macaques The results from the wave analysis showed that there detected during the study had fewer than 50 notionally inde- was a difference in activity within each pair of pendent records, which were relatively low compared with species (best models of most pairs were P < 0.05; those of all other prey species (Table 2), presumably because Table 4). The activity overlap between dhole and of the greater arboreality of the macaque species. clouded leopard (0.51 Δ ;Fig. 2a) was slightly lower than that between dhole and Asian golden cat (0.66 Δ ;Fig. 2b). Although our wave analysis suggested sig- Circadian activity nificant difference in Cos2Θ (P = 0.038) between clouded leopard and Asian golden cat, the SinΘ was There was strong evidence that activity patterns differed not significant (P =0.753; Table 4). This indicated a high among the five carnivore species (CosΘ*Species: F = level of overlap between the clouded leopard and the 14.78, P <0.001; SinΘ*Species: F =3.22, P =0.01). Asian golden cat, a result consistent with the kernel den- The dhole showed a strongly diurnal and crepuscular (both sity analysis which also indicated a strong overlap in dawn and dusk) pattern of activity, with the highest peak of activity between them (0.80 Δ ;Fig. 2c). We found that activity at dusk (Table 3;Fig. 2a). The clouded leopard was activity overlap between the Asian golden cat and the strongly crepuscular, but most active at dawn (Table 3;Fig. marbled cat was much higher than the overlap between 2a). The Asian golden cat was active both by day and by night the Asian golden cat and the leopard cat (0.74 Δ and (Fig. 2b) but with a peak of activity at dawn (Table 3). The 0.55 Δ ;Fig. 2e, d). Notably, the leopard cat and the leopard cat was clearly nocturnal while the marbled cat was marbled cat had the lowest overlap in activity between strongly diurnal with some activity at dawn and dusk (Table 3; any two carnivore species (0.31 Δ ;Fig. 2f). Fig. 2f). 684 Mamm Res (2020) 65:679–689 Table 3 Estimates of coefficients (± SE) of diel activity models and best marbled cat) in Nam Et–Phou Louey National Protected Area, Laos, models with adjusted R values for five carnivore species (D = dhole; 2013–2017. Significant values are designated with *P <0.05, CL = clouded leopard; AC = Asian golden cat; LC = leopard cat; MC = **P < 0.01, and ***P <0.001 1 2 3 4 2 SinΘ CosΘ Sin2Θ Cos2Θ Best model Adjusted R D 0.009 ± 0.005 − 0.023 ± 0.005*** 0.006 ± 0.005 − 0.017 ± 0.005** CosΘ + Cos2Θ 0.533 CL 0.035 ± 0.005*** 0.006 ± 0.005 − 0.004 ± 0.005 − 0.021 ± 0.005*** SinΘ + Cos2Θ 0.737 AC 0.025 ± 0.006*** − 0.002 ± 0.006 − 0.003 ± 0.006 − 0.002 ± 0.006 SinΘ 0.413 LC 0.008 ± 0.006 0.031 ± 0.006*** 0.002 ± 0.006 − 0.002 ± 0.006 CosΘ 0.495 MC 0.019 ± 0.008* − 0.030 ± 0.008*** − 0.009 ± 0.008 − 0.020 ± 0.008* SinΘ + CosΘ + Cos2Θ 0.506 1 2 For sinΘ, a species is considered crepuscular with a single activity peak either at dawn (if positive coefficient) or dusk (if negative coefficient). For cosΘ, a species is considered nocturnal with a positive coefficient or diurnal with a negative coefficient For the bimodal sin2Θ, positive values indicate a species’ peak at pre-dawn and pre-dusk whereas negative values indicate activity peaks at post-dawn and post-dusk For the bimodal cos2Θ, a species is considered crepuscular and active at both dawn and dusk (if negative coefficient) or at both midday and midnight (if positive coefficient) Diel activity overlap between carnivores and their appeared to be synchronized with that of their main prey. prey Thus, our research supports previous studies that showed tem- poral partitioning can reduce interference competition and fa- Dhole activity overlapped most strongly with the dark munt- cilitate coexistence among carnivores, especially those with jac (0.85 Δ ) and the Eurasian wild pig (0.80 Δ ). While both high dietary overlap (Kronfeld-Schor and Dayan 2003; 4 4 prey species were strongly diurnal, there was a peak of activity Hayward and Slotow 2009; Lucherini et al. 2009;Nagy- of the dark muntjac at dusk, closely corresponding to the Reis et al. 2019). For example, the temporal overlap was activity of the dhole (Supplementary Data S2.1a). Overall, low between dholes and clouded leopards, which supported the overlap coefficients between the clouded leopard and their our prediction, indicating temporal partitioning occurred be- candidate prey species were greater than 0.40 Δ tween these species. Dholes were mostly diurnal with a peak (Supplementary Data S2.2). The strongest overlaps were be- of activity at dusk, which is consistent with findings elsewhere tween the clouded leopard and (i) sambar and (ii) Indochinese (Grassman et al. 2005b; Kawanishi and Sunquist 2008; serow (0.79 Δ and 0.75 Δ , respectively). Clouded leopard Kamler et al. 2012a;Bashiret al. 2014). Dhole activity over- 4 4 overlapped most with the prey species that had an activity lapped moderately to strongly with both muntjac species. peak at dawn. Previous research in NEPL and elsewhere in Southeast Asia The Asian golden cat’s activity overlapped strongly with showed that muntjacs were the most preferred prey of dholes that of both types of muntjacs, squirrels and all listed bird regardless of ungulate diversity and densities (Kamler et al. species (with overlap coefficients > 0.70 Δ ; Supplementary 2020a), indicating that the activity of dholes was driven by the Data S2.3); these overlaps were more strongly congruent than activity of their most preferred prey. Clouded leopard activity those revealed for clouded leopard and their candidate prey was crepuscular with a peak at dawn, similar to that observed species. Asian golden cat overlapped most with prey that were in some areas (Azlan and Sharma 2006; Lynam et al. 2013; active by day, and it overlapped little with porcupines (0.45 McCarthy et al. 2015b), but not others (Singh and Macdonald Δ ) and rats/mice (0.42 Δ ). Insofar as rats/mice were strong- 2017; Hearn et al. 2018; Mukherjee et al. 2019; Can et al. 4 4 ly nocturnal, these prey species overlapped strongly with leop- 2020). Although clouded leopard activity synchronised with ard cat (0.84 Δ ; Supplementary Data S2.4f). The marbled cat that of the Indochinese serow and sambar, it is doubtful that overlapped most strongly with candidate prey that were more these two species are preferred prey of clouded leopards, giv- diurnal such as squirrels and birds (with overlap coefficients > en the large body size of these ungulates relative to that of 0.70; Supplementary Data S2.5a - e). clouded leopards. Instead, the preferred prey of clouded Fig. 2 Overlap in temporal activity between (a) dhole and clouded Discussion „ leopard, (b) dhole and Asian golden cat, (c) clouded leopard and Asian golden cat, (d) Asian golden cat and leopard cat, (e) Asian golden cat and Temporal partitioning among carnivores in NEPL was exhib- marbled cat, and (f) leopard cat and marbled cat in Nam Et–Phou Louey ited only between species that were similar in body size, and National Protected Area, Laos (2013–2017), as measured by the kernel density across the 24-h period likely had similar diets. Otherwise, the activity of carnivores Mamm Res (2020) 65:679–689 685 (a) Dhole vs. Clouded leopard (Δ4=0.51; CI=0.39-0.57) (b) Dhole vs. Asian golden cat (Δ4=0.66; CI=0.55-0.74) (c) Clouded leopard vs. Asian golden cat (Δ4=0.80; CI=0.68-0.86) (d) Asian golden cat vs Leopard cat (Δ4=0.55; CI=0.43-0.60) (e) Asian golden cat vs. Marbled cat (Δ4=0.74; CI=0.65-0.81) (f) Leopard cat vs. Marbled cat (Δ4=0.31; CI=0.20-0.33) 686 Mamm Res (2020) 65:679–689 Table 4 Overlap estimates Species pairing Kernel density (Δ ) Wave Adjusted R P(t) between carnivore species 4 calculated from the kernel density Dhole–clouded leopard 0.51 SinΘ 0.525 0.009 (− 2.919) (correlation coefficient Δ ), and significant wave(s) of best models CosΘ 0.046 (− 2.145) for the interactions, from camera- Dhole–Asian golden cat 0.66 SinΘ 0.604 0.010 (− 2.874) trap data collected in Nam Et– CosΘ 0.046 (− 2.144) Phou Louey National Protected Area, Laos, 2013–2017. The P(t) Clouded leopard–Asian golden cat 0.80 SinΘ 0.682 0.753 (− 0.319) represents the P value with the Cos2Θ 0.038 (− 2.233) associated test statistic (t)inpa- Asian golden cat–leopard cat 0.55 SinΘ 0.722 0.044 (− 2.161) rentheses; P < 0.05 indicate that CosΘ < 0.001 (4.992) species differ in the correspond- ing wave Asian golden cat–marbled cat 0.74 SinΘ 0.475 0.278 (− 1.117) CosΘ 0.076 (− 1.883) Leopard cat–marbled cat 0.31 CosΘ 0.366 0.002 (− 3.540) Cos2Θ 0.372 (− 0.915) leopards is most likely smaller prey species such as muntjacs Clouded leopards and Asian golden cats had similar activ- and primates (Table 1), although activity overlap with these ity patterns, which did not support our prediction that they prey species was low. Therefore, we conclude that activity of should exhibit temporal partitioning. Our results were similar clouded leopards was most influenced by avoidance of dholes, to that found in Sumatra, where Sunda clouded leopards rather than prey, likely because the pack-living dholes are (Neofelis diardi) and Asian golden cats had high temporal behaviorally dominant over clouded leopards. overlap (McCarthy et al. 2015b). McCarthy et al. (2015b) The activity pattern of the only meso-carnivore in NEPL, speculated that differences in resource exploitation due to the Asian golden cat, was crepuscular with activity intensified the clouded leopard’s greater arboreality facilitated their co- from dawn until midmorning. Based on the kernel density existence with Asian golden cats. Additionally, the signifi- activity plot, the species seemed to be active both day and cantly greater canine length in clouded leopards suggests that night, which is consistent with previous studies (Kawanishi they have a vastly different predatory niche (Nowell and and Sunquist 2008; Johnson et al. 2009; Lynam et al. 2013; Jackson 1996; Sunquist and Sunquist 2002), with clouded Singh and Macdonald 2017;Haidiretal. 2018; Mukherjee leopards feeding primarily on primates and small ungulates et al. 2019). Its temporal overlap with the dhole was moderate, and Asian golden cat feeding primarily on small rodents and which did not support our prediction that these two species some small ungulates. We conclude that the differences in should have high activity overlap. In NEPL, the Asian golden lifestyle and canine length result in significantly different di- cat was found to have a high dietary niche breadth and broad etary niches between clouded leopards and Asian golden cats, diet, which consisted mostly of muntjacs, murids and other which facilitated their coexistence without the need for tem- rodents (Kamler et al. 2020b). The activity of Asian golden poral partitioning. cats had moderate overlap with both muntjac species, squirrels The activity patterns of the Asian golden cat overlapped more and birds, indicating that the activity of this species was driven with those of the marbled cat than with those of the leopard cat, by prey rather than avoidance of dholes. Indeed, the which supported our prediction. We found that the marbled cat cathemeral activity of Asian golden cats may have been due was primarily diurnal which is consistent with that reported in to the diversity of their prey, which includes some species that previous studies (Johnson et al. 2009; Lynam et al. 2013;Sunarto were active during the day (e.g. muntjacs, squirrels, birds) and et al. 2015;Mukherjeeetal. 2019; Singh and Macdonald 2017; other prey species that were active at night (e.g. murids). Hearn et al. 2018). In NEPL, the activity of marbled cats coin- Although both dholes and Asian golden cats consumed munt- cided with the activity of avian and arboreal prey, indicating their jac in NEPL (Kamler et al. 2020a, b), the Asian golden cat activity pattern was driven by that of their main prey. The mar- consumed less muntjac and much larger quantities of smaller bled cat and Asian golden cat likely have different dietary niches, prey compared to dholes, indicating that there was little com- especially given that the Asian golden cat is about 3 times larger petition for food resources. Therefore, the diversity of both in body size than the marbled cat, and that the marbled cat is small and large prey, and both diurnal and nocturnal prey, in more arboreal than the Asian golden cat. Consequently, temporal the diet of Asian golden cats likely facilitated their coexistence partitioning apparently is not necessary to facilitate their coexis- with dholes without the need for temporal partitioning. tence. The Asian golden cat and leopard cat had low activity Overall, cathemerality and diversity in diet may enable overlap, primarily because the leopard cat was strongly noctur- the Asian golden cat to fit flexibly into the Southeast nal, similar to that reported in previous studies (Johnson et al. Asian felid and canid guild. 2009; Lynam et al. 2013; Sunarto et al. 2015; Singh and Mamm Res (2020) 65:679–689 687 Funding information This study was supported by an Exploration Grant Macdonald 2017;Hearnetal. 2018; Mukherjee et al. 2019;Can to AR from the National Geographic and a grant to DWM from the et al. 2020). The nocturnal activity of the leopard cat is likely Robertson Foundation. adapted to coincide with their main prey, which is predominantly murids (Kamler et al. 2020b). Thus, although leopard cats and Asian golden cats in NEPL were found to have moderate overlap Open Access This article is licensed under a Creative Commons in diets because of the consumption of small rodents (Kamler Attribution 4.0 International License, which permits use, sharing, et al. 2020b), temporal partitioning likely helped to facilitate their adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the coexistence. source, provide a link to the Creative Commons licence, and indicate if Leopard cats and marbled cats had low activity overlap, changes were made. The images or other third party material in this article which supported our prediction that they should exhibit temporal are included in the article's Creative Commons licence, unless indicated partitioning. It is likely that two felid species so similar in body otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not size likely partition other resources as well, such as diets. For permitted by statutory regulation or exceeds the permitted use, you will example, marbled cats are more arboreal than leopard cats; thus, need to obtain permission directly from the copyright holder. To view a the former likely feeds more on arboreal species, such squirrels copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. and birds, which are diurnal. In contrast, leopard cats prey pri- marily on nocturnal murids (Kamler et al. 2020b), which would facilitate dietary partitioning. 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Published: Oct 12, 2020

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