Sunda Clouded Leopard Neofelis Diardi Densities and Human Activities in the Humid Evergreen Rainforests of Sumatra

Home , Sumatran tiger, Sunda clouded leopard

Sunda clouded leopard Neofelis diardi densities and human activities in the humid evergreen rainforests of Sumatra

I DING H AIDIR,DAVID W. MACDONALD and M ATTHEW L INKIE

Abstract Most species of wild felids are threatened, but for Introduction many little is known about their status in the wild. For the cryptic and elusive Vulnerable Sunda clouded leopard cross the tropics of Latin America, Africa and Asia, in- Neofelis diardi, key metrics such as abundance and occu- Aformation on wild felids tends to be based on indirect pancy have been challenging to obtain. We conducted an signs because dense vegetation typically precludes direct intensive survey for this species on the Indonesian island observations and because these species tend to be rare as a  of Sumatra. We deployed camera traps across four study result of their trophic status (Carter et al., ; Rayan &  ę  areas that varied in elevation and threats, for a total of Linkie, ;J drzejewski et al., ). Remote detection de- , trap nights, resulting in  independent clouded vices, primarily camera traps, facilitate surveying felids that leopard photographs, in which we identified  individuals. are otherwise difficult to detect, enabling researchers to Using a Bayesian spatially explicit capture–recapture anal- investigate felid ecology and population status, and gain a ysis, we estimated clouded leopard density to be .–. better understanding of the threats to these species (Linkie     individuals/ km . The highest predicted occurrence of et al., ; Kawanishi et al., ; Henschel et al., ;   people was at lower altitudes and closer to the forest edge, Rich et al., ). There are felid species in South-east where we categorized more than two-thirds of people re- Asia, occurring in open savannahs, deciduous forests and corded by camera traps as bird poachers, .% each as un- humid evergreen forests along the equator (Sunquist &  gulate/tiger poachers and non-timber collectors, and , % Sunquist, ). Little is known about most of these spe- as fishers. Our findings provide important insights into the cies, particularly the smaller-bodied ones. However, recent status of this little known species in Sumatra. We recom- camera-trap surveys have provided new information on mend that the large volume of camera-trap data from the relative abundance, occupancy and/or habitat prefer- other Sumatran landscapes be used for an island-wide as- ence of the Sunda clouded leopard Neofelis diardi, Asiatic sessment of the clouded leopard population, to provide golden cat Catopuma temminckii, Bornean bay cat Catopu- up-to-date and reliable information for guiding future ma badia, marbled cat Pardofelis marmorata, leopard cat conservation planning. Prionailurus bengalensis and flat-headed cat Prionailurus planiceps (Haidir et al., ; Wearn et al., ; McCarthy Keywords Camera trap, clouded leopard, felid, Kerinci et al., ; Hearn et al., a; Rustam et al., ). Seblat National Park, Neofelis diardi, poaching, spatially To date, wildlife research in Sumatra has mainly focused explicit capture–recapture on the Indonesian Ministry of Environment and Forestry’s Supplementary material for this article is available at priority species, the Sumatran tiger Panthera tigris suma- doi.org/./S trae, Sumatran elephant Elephas maximus sumatranus, Sumatran rhinoceros Dicerorhinus sumatrensis, Sumatran orangutan Pongo abelii and, most recently, the newly dis- covered Tapanuli orangutan Pongo tapanuliensis (Hedges et al., ; Wibisono & Pusparini, ; Pusparini et al., ; Sunarto et al., ; Nowak et al., ). This attention is justified because these flagship species or subspecies are endemic, categorized as Critically Endangered on the IUCN Red List, and able to attract international attention and conservation funds that provide wider benefits to the IDING HAIDIR* (Corresponding author, orcid.org/0000-0003-2994-2942) Kerinci Seblat National Park Authority, Indonesian Ministry of Environment wildlife, rainforest habitats and protected areas within and Forestry, Jambi, Indonesia. E-mail [email protected] their range. However, the Sunda clouded leopard can also DAVID W. MACDONALD Department of Zoology, Wildlife Conservation Research play a role as a wildlife conservation ambassador, as shown Unit, University of Oxford, The Recanati-Kaplan Centre, Tubney, UK elsewhere in Asia, through its ability to generate political MATTHEW LINKIE Wildlife Conservation Society, Bogor, Indonesia support for both the species itself and the protected areas *Also at: Department of Zoology, Wildlife Conservation Research Unit,  University of Oxford, The Recanati-Kaplan Centre, Tubney, UK it inhabits (Macdonald et al., ). Received  March . Revision requested  June . Here we investigate demographic parameters of Sunda Accepted  August . First published online  June . clouded leopards in four rainforest areas in one of

This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, Downloadeddistribution, from https://www.cambridge.org/core and reproduction in any medium,. IP address: provided 170.106.33.22 the original work, onis 26 properly Sep 2021 cited. at 08:28:14, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/termsOryx, 2021, 55(2), 189–196 ©. https://doi.org/10.1017/S0030605319001005The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319001005 190 I. Haidir et al.

South-east Asia’s largest protected areas, Kerinci Seblat National Park in west-central Sumatra. The study areas are characterized by different forest types, elevation gradients and human disturbance levels. Our study builds on earlier work that was based on bycatch data from a tiger survey in four study areas in the Park, with estimated Sunda clouded leopard densities of .–. individuals/   km (Sollmann et al., ). We conducted surveys that specifically focused on small to medium-sized felids and applied analyses that explore additional research questions. For example, we examined how detection probability, movement distribution and density of Sunda clouded leopards vary amongst different forest types along an altitudinal gradient.

Study area

Kerinci Seblat National Park is a UNESCO World Heritage  Site on the island of Sumatra. The , km Kerinci Seblat forest landscape stretches along c.  km of the Bukit Barisan mountain range and covers the provinces of Jambi, Bengkulu, South Sumatra and West Sumatra. The altitude is –, m, with lowland forest ,  m   –   FIG. 1 Study areas in Kerinci Seblat National Park (KSNP), ( . % of the landscape), hill forest at m( . %), west-central Sumatra. submontane forest at –, m(.%), midmontane forest at ,–, m(.%) and upper montane and sub-  –  alpine forest . , m(.%). Our four study areas were trail, with a spacing of . . km between camera stations  Ipuh (lowland forest), Bungo and Sipurak (hill forest), and (Supplementary Table ). We used heat-motion sensor Renah Kayu Embun (submontane and midmontane forest; camera traps Cuddeback Ambush IR (Cuddeback, De Pere, Fig. , Table , Supplementary Table ). USA) and Panthera IV (Panthera, New York, USA), without any bait or lure to attract felids. We set camera traps to operate continuously for  months and visited stations every  Methods weeks for maintenance and data retrieval. We compiled all clouded leopard photographs, and at least three experienced Data collection project members then manually identified individual animals based on their unique pelage pattern. We used these – We conducted camera-trap surveys during June data to develop daily detection matrices. December  in Kerinci Seblat National Park and adjacent forest areas. We designed the surveys to target the Sunda clouded leopard, golden cat, marbled cat and leopard cat, Clouded leopard density by placing cameras on ridge trails and animal paths, with the majority (%) of camera traps placed where the forest Heterogeneity in the probability of detecting clouded leo- canopy was disrupted and the semi-arboreal felids could be pards can be influenced by a variety of factors, including expected to descend. All camera stations in Bungo, Sipurak sex and camera trap site-specific covariates, although with and Ipuh, and % of stations in Renah Kayu Embun, con- limited data it is not possible to derive sex-based density sisted of camera traps set up in pairs, to capture both flanks estimates (Efford & Fewster, ). We estimated popula- of passing animals. The camera traps within each study area tion abundance using a spatially explicit capture–recapture  covered  grid cells of  km . Prior to setting the cameras, method, which assumes that each individual animal has a we conducted reconnaissance surveys to determine the loca- unique activity centre and that its probability of detection tions in a grid cell that were most likely to record clouded decreases with increasing distance from this centre. We con- leopards and other small and medium-sized felids. We set structed daily detection matrices, which included the spatial up cameras within  m of the planned deployment points attributes of each individual, for each camera station. We at a height of – cm off the ground. The paired traps analysed camera-trap data and developed detection matrices were positioned at a distance of – m from the target using the package camtrapR in R .. (Niedballa et al., ).

Oryx, 2021, 55(2), 189–196 © The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319001005 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.22, on 26 Sep 2021 at 08:28:14, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605319001005 Sunda clouded leopard densities in Sumatra 191

2 We used a Bayesian spatially explicit capture–recapture approach with the R package SPACECAP .. ; I) and (Gopalaswamy et al., ) because it is more suitable for

 population estimations based on a small sample size

M = 91/F = 21 (Wearn et al., ; Hearn et al., b). We treated the

2 study areas as independent sites because they are separated by at least  km, and a previous study recorded daily movements of clouded leopards of .–. km, with home ranges  of – km (Grassman et al., ). In addition, altitude No. of recaptures (M/F) and forest types vary between the study areas, and some are separated by settlements, towns and major roads that could act as barriers to clouded leopard movement (Grassman et al., ; Linkie et al., ). Using QGIS .. (QGIS, ), we created a state space or habitat mask that describes the potential home range centre of an individual based on their spatial movements and habitat suitability. A habitat mask limits the ranges of individual

No. of individuals (M/F/Unknown) clouded leopard movement estimations to suitable (forested) areas (Gopalaswamy et al., ; Fig. ). We used a habitat mask with a  km buffer, based on movement patterns of clouded leopard studies from Malaysia and Bhutan that used a – and  km buffer,

No. of independent photos respectively (Hearn et al., ; Penjor et al., ). We applied the buffer around the minimum convex polygon con- taining all camera traps in a study area. Using a forest cover layer obtained from the Ministry of Environment and Forestry (KLHK, ), we then categorized the buffer detections in the four study areas in Sumatra, from an earlier study (Sollmann et al., area as habitat (forested area) or non-habitat (other areas), No. of trap nights with a resolution of . × . km. Data augmentation was based on  times the number of identified individual animals. For the analysis, we ran , iterations with a

Neofelis diardi burn-in of , and thinning of . We performed a Total duration (days) Geweke test to investigate models convergence in the Markov chain Monte Carlo that should have values close to zero, as an indication that the data calculation has con- verged. The model also estimated the Bayesian P-value to assess model fit, whereby a value of . indicates a per- Mean spacing of camera stations (km) fect fit, and values should not be close to . or . (Gopalaswamy et al., ). We used the density values derived from SPACECAP to test for differences between the study areas, whereby non- ) 2 overlapping upper and lower highest probability density es-

Minimum convex polygon around camera traps (km timates indicate a significant difference in density. However, overlapping highest probability densities could still be sig-

) consisted of two trapping phases. nificantly different, so we performed a Tukey’s honest sig- ,    nificant difference test, with P . as the significance

34 7638 322 75 64 706 2.00 61 0.87 238 3.50level 147 0.79 (i.e. 2,486 222 8,399 Pr( 110. 3,563 8|z|); 6,278 Tukey, 25 17 6 (5/1/0) 24). 6 (5/1/0) 7 (4/2/1) M = 7/F = 5 1 (1/2/2) M = M 23/F = = 12/F 1 = 4 M = 9/F = 15 No. of camera stations 115 293 1243 251 681 507 9,370 28,404 47 114 22 (17/4/1) 18 (12/4/2) M = 36/F = 6 I II I II I II I II I II I II I II I II

Anthropogenic pressure

To understand the anthropogenic pressures in the study

1 areas, we analysed camera-trap photographs of people. 1 Summary of camera-trap sampling effort and Sunda clouded leopard 1 Where possible, we categorized them as fishers (groups of ABLE Does not include photos of unidentified/unsexed individuals. Earlier study (Sollmann et al., ,  this study (II). Study area T   SipurakRenah Kayu EmbunIpuh 23Total 65 20 121 77 63 94 1.50 63 1.03 130 1.90 115 0.94 2,063 91 6,674 135 16 1,258 7,053 47 6 7 (6/1/0) 4 18 (3/1/0) 2 M (2/0/0) = 11/F = 1 3 M (2/1/0) = 45/F = 1 M = 6/F = 0 M = 14/F = 3 Bungo people with machetes and small backpacks, which are

TABLE 2 Spatially explicit capture–recapture analyses run using maximum likelihood SECR and SPACECAP for the four study areas, with density measured as number of adult individuals/   km in this study and an earlier study (Sollmann et al., ).

This study Earlier study Parameter1 Bayesian (95% HPD2) Bayesian (95% HPD2) Bungo D 2.38 (1.11–4.26) 1.62 (0.58–3.38) N 12.84 (6.00–23.00) σ (km) 3.35 (1.85–5.08) 2.59 (1.83–3.86) ƛ0 0.003 (0.001–0.005) 0.010 (0.004–0.021) Ѱ 0.20 (0.05–0.39) Sipurak D 2.05 (0.52–4.35) 0.77 (0.15–2.10) N 11.79 (3.00–25.00) FIG. 2 Estimated Sunda clouded leopard Neofelis diardi density σ (km) 2.32 (1.08–4.75) 4.48 (2.84–8.10) values derived from SPACECAP (box plots; black line in the box ƛ0 0.005 (0.000–0.011) 0.006 (0.002–0.014) is the median, box is % distribution of the data, the whiskers Ѱ 0.37 (0.05–0.77) represent minimum and maximum values, the circles represent Renah Kayu Embun outlier values) and associated occurrence of people (solid rectangles D 0.81 (0.66–1.33) 1.57 (0.52–2.38) represent the median, whiskers represent minimum and maximum N 4.86 (4.00–8.00) values) illegally entering each of the four study areas. σ (km) 5.34 (3.50–7.35) 4.48 (2.84–8.10) ƛ0 0.005 (0.002–0.009) 0.006 (0.002–0.014) Ѱ – typically used to carry fishing nets), collectors of non-timber 0.13 (0.03 0.24) Ipuh forest products (groups of – people without heavy equip- D 0.75 (0.73–0.88) 1.10 (0.42–2.24) ment such as rifles or machetes), bird poachers (groups N 5.15 (5.00–6.00) .  people carrying baskets/cages made from rattan, tree σ (km) 32.98 (9.66–49.37) 2.59 (1.83–3.86) branches or sticks with glue on one end, and small blades ƛ0 0.001 (0.000–0.001) 0.010 (0.004–0.021) ,  cm length), armed tiger/ungulate poachers (groups Ѱ 0.18 (0.08–0.28) ,    people carrying hunting rifles and/or spears, accompa- D, density (number of animals/ km ); N, number of individuals in the nied by hunting dogs, or who were detected during dusk or sampling area; σ, range parameter for an individual animal’s activity centre at night carrying small rucksacks and torches) and forest (i.e. the average distance of an individual animal’s activity centre to the low- patrol/monitoring team members (the latter being the est probability of detection of an individual at a certain distance from a camera trap); ƛ, expected encounter rate for any given individual whose only people who are permitted to enter the Park). home range centre is exactly at the camera-trap location; ѱ, predicted To investigate the spatial occurrence of people entering ratio of the number of animals actually present in the study areas compared the Park illegally, we used an occupancy modelling frame- with the maximum numbers set in the augmented data.  work approach. We aggregated human detections in each HPD, highest probability density. camera-trap station into -day detection/non-detection intervals, from which we constructed single species single sea- ( males,  females and  of unknown sex), with  captures son occupancy models that tested for associations between and  recaptures (Table ). The most frequently captured the presence of people and four landscape variables: study individual was a male that was recorded in  camera-trap area, elevation, distance to forest and distance to river stations in Renah Kayu Embun. Females were captured in (MacKenzie et al., ). We performed a Tukey’s honest fewer stations, with the highest capture count being of one significant difference test to determine whether the occur- female in five stations in Ipuh. We recorded no cubs rence of people was significantly different between study (Table ). areas (Tukey, ). Clouded leopard density estimates varied amongst study areas, with Bungo having the highest density at . indivi-    –  Results duals/ km (highest probability density . . ) and Ipuh the lowest at . (.–.; Table ). Comparing σ ± Clouded leopard detections and abundance the movement parameters ( SE) between study areas showed that individual animals in Sipurak moved just The  camera-trap stations generated a combined sam- over half (.%) as much those in Renah Kayu Embun, pling effort of , trap nights and captured  inde- and those in Ipuh ranged more widely than in the other pendent clouded leopard photographs, of which  were study areas. The Tukey honest significant difference test identified to an individual. There were  adult individuals showed significant differences between all paired density

TABLE 3 Single season occupancy models for trespassers across the four study areas, showing occupancy (ѱ ± SE), % confidence intervals (CI), detection probability (P), number of parameters (K), Akaike information criterion corrected for small sample size (AICc), difference in AICc between the model and the best-performing model (ΔAICc), likelihood of a model to be selected as the best model, and model weight.

Model Model No. Model1 ѱ ± SE 95% CI P K AICc ΔAICc likelihood weight 2.1 ѱ(site), P(.) 0.277 ± 0.008 0.141–0.470 0.123 5 492.60 0.00 1.00 0.37 2.2 ѱ(forest + river + elevation + site), P(.) 0.283 ± 0.006 0.141–0.479 0.122 8 493.10 0.51 0.78 0.29 2.3 ѱ(site + elevation), P(.) 0.277 ± 0.008 0.135–0.493 0.123 6 494.68 2.08 0.35 0.13 2.4 ѱ(river), P(.) 0.285 ± 0.005 0.162–0.435 0.121 3 496.71 4.12 0.13 0.05 2.5 ѱ(.), P(.) 0.275 ± 0.004 0.166–0.424 0.124 3 497.05 4.46 0.11 0.04 2.6 ѱ(river + elevation), P(.) 0.283 ± 0.006 0.152–0.456 0.122 4 497.49 4.90 0.09 0.03 2.7 ѱ(.), P(.) 0.273 ± 0.000 0.178–0.394 0.126 2 498.49 5.90 0.05 0.02 2.8 ѱ(site + river), P(.) 0.291 ± 0.010 0.098–0.555 0.134 9 498.76 6.16 0.05 0.02 2.9 ѱ(forest + river), P(.) 0.284 ± 0.005 0.150–0.460 0.126 4 498.76 6.16 0.05 0.02 2.10 ѱ(forest + elevation), P(.) 0.277 ± 0.004 0.155–0.450 0.124 4 498.90 6.31 0.04 0.02 2.11 ѱ(forest), P(.) 0.277 ± 0.002 0.166–0.426 0.125 3 499.51 6.92 0.03 0.01 2.12 ѱ(forest + river + elevation), P(.) 0.283 ± 0.006 0.141–0.479 0.122 5 499.56 6.97 0.03 0.01

 Model description: e.g. ѱ(river), P(.) indicates occupancy with associated covariates distance to river and detection probability constant. Covariates are: site, study area; forest, Euclidean distance to forest edge; elevation, altitude above sea level; river, Euclidean distance to river (including medium and major rivers, i. e. order – according to BAKOSURTANAL, Indonesia’s Coordinating Agency for Land Mapping).

estimates (Pr(.|z|) , .). The Geweke tests for the Renah Kayu Embun with . (...; Table ). The Markov chain Monte Carlo differed amongst study areas. In Tukey’s honest significant difference test found significant Ipuh, despite having a large number of iterations, the model differences in human disturbance between Ipuh and exceeded the tolerated Markov chain Monte Carlo range Bungo (P , .), Ipuh and Sipurak (P = .), and value, meaning the population parameters from this study Ipuh and Renah Kayu Embun (P , .), but not between area need to be interpreted with caution. Nonetheless, the Bungo and Sipurak (P = .). Bayesian P-value, which assesses model fit for each study area, was close to ., except for Sipurak (.), indicating that all models across all study areas were adequate Discussion (Gopalaswamy et al., ; Supplementary Table ). Here we present Sunda clouded leopard density estimates Anthropogenic pressure for the main habitat types in the Kerinci Seblat landscape, which advances the work conducted during – Camera traps recorded four independent photographs of (Sollmann et al., ) and adds to the knowledge on this national park rangers and field survey teams, and  of species. Our findings draw attention to the importance of other people. The latter were bird poachers (.%), tiger Kerinci Seblat National Park and its surrounding forests, and ungulate poachers (.%), collectors of non-timber which provide critical habitat for this threatened carnivore. forest products (.%) and fishers (.%; Supplementary The protection of the forest outside the National Park falls Table ). The highest number of camera stations recording under a different management authority and will therefore human presence was in Ipuh ( records, from  stations), require engaging other government stakeholders (Wibisono followed by Bungo (, ), Sipurak (, ) and Renah Kayu et al., ). Embun (, ). People carrying hunting rifles were photo- Our density estimates of the Sunda clouded leopard were graphed in Sipurak (n = ) and Ipuh (n = ). higher than those of the mainland clouded leopard Neofelis  Several covariates (study area, distance to forest edge and nebulosa in Bhutan (. adult individuals/ km ; Penjor elevation) predicted human presence in the forest and were et al., ), but similar to two estimates from Peninsular included in the top ranking models. We predicted higher oc- Malaysia (.–. and .–.; Mohamad et al., ),  currence of people in forests that were easier to access, i.e. and estimates from Sabah (.–./ km ; Hearn et al.,  those at lower elevations and closer to the forest edge, and ) and central Kalimantan (.–./ km ; Cheyne those in the Ipuh and Sipurak study areas. The highest prob- et al., ). Comparing our density estimates with the cor- ability of occupancy (ѱ) of trespassers was in Ipuh with . responding study areas surveyed by Sollmann et al. (), (highest probability density .–.), followed by Sipurak we found similarly high density estimates in Bungo and with . (.–.), Bungo with . (.–) and low density estimates in Ipuh. The results for Sipurak

were difficult to compare because of the low number of captures: Sollmann et al. () recorded two individual males and we recorded two males and one female. There were notable differences between our study design and that used by Sollmann et al. (), which determined Sunda clouded leopard densities using bycatch data from tiger surveys. Sollmann et al. () recorded a greater number of individual clouded leopards (n = ) from a lower sampling effort (, trap nights) over a larger area  (, km ), but had fewer independent photographs (n = ). We opted for a higher trapping intensity over a smaller area  (, trap nights,  km ) to increase the number of clouded leopard records overall (n = ), and captures of females in particular. We also had a shorter trapping period to ensure a demographically closed population. Nevertheless, both study designs had a low number of captured indivi- FIG. 3 Sunda clouded leopard densities across the Sunda region duals (Table ) and were subject to the male-biased sex in Sumatra and Borneo, with results from the four study areas of this study in black, from other studies in grey. Whiskers represent ratio typical for camera-trap studies of solitary carnivores   density estimation ranges with minimum and maximum values. (Tobler & Powell, ; Wearn et al., ). Considering Abbreviations on the x-axis: Hill, hill forest; Lo, lowland forest; these factors, we decided not to use the same parameters Lo-Hill, lowland to hill forest; Mon, montane and submontane as Sollmann et al. (), who categorized study areas into forest; Pr, primary forest; PS, peat swamp; SL, selectively logged. two primary forest and secondary forest. Instead, we performed analyses for each study area individually. Many felids including tigers, jaguars, leopards and Studies have shown that the size of the trapping area clouded leopards are solitary, with a social system character- affects sample size and parameter estimates, with a small ized by a dominant male protecting a territory that encom- trapping area potentially leading to underestimated Sunda passes the home ranges of – females (Sunquist & Sunquist, clouded leopard movements and consequently overestimat- ; Macdonald & Loveridge, ). Within these territor- ing density (Mohamad et al., ; Hearn et al., ). The ies and ranges, boundaries are demarcated through visual movement parameter values derived from Sipurak, Renah signs (e.g. scrapes), scent marks (especially urine) and voca- Kayu Embun and Bungo were consistent with those found lizations. Males tend to move across greater distances than in other studies. However, the value derived from the Ipuh females, probably resulting in higher detection rates and data set was large and probably a consequence of individual biased results when sex is not included as a covariate in clouded leopards being recorded by the outermost camera density models. Male-biased sex ratios are thus common traps, which potentially could have been avoided by design- in camera-trap studies of these species (Mohamad et al., ing a larger trapping area (Fig. ). ; Anile & Devillard, ). Poaching of felids does occur in Kerinci Seblat Nation- Interpreting camera-trap data thus requires caution, and al Park, but discussions with the Kerinci Seblat Tiger we limit comparisons of our results to those of other studies Protection and Conservation Units, which operate across with the same inherent sex bias. Future research should ex- all four study areas, indicated that clouded leopards are plore approaches that better detect females, which would not a target species for poachers. These Units confiscated also facilitate extrapolations to estimate population size at only one clouded leopard skin and one stuffed clouded leo- a landscape scale (Tobler & Powell, ), and should also pard during –, indicating that clouded leopard pro- consider the positioning of camera traps. Although we ducts are not in high demand in Kerinci Seblat (KS-TPCU, deployed many camera stations inside presumed female ). Nonetheless, the species is traded internationally and home ranges, setting cameras on ridge trails may have intro- there may be an increase in the range-wide illegal trade of duced a sex bias. Female clouded leopards in a Malaysian both live individuals and their body parts over the past Borneo study area tended to avoid these types of trails, pos- decades, particularly during – (D’Cruze & Macdonald, sibly to reduce infanticide by unknown adult males (Wearn ). et al., ). Setting cameras off trail would be logisti- Our study cannot conclusively prove the direct impact cally challenging in the rugged terrain of Kerinci Seblat of human disturbance on clouded leopard subpopulations National Park, but should be considered in future sampling because of the influence of other explanatory factors such designs. Future studies aiming to detect more females could as prey availability and topography of the landscape. also help determine whether males are at greater risk of fall- However, the clouded leopard density pattern is similar to ing victim to snare traps set along ridge trails. that found for tigers in the same study area  years prior

to our study (Linkie et al., ). Compared to Bungo and D’CRUZE,N.&MACDONALD, D.W. () Clouded in mystery: the Sipurak, Ipuh is more easily accessible, has a higher occur- global trade in clouded leopards. Biodiversity and Conservation,  – rence of people, has experienced higher forest conversion , . EFFORD, M.G. & FEWSTER, R.M. () Estimating population size by rates at its border and has lower levels of protection spatially explicit capture–recapture. Oikos, , –.  (Risdianto et al., ). This suggests an impact of anthro- GOPALASWAMY, A.M., ROYLE, J.A., HINES, J.E., SINGH, P., JATHANNA, pogenic disturbance. The lowland forests of Ipuh, which D., KUMAR, N.S. & KARANTH, K.U. () Program SPACECAP: should be rich in prey and therefore present ideal habitat software for estimating animal density using spatially explicit – for both tigers and clouded leopards, had lower values for capture recapture models. Methods in Ecology and Evolution, , –. both densities than the hill–submontane forests of Bungo GRASSMAN, L.I., TEWES, M.E., SILVY, N.J. & KITTI,K.() Ecology and Sipurak (Linkie et al., ). of three sympatric felids in a mixed evergreen forest in north-central Based on our findings, we recommend an island-wide Thailand. Journal of Mammalogy, , –. assessment of clouded leopard densities and populations HAIDIR, I.A., MATTHEW, L., YOAN,D.&MACDONALD, D.W. () that utilizes the large volumes of bycatch data available Asiatic golden cat and Sunda clouded leopard occupancy in the Kerinci Seblat landscape, west-central Sumatra. CatNews, , –. from tiger population surveys, as was recently done for HEARN, A., ROSS, J., MACDONALD, D., SAMEJIMA, H., HEYDON, M.,  Peninsular Malaysia (Tan et al., ). A range-wide assess- BERNARD, H. et al. (a) Predicted distribution of the bay cat ment could initiate a national dialogue on clouded leopard Catopuma badia (Mammalia: Carnivora: Felidae) on Borneo. population status and conservation needs across Sumatran The Raffles Bulletin of Zoology, , –. landscapes and Indonesian Borneo. It would also enable HEARN, A.J., ROSS, J., BERNARD, H., BAKAR, S.A., HUNTER, L.T.B. & MACDONALD, D.W. (b) The first estimates of marbled cat the clouded leopard to be considered by the Indonesian Pardofelis marmorata population density from Bornean primary Ministry of Environment and Forestry for Priority Species and selectively logged forest. PLOS ONE, ,e. status, thereby affording this Vulnerable felid greater con- HEARN, A.J., ROSS, J., BERNARD, H., BAKAR, S.A., GOOSSENS, B., servation attention and targeted management actions. HUNTER, L.T.B. & MACDONALD, D.W. () Responses of Sunda clouded leopard Neofelis diardi population density to anthropogenic Acknowledgements We thank Bambang Dahono Aji (Director of disturbance: refining estimates of its conservation status in Sabah. Biodiversity Conservation, Indonesia Ministry of Environment and Oryx, , –. Forestry) for supporting our work in Sumatra; Arief Toengkagie HEDGES, S., TYSON, M.J., SITOMPUL, A.F., KINNAIRD,M.F., (then Head of Kerinci Seblat National Park) and his staff for granting GUNARYADI,D.&ASLAN () Distribution, status, and us permission to conduct this research and use the park facilities; World conservation needs of Asian elephants (Elephas maximus)inLampung Animal Protection, Robertson Foundation, Rufford Foundation and Province, Sumatra, Indonesia. Biological Conservation, , –. Holly Reed (PDZA Conservation Fund) for funding; Panthera for pro- HENSCHEL, P., HUNTER, L.T.B., COAD, L., ABERNETHY, K.A. & viding camera-trap units; Debbie Martyr (Fauna & Flora International) MÜHLENBERG,M.() Leopard prey choice in the Congo Basin and the field team (Sabirudin, Kariyanto, Yosse Hendra, Ridwan and rainforest suggests exploitative competition with human bushmeat Redhi) for collecting and processing the field data; Muhammad Lubis, hunters. Journal of Zoology, , –. Mike Meredith, Wulan Pusparini, Arjun Gopalasswamy, Soumen Dey JĘDRZEJEWSKI, W., PUERTO, M.F., GOLDBERG, J.F., HEBBLEWHITE, and Jedediah Brodie for feedback on the manuscript. M., ABARCA, M., GAMARRA, G. et al. () Density and population structure of the jaguar (Panthera onca) in a protected area of Los Author contributions Study design, data collection and analysis, Llanos, Venezuela, from  year of camera trap monitoring. Mammal writing: IAH; conception and direction of the wider project of which Research, , –. this study is a part, supervision, writing: DWM; assistance with study KAWANISHI, K., SUNQUIST, M.E., EIZIRIK, E., LYNAM, A.J., design, data analysis, writing: ML. NGOPRASERT, D., WAN SHAHRUDDIN, W.N. et al. () Near fixation of melanism in leopards of the Malay Peninsula. Journal of Conflict of interest None. Zoology, , –. KS-TPCU (KERINCI SEBLAT TIGER PROTECTION AND Ethical standards This study abided by the Oryx guidelines on eth- CONSERVATION UNIT)() Kerinci Seblat Tiger Protection and ical standards and did not involve human subjects and/or any animal Conservation Unit Report Activities. Fauna & Flora International experiments or collection of specimens. Indonesia Programme, Jambi, Indonesia. KLHK (KEMENTERIAN LINGKUNGAN HIDUP DAN KEHUTANAN/ MINISTRY OF ENVIRONMENT AND FORESTRY)() Peta Penutupan Lahan Indonesia. Direktorat Inventarisasi dan References Pemantauan Sumber Daya Hutan, Direktorat Jenderal Planologi Kehutanan dan Tata Lingkungan, Jakarta, Indonesia. ANILE,S.&DEVILLARD,S.() Camera-trapping provides insights LINKIE, M., CHAPRON, G., MARTYR, D.J., HOLDEN,J.& into adult sex ratio variability in felids. Mammal Review, , –. LEADER-WILLIAMS,N.() Assessing the viability of tiger CARTER, N., JASNY, M., GURUNG,B.&LIU,J.() Impacts of people subpopulations in a fragmented landscape. Journal of Applied and tigers on leopard spatiotemporal activity patterns in a global Ecology, , –. biodiversity hotspot. Global Ecology and Conservation, , –. LINKIE, M., HAIDIR, I.A., NUGROHO,A.&DINATA,Y.() CHEYNE, S., DANIKA, D., LIMIN,S.&MACDONALD, D.W. () First Conserving tigers Panthera tigris in selectively logged Sumatran estimates of population ecology and threats to Sunda clouded forests. Biological Conservation, , –. leopards Neofelis diardi in a peat-swamp forest, Indonesia. MACDONALD,D.&LOVERIDGE,A.() The Biology and Endangered Species Research, , –. Conservation of Wild Felids. Oxford University Press, Oxford, UK.

MACDONALD, E.A., HINKS, A., WEISS, D.J., DICKMAN, A., BURNHAM, mark–resight, and spatial mark–resight models for estimating puma D., SANDOM, C.J. et al. () Identifying ambassador species for densities via camera traps. Journal of Mammalogy, , –. conservation marketing. Global Ecology and Conservation, RISDIANTO, D., MARTYR, D.J., NUGRAHA, R.T., HARIHAR, A., , –. WIBISONO, H.T., HAIDIR, I.A. et al. () Examining the shifting MACKENZIE, D.I., NICHOLS, J.D., LACHMAN, G.B., DROEGE, S., patterns of poaching from a long-term law enforcement ROYLE, J.A. & LANGTIMM, C.A. () Estimating site occupancy intervention in Sumatra. Biological Conservation, , –. rates when detection probabilities are less than one. Ecology, RUSTAM, R., HEARN, A., ROSS, J., ALFRED, R., SAMEJIMA, H., , –. HEYDON, M. et al. () Predicted distribution of the marbled cat MCCARTHY, J.L., WIBISONO, H.T., MCCARTHY, K.P., FULLER, T.K. & Pardofelis marmorata (Mammalia: Carnivora: Felidae) on Borneo. ANDAYANI,N.() Assessing the distribution and habitat use of The Raffles Bulletin of Zoology, , . four felid species in Bukit Barisan Selatan National Park, Sumatra, SOLLMANN, R., LINKIE, M., HAIDIR, I.A. & MACDONALD, D.W. () Indonesia. Global Ecology and Conservation, , –. Bringing clarity to the clouded leopard Neofelis diardi: first density MOHAMAD, S.W., RAYAN, D.M., CHRISTOPHER, W.C.T., HAMIRUL, estimates from Sumatra. Oryx, , –. M., MOHAMED, A., LAU, C.F. & SIWAN, E.S. () The first SUNARTO, S., KELLY, M.J., PARAKKASI,K.&HUTAJULU, M.B. () description of population density and habitat use of the mainland Cat coexistence in central Sumatra: ecological characteristics, spatial clouded leopard Neofelis nebulosa within a logged-primary forest in and temporal overlap, and implications for management. Journal of South East Asia. Population Ecology, , –. Zoology, , –. NIEDBALLA, J., SOLLMANN, R., COURTIOL,A.&WILTING,A.() SUNQUIST, M.E. & SUNQUIST,F.() Wild Cats of The World. The CamtrapR:anR package for efficient camera trap data management. University of Chicago Press, Chicago, USA. Methods in Ecology and Evolution, , –. TAN, C.K.W., ROCHA, D.G., CLEMENTS, G.R., BRENES-MORA, E., NOWAK, M.G., RIANTI, P., WICH, S.A., MEIJAARD,E.& HEDGES, L., KAWANISHI, K. et al. () Habitat use and predicted FREDRIKSSON,G.() Pongo tapanuliensis.InThe IUCN Red List range for the mainland clouded leopard Neofelis nebulosa in of Threatened Species . dx.doi.org/./IUCN.UK.-. Peninsular Malaysia. Biological Conservation, , –. RLTS.TA.en [accessed  June ]. TOBLER, M.W. & POWELL, G.V.N. () Estimating jaguar densities PENJOR, U., MACDONALD, D.W., WANGCHUK, S., TANDIN,T.&TAN, with camera traps: problems with current designs and recommendations C.K.W. () Identifying important conservation areas for the for future studies. Biological Conservation, , –. clouded leopard Neofelis nebulosa in a mountainous landscape: TUKEY, J.W. () Comparing individual means in the analysis of inference from spatial modeling techniques. Ecology and Evolution, variance. Biometrics, , –. , –. WEARN, O.R., ROWCLIFFE, J.M., CARBONE, C., BERNARD,H.& PUSPARINI, W., SIEVERT, P.R., FULLER, T.K., RANDHIR, T.O. & EWERS, R.M. () Assessing the status of wild felids in a highly- ANDAYANI,N.() Rhinos in the parks: an island-wide survey of disturbed commercial forest reserve in Borneo and the implications the last wild population of the Sumatran rhinoceros. PLOS ONE, for camera trap survey design. PLOS ONE, ,e. ,e. WIBISONO, H.T. & PUSPARINI,W.() Sumatran tiger (Panthera QGIS () QGIS Geographic Information System.OpenSource tigris sumatrae): a review of its conservation status. Integrative Geospatial Foundation Project. qgis.osgeo.org [accessed  June ]. Zoology, , –. RAYAN, D.M. & LINKIE,M.() Conserving tigers in Malaysia: a WIBISONO, H.T., WAHYUDI, H.A., WILIANTO, E., PINONDANG, I.M. science-driven approach for eliciting conservation policy change. R., PRIMAJATI, M., LISWANTO,D.&LINKIE,M.() Identifying Biological Conservation, , –. priority conservation landscapes and actions for the Critically RICH, L.N., KELLY, M.J., SOLLMANN, R., NOSS, A.J., MAFFEI, L., Endangered Javan leopard in Indonesia: conserving the last large ARISPE, R.L. et al. () Comparing capture–recapture, carnivore in Java Island. PLOS ONE, ,e.