Estimating leopard density across the highly modified human-dominated landscape of the Western Cape, South Africa
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
Estimating leopard density across the highly modified human-dominated landscape of the Western Cape, South Africa CAROLYN H. DEVENS, MATT W. HAYWARD, THULANI TSHABALALA, AMY DICKMAN J E A N N I N E S . M C M A N U S , B O O L S M U T S and M I C H A E L J . S O M E R S Abstract Apex predators play a critical role in maintaining Keywords Camera trapping, carnivore conservation, the health of ecosystems but are highly susceptible to habitat leopard, Panthera pardus, secr, SPACECAP, spatially degradation and loss caused by land-use changes, and to explicit capture–recapture anthropogenic mortality. The leopard Panthera pardus is Supplementary material for this article is available at the last free-roaming large carnivore in the Western https://doi.org/./S Cape province, South Africa. During –, we carried out a camera-trap survey across three regions covering c. , km of the Western Cape. Our survey comprised camera sites sampling nearly , camera-trap nights, Introduction resulting in the identification of individuals. We used two spatially explicit capture–recapture methods (R programmes secr and SPACECAP) to provide a comprehensive density analysis capable of incorporating environmental and an- T he exponential growth of the human population is threatening all levels of biodiversity, including large carnivores, with % of species’ populations experiencing thropogenic factors. Leopard density was estimated to be continuing declines (Estes et al., ; Ripple et al., ). . and . leopards/ km, using secr and SPACECAP, Large carnivores are particularly at risk of extinction respectively. Leopard population size was predicted to be because of their small population sizes, slow reproductive – individuals for our three study regions. With these rates, complex social structures and requirement for estimates and the predicted available leopard habitat for the large and contiguous habitats with sufficient prey (Cardillo province, we extrapolated that the Western Cape supports an et al., ; Ripple et al., ). These characteristics, and estimated – individuals. Providing a comprehensive their vulnerability to negative interactions with humans, baseline population density estimate is critical to understand- have driven declines of some of the most wide-ranging ing population dynamics across a mixed landscape and help- carnivores (Cardillo et al., ; Ray et al., ; ing to determine the most appropriate conservation actions. Swanepoel et al., ; Wolf & Ripple, ). Spatially explicit capture–recapture methods are unbiased Although the leopard is considered the most adaptable by edge effects and superior to traditional capture–mark– large carnivore (Ripple et al., ), range declines of –% recapture methods when estimating animal densities. We globally, –% in Africa and –% in southern therefore recommend further utilization of robust spatial Africa indicate that leopard populations are not as re- methods as they continue to be advanced. silient to anthropogenic influences as previously believed (Jacobson et al., ). Major anthropogenic threats to leopards include ongoing habitat loss and fragmentation CAROLYN H. DEVENS* (Corresponding author, orcid.org/0000-0002-7539- 0969), MATT W. HAYWARD† and MICHAEL J. SOMERS¶ ( orcid.org/0000-0002- (Harcourt et al., ; Crooks, ; Swanepoel et al., 5836-8823) Mammal Research Institute, Department of Zoology and ), depletion of prey resources (Woodroffe, ; Entomology, University of Pretoria, Pretoria, South Africa E-mail chdevens@gmail.com Karanth & Chellam, ), unsustainable hunting levels (Woodroffe, ; Harcourt et al., ) and direct perse- THULANI TSHABALALA‡, JEANNINE S. MCMANUS§ and BOOL SMUTS§ Research Department, Landmark Foundation, Riversdale, South Africa cution by people (Harcourt et al., ; Treves & Karanth, AMY DICKMAN WildCRU, Oxford University, Abingdon, UK ; Treves et al., ; Treves & Naughton-Treves, *Also at: Research Department, Landmark Foundation, Riversdale, South Africa ; McManus et al., ; Swanepoel et al., ). †Also at: School of Environmental and Life Sciences, University of Newcastle, Increasing human population density and loss of habitat Callaghan, Australia increase the likelihood of resource competition with people, ‡Also at: School of Agricultural, Earth and Environmental Sciences, University of KwaZulu-Natal, Durban, South Africa often resulting in human–carnivore conflict (Woodroffe, §Also at: Department of Biodiversity and Conservation Biology, University of ; Cardillo et al., ). Persecution often includes the Western Cape, Cape Town, South Africa indiscriminate use of lethal methods to manage livestock ¶Also at: Centre for Invasion Biology, University of Pretoria, Pretoria, South Africa depredation by carnivores (e.g. snares, poisoned carcasses, Received December . Revision requested March . gin traps (leg-hold traps), gun traps, live trapping) and tar- Accepted November . First published online September . geted (often retaliatory) hunting (McManus et al., ). 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, Downloaded from https://www.cambridge.org/core. distribution, IP address: and reproduction in any medium, 46.4.80.155, provided the originalonwork 22 Jan 2021 at cited. is properly 15:24:38, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001473 Oryx, 2021, 55(1), 34–45 © The Author(s), 2019. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605318001473
Leopard density in South Africa’s Western Cape 35 Estimating a species’ density across various types of land Fewster, ), spatially explicit capture–recapture models cover (i.e. habitat and vegetation type) and land uses (i.e. are becoming increasingly robust and comprehensive. residential/urban land, cultivated land, commercial and These statistical and methodological advances provide recreational land and areas protected for conservation) multiple options that can be applied to specific study ques- can help determine how population numbers are affected tions while making population density estimates increasing- by landscape features. Density estimates are not equally ly reliable. Inaccurate density estimates can lead to biased robust, and under- or overestimating populations can have population estimates, with serious implications for conser- substantial implications for conservation management and vation management (Soisalo & Cavalcanti, ). policy (Foster & Harmsen, ; Hayward et al., ). For The estimation of a baseline population density for example, Soisalo & Cavalcanti () demonstrated how leopards in South Africa’s Western Cape province is overestimating jaguar Panthera onca populations by five fundamental for understanding how this regionally im- individuals per km inflated the overall population portant population responds to landscape-scale threats estimate by , individuals across their , km and changes. By estimating densities across landscapes of study region. Density estimation also depends upon data varying resource availability and threats, we can examine quality, with a large enough sample size and capture prob- drivers of regional density variation and improve conserva- ability for the chosen analysis method (Foster & Harmsen, tion management for disjunct populations. ). Conservationists and ecologists constantly seek to im- prove the methodology for estimating animal population Study area abundances and densities (Griffiths & van Schaik, ; This study covers c. , km in three areas (Langeberg, Karanth & Nichols, ; Karanth & Nichols, ). The Overberg and Garden Route) in the Western Cape, South use of camera traps and photo capture–recapture analysis Africa (Fig. ). The topography varies from the Cape Fold is a common and effective non-invasive practice for ob- Mountain peaks with an altitude of . , m that extend taining data on wildlife population dynamics, particularly , km east to west, to coastal and low-lying valleys of rare or elusive species (Foster & Harmsen, ). Leo- at , m altitude (Thamm & Johnson, ). Biomes pards, like many other large felids, are challenging to included in our study are Thicket, Afro-temperate forest monitor because of their large home ranges, low population (Forest), Sandstone fynbos (Fynbos), Nama-Karoo, Succu- density and primarily solitary and elusive nature (Karanth & lent-Karoo and Savanna (Mucina & Rutherford, ). Nichols, ; Treves & Karanth, ). Global population In the Langeberg we deployed camera traps in the estimates across the leopard’s vast geographical distribution greater Riversdale/Heidelberg area on the southern slopes do not account for the health and sustainability of smaller, of Langeberg Mountain Range, in the greater Greyton area isolated regional metapopulations across a variety of habitat on the southern slope of Riviersonderend Mountain Range types, countries and levels of human landscape modification and in the Robertson Wine Valley (Breede River Valley) and pressure. situated between the Langeberg and Riviersonderend Camera-trap surveys have become an important data Mountain Ranges. In the Overberg we surveyed the greater collection method for population and density studies Hermanus area to the west, the greater Cape Agulhas and because they are non-invasive, practical and affordable Arniston areas to the south along the coast, and the greater (Karanth, ; Karanth & Nichols, ; Foster & De Hoop Nature Reserve area to the eastern extent of the Harmsen, ). The capture–recapture method relies on surveyed region. Along the Garden Route we surveyed individuals being identifiable (Karanth, ; Silver et al., temperate forest along the southern slopes of the Outeniqua ) and has been the predominant approach used in and Tsitsikamma Mountains from George in the west to felid density studies. the Bloukrans River in Plettenberg Bay in the east. More recently, spatial capture–recapture or spatially explicit capture–recapture methods have become popular because they provide comprehensive analyses that can in- Methods corporate environmental and anthropogenic factors when estimating animal densities. These methods enable density Camera-trap surveys analyses to include spatio-temporal data from capture histories, providing direct estimates of population density We undertook seven large-scale camera-trap surveys during that remain unbiased by edge effects (Chase Grey et al., June –March , focusing on likely presence of leo- ). By allowing for flexibility in individual heterogeneity pards inside and outside protected areas and across different with the consideration of capture probability relative to trap agricultural land-use zones (livestock, crops, forestry). We location, spatial covariates such as habitat, and intrinsic fac- used Cuddeback Attack IR (Cuddeback, Green Bay, USA) tors such as sex and age (Foster & Harmsen, ; Efford & digital infrared cameras and selected camera-trap locations Oryx, 2021, 55(1), 34–45 © The Author(s), 2019. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605318001473 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 22 Jan 2021 at 15:24:38, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001473
36 C. H. Devens et al. FIG. 1 (a) Location of the study areas in the Western Cape province, South Africa. (b) Camera-trap surveys conducted across the Langeberg (, km), Garden Route (, km) and Overberg (, km) areas. Data from camera stations with identified leopards were analysed with programmes SPACECAP and secr with various buffers. based on the highest likelihood of leopard activity as deter- density estimates than non-spatial methods (Obbard et al., mined by physical evidence (scat, spoor and territorial scent ; Gerber et al., ; Gopalaswamy et al., ; Noss and scratch markings on trees), as well as habitat type and et al., ; Braczkowski et al., ). We calculated density topography (Karanth & Nichols, ). At each camera- estimates using two spatially explicit capture–recapture trap station, we positioned two cameras to capture both methods within the programming environment R .. flanks of a passing leopard. The stations were placed – (R Development Core Team, ): () the maximum km apart to achieve even coverage of the sampling area likelihood based estimator programme secr .. (Efford and camera stations remained active for a minimum of et al., ; Efford, , ), which is a more robust months to ensure maximum likelihood of leopard activity version of programme DENSITY (Efford, ), and () the being captured without violating the closed population as- Bayesian estimator programme SPACECAP .. (Gopalaswamy sumption (Karanth & Nichols, ; Devens et al., ). et al., ). Previous studies have applied these two pro- grammes to compare density estimates (Kalle et al., ; Thapa et al., ) and to compare results of spatially explicit Capture–recapture identification capture–recapture with non-spatial methods (Noss et al., ; Braczkowski et al., ). We used these programmes Individual leopards can be identified from clear photo- for comparison of two spatially explicit capture–recapture graphs of both flanks by their unique rosette markings. methods and to determine the most robust and inclusive Identification from single flank photos is possible, but density estimate range for each study region. needs to be based upon the observation of characteristics For the analysis with secr we categorized camera traps as such as the animal’s overall size, neck girth, injuries or count detectors, which allows repeat detections. Count data scars. Although such characteristics may be useful, incor- can result from devices such as automatic camera traps. rectly identified individuals could bias density estimates, Count detectors record the presence of an animal at a trap resulting in overestimation of the population if flank photos location without restricting movement and allow . detec- of the same animal were erroneously assigned to two indi- tion of an individual at a particular site on any occasion. The viduals. We therefore only utilized double flank capture secr.fit function was run for each regional survey phase events for identification. using models of time (g*T) and behavioural response (g*b), as well as buffers of , , , and km Data analysis surrounding the minimal convex polygon around camera stations in each camera-trapping area. These buffers Spatially explicit capture–recapture methods for density ensured inclusion of all leopard home ranges within reach analyses are more comprehensive and reliable than tra- of camera traps (Kalle et al., ) and made density estima- ditional capture–recapture analyses (Borchers & Efford, tion more reliable by determining the point at which the ; Kalle et al., ; Gopalaswamy et al., ; Chase density estimate stabilized (Kalle et al., ; Chase Grey Grey et al., ; Thapa et al., ) and produce lower et al., ). Oryx, 2021, 55(1), 34–45 © The Author(s), 2019. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605318001473 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 22 Jan 2021 at 15:24:38, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001473
Leopard density in South Africa’s Western Cape 37 SPACECAP was used to estimate abundance and density ‘Spatial Capture–Recapture’ option runs a spatially explicit using spatially-explicit capture–recapture models to derive capture–recapture analysis. The Markov-Chain Monte spatial Bayesian estimates with trap response. A grid of Carlo settings varied between study areas and buffers. equally spaced points km apart was generated in QGIS Markov-Chain Monte Carlo iterations were set between . (QGIS Development Team, ) and clipped to the sur- , and , with a burn-in period between , veyed area containing the camera trap array combined with and , iterations and a thinning rate of . The data aug- an extended surrounding area, known as the state-space, at mentation numbers were c. – times the number of ani- distances of , , , and km. These points represent mals identified in each regional survey and varied between all potential home range centres of all leopards within the and ,. We assessed chain convergence with the survey. The potential home range centres file included the Geweke diagnostic test produced within the SPACECAP out- geographical coordinates and habitat suitability of each of put in the form of z-score values. Z-scores between −. and these points within the state-space. We determined habitat +. implied adequate convergence and confirmed that the suitability using Maxent .. (Phillips et al., ; Phillips Markov-Chain Monte Carlo analysis was run with a suffi- et al., ) model output comprising environmental vari- ciently long burn-in period. The SPACECAP output also pro- ables, including eight WorldClim bioclimatic variables duces a Bayesian P-value to provide additional assessment of obtained from WorldClim website (Hijmans et al., ), the model fit where P-values close to or imply that the human footprint index (WCS & CIESIN, ), altitude, an- model is inadequate. The adequacy of the data augmentation thropogenic biomes (Ellis & Ramankutty, ), Globcover number can be checked in the ‘density plot for psi’ and (FAO, ), South African National Bio-diversity ‘density plot for N’ files included within the output files. Institute ecosystem status of vegetation types (Rouget All densities obtained with SPACECAP produced z-scores et al., ), and a subset of location data obtained from that achieved convergence, as well as sufficient model fit two leopards resident in the area that were equipped with and data augmentation number. The output also included GPS collars. We used the Natural Breaks function (Jenks, pixel-specific density estimates (animals per km), which ) in ArcMap .. to code the model output as either we used to create a pixel density map of the study areas (not suitable = –.) or (suitable = .–.). and compare leopard densities across various land covers The habitat suitability generated in this way (Jenks and uses to illustrate relationship with anthropogenic factors. method) was recorded for each point and a home range cen- tre input file was generated for each area’s buffer distances (Fig. ). Results We ran SPACECAP with a km pixel area, and set the model definitions to ‘Trap response present’, ‘Spatial Camera-trap data and sampling effort Capture–Recapture’, ‘half normal’ detection function and the capture encounters ‘Bernoulli’s process’. The ‘Trap The total sampling effort for the Overberg (November – response present’ option implements a ‘trap-specific’ behav- March ) was , camera-trap nights across a total ioural response in which the probability of capture at a spe- of camera-trap locations ( cameras). This yielded cific trap increases (or decreases) after the initial capture. The leopard photographs (captures), with eight individuals FIG. 2 Maxent probability distribution model of leopard habitat suitability in the Western Cape and considering this study’s km buffers around camera-trap areas. Distribution model is reclassified with Natural Breaks function. Oryx, 2021, 55(1), 34–45 © The Author(s), 2019. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605318001473 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 22 Jan 2021 at 15:24:38, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001473
38 C. H. Devens et al. identified in of them. These individuals were detected at Identified leopards nine of the camera-trap sites (Table ). TABLE 1 Summary of capture–recapture camera-trap survey sampling effort and leopard Panthera pardus capture results across three study areas in the Western Cape, South Africa. The total sampling effort for the two phases of the 8 21 42 24 71 Langeberg survey (April –December ) consisted of , camera-trap nights across a total of camera-trap Total leopard pictures locations ( cameras). This yielded leopard captures, from which individual leopards were identified in enabling leopard photographs, and these individuals were detected at of identification the camera-trap sites (Table ). The total sampling effort for the three phases of the 40 86 250 125 376 Garden Route survey area (May –December ) was , camera-trap nights across a total of camera-trap locations ( cameras). This yielded leopard captures, Total leopard of which individual leopards were identified in photo- pictures graphs, and these individuals were detected at of the 118 142 454 238 714 camera-trap sites (Table ). The total sampling effort was , camera-trap nights across camera-trap locations ( cameras), with leopard captures and identified Total camera- individuals (Table ). trap nights 2,880 3,600 7,110 4,530 13,590 Density estimates The spatially explicit capture–recapture density estimates Camera-trap stations varied by region and between regional phases, and estimates with leopard IDs from secr were lower than those from SPACECAP. The effect of using various buffers within the two programmes, par- ticularly SPACECAP, demonstrated the sensitivity to buffer width and data augmentation size (Kalle et al., ). We cal- 9 33 58 33 100 culated mean density estimates from stabilized buffer values to ensure the study area was large enough to avoid capturing Camera-trap any individuals residing outside the buffered region during stations the survey. In the Overberg, secr density estimates stabilized at 32 40 79 42 151 . leopards/ km (CI .–.). Both phases in the Langeberg had density estimates that were stable across all Regional phases five buffers with a phase one density estimate of . leo- pards/ km (CI .–.) and a phase two estimate of 1 3 2 6 . leopards/ km (CI .–.). The Garden Route’s first phase had an estimated density of . leopards/ km (active nights) Survey phase (CI .–.) with densities stable across all buffers, whereas duration phase two had an estimated density of . leopards/ km (CI .–.) and phase three produced a density estimate of 90 90 90 90 270 . leopards/ km (CI .–.; Table ). We calculated Oct. 2012–Mar. 2015 July 2011–Mar. 2015 Apr. 2012–Jan. 2013 the mean density for multi-phase study areas resulting in July 2011–Sep. 2012 . leopards/ km in the Overberg, compared to . leopards/ km (CI .–.) in the Langeberg and Survey period . leopards/ km (CI .–.) along the Garden Route. The highest estimated density was Langeberg’s phase two with . leopards/ km, and the lowest was . leopards/ km in the Overberg (Table ). Garden Route SPACECAP produced an Overberg density estimate of Study area Langeberg . leopards/ km (CI .–.), Langeberg phase one Overberg and two density estimates of . (CI .–.) and . (CI Mean Total .–.) leopards/ km, respectively, and Garden Oryx, 2021, 55(1), 34–45 © The Author(s), 2019. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605318001473 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 22 Jan 2021 at 15:24:38, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001473
https://doi.org/10.1017/S0030605318001473 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 22 Jan 2021 at 15:24:38, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. Oryx, 2021, 55(1), 34–45 © The Author(s), 2019. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605318001473 TABLE 2 Density estimates from programmes secr and SPACECAP, with standard error (SE), standard deviation (SD), % confidence intervals (CI), range of buffers that achieved mean density estimate stabilization, area of regional km buffer, number of leopards estimated within the surveyed area, and the Bayesian P-value for model fit. Density estimate Buffer range of means’ (leopards/100 km2) stabilization (km) Estimated no. of leopards P-value secr SPACECAP secr SPACECAP mean ± SE (95% CI) mean ± SD (95% CI) secr SPACECAP 35 km buffer area (km2) (95% CI) (95% CI) SPACECAP Langeberg Phase 1 0.29 ± 0.05 (0.20–0.41) 1.67 ± 0.26 (1.21–2.18) 15–35 15–30 0.86 Phase 2 0.70 ± 0.15 (0.57–1.76) 2.11 ± 0.35 (1.46–2.82) 15–35 25–35 0.55 Area mean 0.50 ± 0.10 (0.39–1.09) 1.89 ± 0.30 (0.89–2.50) 19,063.42 93.41 360.30 0.71 (74.35–205.88) (169.70–476.60) Garden Route Phase 1 0.50 ± 0.26 (0.19–1.32) 1.44 ± 0.58 (0.55–2.54) 15–35 20–30 0.47 Phase 2 0.34 ± 0.11 (0.18–0.63) 0.92 ± 0.16 (0.65–1.22) 25–35 20–35 0.73 Phase 3 0.29 ± 0.13 (0.13–0.67) 0.51 ± 0.10 (0.36–0.70) 20–35 15–35 0.60 Area mean 0.38 ± 0.17 (0.17–0.87) 0.96 ± 0.28 (0.52–1.49) 6,680.34 25.39 64.13 0.60 (11.36–58.12) (34.74–99.54) Overberg Leopard density in South Africa’s Western Cape Phase 1 0.17 ± 0.10 (0.06–0.48) 0.69 ± 0.30 (0.39–1.28) 30–35 25–35 7,910.04 13.45 54.58 0.63 (4.75–37.97) (30.85–101.25) Overall mean 0.35 ± 0.12 (0.21–0.81) 1.18 ± 0.29 (0.60–1.76) 11,217.93 44.08 159.67 0.65 (30.15–100.66) (78.42–225.79) Total area without overlap1 29,258.43 132.25 479.01 (90.46–301.97) (235.25–677.38) The area total is without km buffer land overlap between survey areas. 39
40 C. H. Devens et al. Route phase one, two and three of . leopards/ km (CI Analysis with secr and SPACECAP resulted in an .–.), . leopards/ km (CI .–.) and . leo- overall estimated leopard density of . leopards/ km pards/ km (CI .–.), respectively. Again, we calcu- (CI .–.) and . leopards/ km (CI .–.) re- lated the mean density for multi-phase areas; the Overberg spectively. The output from SPACECAP includes a pixel was . leopards/ km, compared to . leopards/ density file, which we converted into a fine-scale map km (CI .–.) in the Langeberg and . leopards/ using QGIS, showing the variation of estimated animal km (CI .–.) along the Garden Route (Table ). densities across each of the potential home range centres FIG. 3 Pixelated ( km) SPACECAP leopard density maps showing the (a) Overberg, (b) Langeberg and (c) Garden Route study areas. Camera-trap sites shown are sites with individually identified leopards. Oryx, 2021, 55(1), 34–45 © The Author(s), 2019. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605318001473 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 22 Jan 2021 at 15:24:38, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001473
Leopard density in South Africa’s Western Cape 41 estimate of leopards (CI .–.) in the total study area (Table ). With the regional SPACECAP mean density estimates there would be c. leopards (CI .–.) in the Garden Route, leopards (CI .–.) in the Overberg and leopards (CI .–.) in the Langeberg (Table ), yield- ing a total estimate of leopards (CI .–.; Table ). Comparatively, using the total area of all three regions’ km buffers (without overlap) and the overall SPACECAP mean density provides a population estimate of leopards (CI .–.) for the entire study area (Table ). Our study area of ,. km comprises % of the Western Cape’s total area (, km). To provide a population outlook at the provincial level we extrapolated an ecologically useful Western Cape abundance estimate using our secr and SPACECAP mean density estimates and Swanepoel et al.’s () estimated , km of remaining suitable leopard habitat in Western Cape (% of the province). This suggests that the entire Western Cape could harbour as few as (CI .–.) and as FIG. 4 Sum of SPACECAP leopard pixel density estimates many as (CI .–.) leopards (Table ). (leopards/km) for different land-cover types in the Western Cape study areas. ‘Agriculture’ includes cultivated commercial fields, orchards and plantations, ‘urban’ includes residential and Discussion urban commercial land, and ‘other’ includes dams, roads and railways. This study covered c. , km and is one of the most extensive leopard camera-trap density estimate surveys con- ducted in the Western Cape province of South Africa. We (Fig. ). Using these pixel density values, we also created compared the use of two spatially explicit capture–recapture study area graphs depicting the sum of pixel densities across methods for a regionally imperilled disjunct leopard popu- land cover categories (CapeNature, ) and protected lation. Our comprehensive density analysis investigated areas (Department of Environmental Affairs, ; Fig. ). leopard persistence in a predominately human-modified and privately-owned landscape with varying degrees of Estimated population numbers conflict and persecution. It is important to reiterate that our study area incorpo- Combining this study’s total area with each region’s rates variation across vegetation types, landscape topography km buffer width (Garden Route ,. km; Overberg and degree of landscape modification and fragmentation. ,. km; Langeberg ,. km) with the regional Because of its highly cultivated agricultural landscape secr mean density estimates results in an estimate of leo- (mainly grain production, as well as livestock farming), the pards (CI .–.) in the Garden Route, leopards (CI Overberg is commonly considered as the breadbasket of the .–.) in the Overberg and leopards (CI .–.) Cape. The Langeberg’s Breede River Valley is encircled by in the Langeberg (Table ). The total estimate for all areas the Cape Fold Mountain ranges and is dominated by combined was leopards (CI .–.; Table ). In fynbos, vineyards and orchards, whereas the Garden Route comparison, combining the total non-overlapping area is a long stretch of the south-western coast situated between of all three study area’ km buffers (,. km) with mountains to the north and the Indian Ocean to the south, the overall secr mean density produces a population which harbours a unique mixture of fynbos, indigenous TABLE 3 Comparison of estimated population size of leopards using the total area within this study’s km buffer distance (without regional survey overlap) and Swanepoel et al.’s () estimate for suitable leopard habitat in the Western Cape. Area secr (0.35 leopards/100 km2) SPACECAP (1.18 leopards/100 km2) Total buffered area of this study (29,258.43 km2) 102.4 (95% CI 61.4–237.0) 345.3 (95% CI 175.6–515.0) Suitable leopard habitat in the Western Cape (49,850 km2; 174.5 (95% CI 104.7–403.8) 588.2 (95% CI 299.1–877.4) Swanepoel et al., 2013) Oryx, 2021, 55(1), 34–45 © The Author(s), 2019. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605318001473 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 22 Jan 2021 at 15:24:38, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001473
42 C. H. Devens et al. predominantly non-conflict crop cultivation (vineyard and orchard) in a valley surrounded by natural mountain vege- tation. Additionally, the majority (%) of the estimated leopard pixel density on agricultural land across all study areas occurs in cultivated commercial fields and % occurs in forestry plantations, which can generally be considered non-conflict agriculture. All three areas demonstrate a discrepancy between suit- able habitat and land designated as protected for the conser- vation and sustainability of biodiversity (Figs & ). The vast majority of each area’s estimated leopard pixel density occurs on non-protected land with the highest percentage occurring in the Overberg (%) (Fig. ; Supplementary Table ). Our secr and SPACECAP estimates are some of the lowest national density estimates for leopards and are comparable to three other studies in the Western Cape (Martins, ; Mann, ; Devens et al., ; Table ). The difference be- tween the estimates from the two programmes was greater than expected, which could be attributed partially to the FIG. 5 Sum of SPACECAP leopard pixel density estimates extra Maxent habitat mask covariate modelling incorpo- (leopards/km) for suitable leopard habitat within protected and rated into the SPACECAP analyses. The likelihood method non-protected areas for each study area in the Western Cape. requires substantially less computation time than the Bayesian approach (seconds or minutes vs hours or days), temperate forest and forestry plantations. The agricultural is less sensitive to buffer width and data augmentation size land in all three areas is utilized by leopards, as evidenced and has greater convenience and versatility for customiza- by capture and recapture locations and suitable habitat tion with covariates and models. SPACECAP entails checks extending beyond natural vegetation (Fig. ) and protected to verify that convergence is achieved, model fit is sufficient, area boundaries (Fig. ). None of our identified territorial and data augmentation is adequate. Hence, it is more adult leopards remained strictly within protected areas, appropriate and robust for small sample sizes. Our mean and most did not utilize any protected land within their SPACECAP density estimate of . leopards/ km is home range. Although protected areas play a crucial role directly comparable to results from Devens et al. (), in the conservation of natural landscapes, they do not who reported mean density estimates of . and .–. encompass the entirety of remaining natural vegetation or leopards/ km for SPACECAP and two GPS methods, existing leopard habitat. In the Western Cape % of conser- respectively (Table ). The GPS methods used data from vation areas contain suitable leopard habitat but only % of collared leopards and incorporated home range size leopard habitat occurs within conservation areas (Swanepoel (home range density estimate) and home range overlap of et al., ). same-sex neighbouring leopards (socially considerate dens- These findings, together with estimated leopard densities ity estimate). Therefore, we suggest our SPACECAP results within highly modified, cultivated and non-protected land are more accurate and reliable for determining the spatial (Figs & ), suggest that non-protected, mostly privately requirements of species. We recommend spatially explicit owned land plays an important role in sustaining the capture–recapture methods for future research, with the Western Cape leopard population. Both spatially explicit specific incorporation of GPS collar data, because these capture–recapture methods suggest that the Langeberg methods are the most robust at capturing a species’ spatial winelands region supports the highest leopard density and ecology within a population. the Overberg’s agricultural landscape the lowest. The sum We extrapolated an ecological density (number of indivi- of each study area’s pixel densities is consistent with these duals per useable area) using our density estimates and a findings (Fig. ). Although densities estimates vary between prediction of , km suitable leopard habitat remaining study areas, the composition of land-cover and protected in the Western Cape (Swanepoel et al., ). Our findings land utilized within each area is comparatively consistent suggest that there are – leopards remaining (Table ). (Supplementary Tables & ). The Langeberg’s leopard However, this may be an optimistic estimation. Habitat pixel densities on agricultural land are higher than in the modelling is not infallible and identified suitable habitat is other two study areas, and equal to the Garden Route’s not necessarily useable for wide-ranging species such as the natural vegetation (Fig. ). This can be attributed to the leopard. The available habitat estimate included fragmented Oryx, 2021, 55(1), 34–45 © The Author(s), 2019. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605318001473 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 22 Jan 2021 at 15:24:38, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001473
Leopard density in South Africa’s Western Cape 43 TABLE 4 Published South African leopard population density estimates for data collected after , with the analysis programme used. Region Source Density estimate (leopards/100 km2) Programme1 Various (Western Cape) This study 0.17–0.50 (mean 0.35) secr 0.69–1.89 (mean 1.18) SPACECAP Various (Western Cape, Eastern Cape) Devens et al. (2018) 0.24–1.89 (mean 0.95) SPACECAP 0.90 HRDE 1.11 SCDE Little Karoo (Western Cape) Mann (2014) 0.50 CAPTURE 1.18 DENSITY Cederberg Mountains (Western Cape) Martins (2010) 1.80–2.30 CAPTURE Phinda-Mkhuze Complex (Kwazulu-Natal) Balme et al. (2010) 2.49–11.11 CAPTURE Zululand Rhino Reserve (Kwazulu-Natal) Chapman & Balme (2010) 2.50–7.00 CAPTURE Phinda Private Game Reserve (Kwazulu-Natal) Braczkowski et al. (2016) 3.40 secr 3.65 SPACECAP 7.28–9.28 CAPTURE Waterberg Mountains (Limpopo) Swanepoel et al. (2015) 4.56–6.59 secr Phinda Private Game Reserve (Kwazulu-Natal) Balme et al. (2009a) 6.97 CAPTURE Phinda Private Game Reserve (Kwazulu-Natal) Balme et al. (2009b) 7.17–11.21 CAPTURE Soutpansberg Mountains (Limpopo) Chase Grey et al. (2013) 10.70 SPACECAP N’wanetsi Concession (Kruger National Park) Maputla et al. (2013) 12.70 CAPTURE HRDE, home range density estimate; SCDE, socially considerate density estimate. habitat, small isolated pockets of habitat and areas of habitat Iris Englund Foundation, National Lotteries Distribution Trust subject to edge effects and anthropogenic pressures. These Fund, Mones Michaels Trust, Arne Hanson and the Deutsche Bank South Africa Foundation for assisting in funding this research. MJS factors can lead to habitat areas being unable to accommo- was supported by the National Research Foundation. We acknowledge date viable populations (Woodroffe & Ginsberg, ). In Landmark Foundation for providing the resources to enable this addition, our maximum Western Cape population estimate research, and thank private landowners and CapeNature for their of individuals is well below the minimum viable popu- cooperation and assistance. lation size necessary to maintain genetic diversity (Traill Author contributions Study conception: CHD, BS, JM; method- et al., ). The genetic population structure of leopards ology design, data collection and writing: CHD; data analysis: CHD, in the Western Cape and Eastern Cape provinces indicates TT; revisions: MS, MH, AD, TT, BS. very low to moderate gene flow between the three subpopu- lations (McManus et al., ). Conflicts of interest None. Although highly adaptable, the leopard is a widely per- secuted species that experiences varying levels of anthro- Ethical standards All authors have abided by the Oryx guidelines on ethical standards, and fieldwork was conducted with the necessary pogenic threats and habitat loss. Our results suggest that approvals and permits from appropriate institutions and statutory protected areas are inadequate to secure the long-term con- authorities. Cape Nature Research Permit to collect fauna specimens servation of leopards in the Western Cape. By establishing for scientific research in the Western Cape was granted to CHD in density and population size estimates in an increasingly August 2014 (permit no.: AAA007-00130-0056) and prior camera- fragmented and modified landscape, we increase the under- trap data was covered under a Cape Nature Permit for JM. These per- mits were granted for the purposes of collaring leopards. CHD was also standing of how leopards can persist in human-dominated granted an Animal Ethics Committee Approval Certificate from the areas, influencing conservation planning for the species. For University of Pretoria in February 2014–December 2016 (project num- adaptive and wide-ranging species such as large carnivores, ber: EC005-14). We did not collect specimens for this study, and all non-protected and human-dominated areas are becoming fieldwork was conducted ethically with the cooperation of local conser- increasingly important for genetic dispersal and land- vation authorities and landowners. scape connectivity (Boron et al., ). The threats and con- servation conflicts affecting the leopard in South Africa’s Cape region are affecting all apex carnivores globally. References Accurate density estimates are critically important as B A L M E , G.A., H U N T E R , L.T. & S LO TO W , R. (a) Evaluating numerous anthropogenic interests continue to threaten methods for counting cryptic carnivores. Journal of Wildlife leopards, their resources and habitat. Management, , –. B A L M E , G.A., S LO T O W , R. & H U N T E R , L.T. (b) Impact of Acknowledgements We thank the ABAX Foundation, conservation interventions on the dynamics and persistence Development Bank South Africa, Green Fund, United Nations of a persecuted leopard (Panthera pardus) population. Biological Environmental Program, Global Environmental Facility, Henry and Conservation, , –. Oryx, 2021, 55(1), 34–45 © The Author(s), 2019. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605318001473 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 22 Jan 2021 at 15:24:38, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001473
44 C. H. Devens et al. B A L M E , G.A., S LO T OW , R. & H U N T E R , L.T.B. () Edge effects F O S T E R , R.J. & H A R M S E N , B.J. () A critique of density estimation and the impact of non-protected areas in carnivore conservation: from camera-trap data. The Journal of Wildlife Management, , leopards in the Phinda-Mkhuze Complex, South Africa. Animal –. Conservation, , –. G E R B E R , B.D., K A R P A N T Y , S.M. & K E L LY , M.J. () Evaluating the B O R C H E R S , D.L. & E F F O R D , M.G. () Spatially explicit maximum potential biases in carnivore capture–recapture studies associated likelihood methods for capture–recapture studies. Biometrics, , with the use of lure and varying density estimation techniques using –. photographic-sampling data of the Malagasy civet. Population B O R O N , V., T Z A N O P O U LO S , J., G A L LO , J., B A R R A G A N , J., J A I M E S - Ecology, , –. R O D R I G U E Z , L., S C H A L L E R , G. & P A Y Á N , E. () Jaguar densities G O P A L A S WA M Y , A.M., R OY L E , J.A., H I N E S , J.E., S I N G H , P., J AT H A N N A , across human-dominated landscapes in Colombia: the contribution D., K U M A R , N.S. & K A R A N T H , K.U. () Program SPACECAP: of unprotected areas to long term conservation. PLOS ONE, , software for estimating animal density using spatially explicit e. capture–recapture models. Methods in Ecology and Evolution, B R AC Z KO W S K I , A.R., B A L M E , G.A., D I C K M A N , A., F AT T E B E R T , J., , –. J O H N S O N , P., D I C K E R S O N , T. et al. () Scent lure effect on G R I F F I T H S , M. & VA N S C H A I K , C.P. () The impact of human traffic camera-trap based leopard density estimates. PLOS ONE, , on the abundance and activity periods of Sumatran rain forest e. wildlife. Conservation Biology, , –. C A R D I L LO , M., P U R V I S , A., S E C H R E S T , W., G I T T L E M A N , J.L., B I E L B Y , J. H A R C O U R T , A., P A R K S , S. & W O O D R O F F E , R. () Human & M AC E , G.M. () Human population density and extinction density as an influence on species/area relationships: double risk in the world’s carnivores. PLOS Biology, , e. jeopardy for small African reserves? Biodiversity & Conservation, C A P E N AT U R E () / Western Cape Landcover Product. , –. Vector Geospatial Dataset. Western Cape Nature Conservation H A Y WA R D , M.W., B O I TA N I , L., B U R R O W S , N.D., F U N S T O N , P., Board, Bridgetown, South Africa. K A R A N T H , K.U., M AC K E N Z I E , D. et al. () Ecologists need to use C H A P M A N , S. & B A L M E , G. () An estimate of leopard population robust survey design, sampling and analysis methods. Journal of density in a private reserve in KwaZulu-Natal, South Africa, using Applied Ecology, , –. camera traps and capture–recapture models. South African Journal H I J M A N S , R.J., C A M E R O N , S.E., P A R R A , J.L., J O N E S , P.G., J A R V I S , A. of Wildlife Research, , –. () Very high resolution interpolated climate surfaces for global C H A S E G R E Y , J.N., K E N T , V.T. & H I L L , R.A. () Evidence of a high land areas. International Journal of Climatology: a Journal of the density population of harvested leopards in a montane Royal Meteorological Society, , –. environment. PLOS ONE, , –. J AC O B S O N , A.P., G E R N G R O S S , P., L E M E R I S , JR, J.R., S C H O O N O V E R , R.F., C R O O K S , K.R. () Relative sensitivities of mammalian A N C O , C., B R E I T E N M O S E R -W Ü R S T E N , C. et al. () Leopard carnivores to habitat fragmentation. Conservation Biology, , (Panthera pardus) status, distribution, and the research efforts –. across its range. PeerJ, , e. D E P A R T M E N T O F E N V I R O N M E N T A L A F F A I R S () South Africa J E N K S , G.F. () The data model concept in statistical mapping. Protected Areas Database (SAPAD_OR__Q). Http://egis. International Yearbook of Cartography, , –. environment.gov.za [accessed March ]. K A L L E , R., R A M E S H , T., Q U R E S H I , Q. & S A N K A R , K. () Density of D E V E N S , C., T S H A B A L A L A , T., M C M A N U S , J. & S M U T S , B. () tiger and leopard in a tropical deciduous forest of Mudumalai Tiger Counting the spots: the use of a spatially explicit capture–recapture Reserve, southern India, as estimated using photographic capture– technique and GPS data to estimate leopard (Panthera pardus) recapture sampling. Acta Theriologica, , –. density in the Eastern and Western Cape, South Africa. African K A R A N T H , K.U. () Estimating tiger (Panthera tigris) populations Journal of Ecology, , –. from camera-trap data using capture–recapture models. Biological E F FO R D , M.G. () secr—spatially explicit capture–recapture in R. Conservation, , –. R package version ... Https://CRAN.R-project.org/package=secr K A R A N T H , K.U. & C H E L L A M , R. () Carnivore conservation at the [accessed March ]. crossroads. Oryx, , –. E F FO R D , M.G. () secr: Spatially explicit capture–recapture models. K A R A N T H , K.U. & N I C H O L S , J.D. () Estimation of tiger densities in R package version ... Https://CRAN.R-project.org/package=secr India using photographic captures and recaptures. Ecology, , [accessed March ]. –. E F FO R D , M.G. & F E W S T E R , R.M. () Estimating population size by K A R A N T H , K.U. & N I C H O L S , J.D. () Ecological Status and spatially explicit capture–recapture. Oikos, , –. Conservation of Tigers in India. Final Technical Report to the E F FO R D , M.G., B O R C H E R S , D.L. & B Y R O N , A.E. () Density Division of International Conservation, US Fish and Wildlife estimation by spatially explicit capture–recapture: likelihood-based Service, Washington, DC, USA, Wildlife Conservation Society, methods. In Modeling Demographic Processes in Marked New York, USA, and Centre for Wildlife Studies, Bangalore, India. Populations (eds D.L. Thomson, E.G. Cooch & M.J. Conroy), M A N N , G. () Aspects of the ecology of leopards (Panthera pardus) in pp. –. Springer, New York, USA. the Little Karoo, South Africa. PhD thesis, Rhodes University, E L L I S , E.C. & R A M A N K U T T Y , N. () Putting people in the map: Grahamstown, South Africa. anthropogenic biomes of the world. Frontiers in Ecology and the M A P U T L A , N.W., C H I M I M B A , C.T. & F E R R E I R A , S.M. () Environment, , –. Calibrating a camera-trap based biased mark–recapture sampling E S T E S , J.A., T E R B O R G H , J., B R A S H A R E S , J.S., P O W E R , M.E., B E R G E R , J., design to survey the leopard population in the N’wanetsi B O N D , W.J. et al. () Trophic downgrading of planet Earth. concession, Kruger National Park, South Africa. African Journal of Science, , –. Ecology, , –. FAO (F O O D A N D A G R I C U LT U R E O R G A N I Z A T I O N O F T H E U N I T E D M A R T I N S , Q.E. () The ecology of the leopard Panthera pardus N AT I O N S ) () FAO GeoNetwork. Land Cover of South Africa – in the Cederberg Mountains. PhD thesis, University of Bristol, Globcover Regional. FAO, Rome, Italy. Http://www.fao.org/ Bristol, UK. geonetwork/srv/en/metadata.show?currTab=simple&id= M C M A N U S , J., D I C K M A N , A., G AY N O R , D., S M U T S , B. & [accessed June ]. M AC D O N A L D , D. () Dead or alive? Comparing costs and Oryx, 2021, 55(1), 34–45 © The Author(s), 2019. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605318001473 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 22 Jan 2021 at 15:24:38, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001473
Leopard density in South Africa’s Western Cape 45 benefits of lethal and non-lethal human–wildlife conflict mitigation S O I S A LO , M.K. & C AVA L C A N T I , S.M.C. () Estimating the density on livestock farms. Oryx, , –. of a jaguar population in the Brazilian Pantanal using camera traps M C M A N U S , J., D A LT O N , D.L., K OT Z É , A., S M U T S , B. & D I C K M A N , A. and capture–recapture sampling in combination with GPS () Gene flow and population structure of a solitary top radio-telemetry. Biological Conservation, , –. carnivore in a human-dominated landscape. Ecology and Evolution, S WA N E P O E L , L.H., L I N D S E Y , P., S O M E R S , M.J., H O V E N , W.V. & , –. D A L E R U M , F. () Extent and fragmentation of suitable leopard M U C I N A , L. & R U T H E R FO R D , M.C. (eds) () The Vegetation of habitat in South Africa. Animal Conservation, , –. South Africa, Lesotho and Swaziland. South African National S WA N E P O E L , L.H., S O M E R S , M.J. & D A L E R U M , F. () Density Biodiversity Institute, Pretoria, South Africa. of leopards Panthera pardus on protected and non-protected N O S S , A.J., G A R D E N E R , B., M A F F E I , L., C U É L L A R , E., M O N TA Ñ O , R. land in the Waterberg Biosphere, South Africa. Wildlife Biology, et al. () Comparison of density estimation methods for mammal , –. populations with camera traps in the Kaa-lya del Gran Chaco T H A M M , A.G. & J O H N S O N , M.R. () The Cape Supergroup. In landscape. Animal Conservation, , –. The Geology of South Africa (eds M.R. Johnson, C.R. Anhaeusser & O B B A R D , M.E., H O W E , E.J. & K Y L E , C.J. () Empirical comparison R.J. Thomas), pp. –. Geological Society of South Africa, of density estimators for large carnivores. Journal of Applied Ecology, Johannesburg/Council for Geoscience, Pretoria, South Africa. , –. T H A P A , K., S H R E S T H A , R., K A R K I , J., T H A P A , G.J., S U B E D I , N., P H I L L I P S , S.J., D U D I K , M., S C H A P I R E , R.E. () Maxent Software P R A D H A N , N.M.B. et al. () Leopard Panthera pardus fusca for Modelling Species Niches and Distributions (version ..). density in the seasonally dry, subtropical forest in the Bhabhar of Http://biodiversityinformatics.amnh.org/open_source/maxent Terai Arc, Nepal. Advances in Ecology, , –. [accessed July ]. T R E V E S , A. & K A R A N T H , K.U. () Human–carnivore conflict and P H I L L I P S , S.J., A N D E R S O N , R.P. & S C H A P I R E , R.E. () Maximum perspectives on carnivore management worldwide. Conservation entropy modeling of species geographic distributions. Ecological Biology, , –. Modelling, , –. T R E V E S , A. & N A U G H T O N -T R E V E S , L. () Evaluating lethal control QGIS D E V E LO P M E N T T E A M () QGIS Geographic Information in the management of human–wildlife conflict. Conservation System. Open Source Geospatial Foundation, Beaverton, USA. Biology, , –. Http://qgis.osgeo.org [accessed March ]. T R E V E S , A., N A U G H T O N -T R E V E S , L., H A R P E R , E.K., M L A D E N O F F , R C O R E T E A M () R: a Language and Environment for Statistical D.J., R O S E , R.A., S I C K L E Y , T.A. & W Y D E V E N , A.P. () Computing. R Foundation for Statistical Computing, Vienna, Predicting human–carnivore conflict: a spatial model derived Austria. Http://www.R-project.org [accessed July ]. from years of data on wolf predation on livestock. Conservation R A Y , J.C., H U N T E R , L.T.B. & Z I G O U R I S , J. () Setting Conservation Biology, , –. and Research Priorities for Larger African Carnivores. Wildlife T R A I L L , L.W., B R A D S H AW , C.J.A. & B R O O K , B.W. () Minimum Conservation Society, New York, USA. viable population size: a meta-analysis of years of published R O U G E T , M., R E Y E R S , B., J O N A S , Z., D E S M E T , P., D R I V E R , A., M A Z E , estimates. Biological Conservation, , –. K. et al. () South African National Spatial Biodiversity WCS (W I L D L I F E C O N S E R VA T I O N S O C I E T Y ) & CIESIN (C E N T E R Assessment : Technical Report. Volume : Terrestrial F O R I N T E R N AT I O N A L E A R T H S C I E N C E I N F O R M AT I O N N E T W O R K ) Component. South African National Biodiversity Institute, () Last of the Wild Project, Version , (LWP-): Global Pretoria, South Africa. Human Footprint Dataset (Geographic). NASA Socioeconomic Data R I P P L E , W.J., E S T E S , J.A., B E S C H TA , R.L., W I L M E R S , C.C., R I T C H I E , and Applications Center, Palisades, USA. Https://doi.org/./ E.G., H E B B L E W H I T E , M. et al. () Status and ecological effects HMHF [accessed June ]. of the world’s largest carnivores. Science, , . W O L F , C. & R I P P L E , W.J. () Range contractions of the world’s R S T U D I O T E A M () R Studio: Integrated Development for R. large carnivores. Royal Society Open Science, , . RStudio, Inc., Boston, USA. Http://www.rstudio.com [accessed W O O D R O F F E , R. () Predators and people: using human densities March ]. to interpret declines of large carnivores. Animal Conservation, , S I LV E R , S.C., O S T R O , L.E.T., M A R S H , L.K., M A F F E I , L., N O S S , A.J., –. K E L LY , M.J. et al. () The use of camera traps for estimating W O O D R O F F E , R. & G I N S B E R G , J.R. () Edge effects and the jaguar Panthera onca abundance and density using capture/ extinction of populations inside protected areas. Science, , recapture analysis. Oryx, , –. –. Oryx, 2021, 55(1), 34–45 © The Author(s), 2019. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605318001473 Downloaded from https://www.cambridge.org/core. IP address: 46.4.80.155, on 22 Jan 2021 at 15:24:38, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318001473
You can also read