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Carnivore coexistence facilitated by spatial and dietary partitioning and fine-

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DOI: 10.1111/jzo.12964

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 Journal of Zoology. Print ISSN 0952-8369

Carnivore coexistence facilitated by spatial and dietary

partitioning and fine-scale behavioural avoidance in a
semi-arid ecosystem
Lana Müller1 , Willem Daniel Briers-Louw2 , Rajan Amin3 , Christiaan Stefanus Lochner1
& Alison Jane Leslie4
1
The Cape Leopard Trust, Cape Town, South Africa
2
Zambeze Delta Conservation, Marromeu, Mozambique
3
Conservation Programmes, Zoological Society of London, Regent’s Park, London, UK
4
Department of Conservation Ecology and Entomology, Stellenbosch University, Stellenbosch, Western Cape, South Africa

Keywords
activity patterns; camera trapping; Caracal
caracal; coexistence; diet; Panthera pardus; scat
analysis; spatial overlap.
Correspondence
Lana Müller, The Cape Leopard Trust, P.O.
Box 31139, Tokai, Cape Town, 7966, South
Africa.
Email: lmuller1985@gmail.com
Editor: Femke Broekhuis
Associate Editor: Meredith Palmer
Received 28 April 2021; revised 10 February
2022; accepted 18 February 2022
doi:10.1111/jzo.12964
Abstract
Sympatric carnivores compete for similar resources which may lead to dominant
species influencing the ecology of subordinate ones. However, carnivores often
make use of coevolutionary strategies which enable them to minimise competition
with dominant competitors and thus facilitate coexistence. We used camera trapping
and scat analysis to investigate the potential competition between leopards (Pan-
thera pardus) and caracals (Caracal caracal) along spatial, temporal and dietary
axes to determine the mechanisms of their coexistence in the Cederberg, South
Africa. Our results showed that both carnivores co-occurred at 39.73% of camera
trapping sites, but spatial overlap based on Pianka’s index was relatively low. We
found a high overlap in daily activity patterns between these carnivore species both
during winter and summer. Leopards and caracals exhibited fine-scale behavioural
avoidance of one another, with time-to-encounters between interspecific competitors
being significantly larger compared to intraspecific competitors. The two carnivores
had a relatively high diet overlap, although this was largely due to one prey spe-
cies, namely rock hyrax (Procavia capensis), which appears to be an important
shared prey item. However, we did find evidence of dietary niche segregation, as
leopards consumed larger prey compared to caracals. Our study suggests that carni-
vore coexistence in the Cederberg is facilitated by a combination of population-
level partitioning in space-use and dietary habits, as well as fine-scale behavioural
avoidance at the individual level to reduce interference competition. This study pro-
vides insights into the competition and coexistence mechanisms between sympatric
carnivores and broadens our understanding of these ecological processes in carni-
vore guild systems.

partitioning along spatial, temporal and/or dietary axes to limit

Introduction
Competition plays an important role within carnivore assem-
blages by influencing the ability for carnivores to access lim-
ited resources (exploitation competition) and through direct and
indirect antagonistic interactions between carnivores (interfer-
ence competition), thus shaping carnivore ecological niches
(Linnell & Strand, 2000). More specifically, carnivore guilds
are structured by the influence of dominant species on subordi-
nate predators through suppression of their population abun-
dance and density (Caro & Stoner, 2003; Ritchie & Johnson,
2009), alteration of their spatial distribution (du Preez et al.,
2015) and modification of their feeding ecology (Elmhagen
et al., 2010; Périquet et al., 2015). However, sympatric carni-
vores may coexist through coevolutionary strategies of resource
the effects of interspecific competition (Durant, 1998; Karanth
& Sunquist, 1995; Périquet et al., 2015). Identifying and
understanding the mechanisms facilitating carnivore coexistence
is pertinent as these co-occurring species may provide essential
ecosystem (e.g. mesopredator suppression; Ritchie & Johnson,
2009) and economic services (e.g. tourism and public health
benefits; Braczkowski et al., 2018; Sonawane et al., 2021),
making it crucial to conserve these carnivore assemblages
(Estes et al., 2011; Rafiq et al., 2020).
Interference competition has been described as a strong
determinant of carnivore spatial distribution, temporal patterns
and behaviour (Berger & Gese, 2007; Broekhuis et al., 2013;
Hayward & Slotow, 2009). Mesopredators are naturally held in
their food web position by more dominant apex carnivores and

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Leopard and caracal coexistence
are buffered against population collapse by their ability to
switch prey species (Prugh et al., 2009). However, removal of
the apex predator from a system may result in the irruption of
these middle-ranking predators, known as the ‘mesopredator
release hypothesis’ (Crooks & Soulé, 1999), whereby released
mesopredators can attain higher densities and/or broader distri-
butions which may result in declines or extinctions of prey
populations (Loehle & Eschenbach, 2012; Prugh et al., 2009).
For example, the extirpation of wolves (Canis lupus) in the
American West released coyotes (Canis latrans) which resulted
in the killing of threatened and endangered species and the
decline of small mammal populations (Ripple et al., 2013).
These indirect effects can cause wide-ranging cascading effects
which can alter the structure and function of a whole ecosys-
tem (Estes et al., 2011; Terborgh et al., 2001). Therefore, to
ensure ecosystem structure and function are maintained, it is
important to preserve interactions between apex predators and
mesopredators (Ritchie & Johnson, 2009). However, recent lit-
erature questions the ubiquity of mesopredator release in multi-
predator communities, suggesting that impacts of apex preda-
tors on mesopredators are not homogenous and thus largely
context-dependent (Haswell et al., 2017; Jachowski et al.,
2020).
The threat of direct antagonistic encounters can create a
‘landscape of fear’ (Laundré et al., 2001), whereby subordinate
carnivores are limited to smaller or less suitable areas within a
landscape due to the presence of dominant carnivores (Swan-
son et al., 2014). However, heterogeneity across the landscape
reduces the probability of encounters and therefore risk (Brown
et al., 1999). This presents subordinate carnivores with oppor-
tunities to evade dominant predators by utilising low-risk
refuges (Durant, 1998), diurnal–nocturnal adaptations and vari-
ations in activity peaks (Hayward & Slotow, 2009) or modify-
ing their behaviour through habitat transitioning (du Preez
et al., 2015) or vigilance in response to the degree of risk
(Pangle & Holekamp, 2010; Switalski, 2003). Furthermore,
where the purely spatial or temporal overlap is high, carnivores
are also known to utilise fine-scale behavioural adaptations to
reduce the degree of encountering competitors which may
facilitate co-occurrence (Karanth et al., 2017). Such adaptations
may involve fine-scale spatial–temporal avoidance (Harmsen
et al., 2009; Karanth et al., 2017; Lahkar et al., 2020; Périquet
et al., 2021), reactive adjustment of subordinate carnivore
behaviour to the nearest dominant carnivore (Broekhuis et al.,
2013) or active tracking of dominant carnivores to reduce the
risk of agnostic encounters for subordinate carnivores (López-
Bao et al., 2016).
Leopards (Panthera pardus) are large carnivores that are
considered apex predators, while caracals (Caracal caracal)
are medium-sized carnivores that are considered mesopredators.
Both are highly adaptable, solitary felids that co-occur across
much of sub-Saharan Africa (Caro & Stoner, 2003). Through-
out their range, these carnivores occupy different ecological
niches and are capable of variable spatial and temporal
responses to the presence of interspecific competitors (Avenant
et al., 2016; Drouilly, Clark et al., 2018; Edwards et al., 2015;
Rafiq et al., 2020). In the Western Cape province of South
Africa, their spatial distributions and population densities are
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L. Müller et al.
considerably different, as leopards occur at low densities
(0.25–2.3 leopards/100 km2) and display large home ranges
(74–910 km2, Martins, 2010), while caracals occur at high den-
sities (23–47 caracals/100 km2) and have small home ranges
(7–65 km2, Avenant & Nel, 1998; Norton & Lawson, 1985).
This spatial heterogeneity within the landscape may reduce
direct costly encounters between these felids. In terms of their
temporal ecology, both carnivores generally display nocturnal
behaviour with bimodal activity patterns, that is, two activity
peaks, one after sunset and one before sunrise (Avenant &
Nel, 1998; Martins & Harris, 2013).
Quantifying carnivore dietary ecology is a fundamental com-
ponent in evaluating predator-prey dynamics and relationships
with sympatric carnivores (Vogel et al., 2019). Due to their
dietary plasticity, leopard and caracal can have catholic diets,
although they generally consume the most abundant, suitable
prey in a given area (Avenant & Nel, 2002; Hayward et al.,
2006) and for leopards these species fall within a preferred
weight range of 10–40 kg (Hayward et al., 2006). However,
unlike in the rest of their range, leopards in the Western Cape
are exposed to a low density, small-bodied prey base and as a
result, this leopard population has a limited prey selection,
showing a preference for smaller prey species such as small-
to medium-sized ungulates and rock hyrax (Procavia capensis,
Fröhlich et al., 2012; Martins et al., 2011; Norton et al.,
1986). A recent comparative study from Anysberg Nature
Reserve, a state-protected area in the Western Cape province
of South Africa, showed that leopards consumed mostly wild
ungulates while caracals fed mostly on micromammals, with a
dietary niche overlap of 53% (Drouilly, Nattrass et al., 2018).
Although carnivore diets often reflect prey availability (Grif-
fiths, 1975; Karanth & Sunquist, 1995), prey selection may
also depend on factors such as interspecific competition, with
larger carnivores potentially outcompeting smaller carnivores
(Carbone et al., 1997; McVittie, 1979).
Leopards in the Western Cape historically occurred sympatri-
cally with a large carnivore assemblage including lions (Pan-
thera leo) and spotted hyenas (Crocuta crocuta), although the
latter competitors were extirpated around 300 years ago (Shor-
tridge, 1934; Skead, 1980). These leopards are genetically sim-
ilar to the ‘bushveld’ leopard from the savanna region in
southern Africa, but their body size and mass differ signifi-
cantly, with the former weighing between one-third to half that
of the latter, for example, mean mass of females: 21 kg
(Cederberg) vs. 38 kg (Kruger National Park); and males: 35
vs. 58 kg (Bailey, 1993; Martins, 2010). Most carnivore guild
studies involving leopards have focused on competition with
larger carnivores such as lions and spotted hyenas (e.g. du
Preez et al., 2015; Balme et al., 2017; Miller et al., 2018),
despite leopards co-occurring and competing with smaller guild
members across their African range (Rafiq et al., 2020). As
such, there is limited knowledge on how leopards interact and
coexist with smaller carnivores.
Caracals are a smaller carnivore species with females weigh-
ing up to 12 kg and males up to 15 kg in the Western Cape
(Skinner & Chimimba, 2005). Carbone et al. (1999) showed
that carnivores weighing 21.5 kg or more, select vertebrate
prey that weighs >45% of their own body mass, whereas
L. Müller et al.
carnivores smaller than 21.5 kg select prey that weighs <45%
of their own body mass, with the latter selecting both verte-
brate and invertebrate prey. Thus, based on this energetic
model, leopards should occupy a distinct functional group
above caracals and maintain a competitive advantage over the
mesopredator, despite their smaller than usual body size and
mass. Furthermore, leopards are known to affect the detection
probability of subordinate mesopredators (Ramesh et al., 2017)
and interspecific killing of caracals by leopards has been docu-
mented (Martins, 2010). It is therefore likely that direct compe-
tition between these two felids may lead to caracals avoiding
areas where leopards are present (Avenant et al., 2016).
The Cederberg Mountains of South Africa provides a unique
opportunity to investigate the mechanisms of co-occurrence
between these two carnivores where (1) other large, dominant
predators are absent, (2) leopards are physically smaller com-
pared to the ‘bushveld‘ leopard and their body mass extends
either side of the 21.5 kg threshold of obligate carnivory (Car-
bone et al., 1999) thus potentially reducing the ecological
niche gap with caracals and (3) prey species are both small-
bodied and limited, which might result in the increased dietary
overlap.
The aim of this study was to determine how leopards and
caracals coexist within the Cederberg by investigating their
spatial distributions, temporal patterns and feeding ecologies.
We hypothesised that (1) caracals spatially avoid leopards, (2)
caracals avoid peak activity of leopards where they overlap
spatially, (3) fine-scale behavioural avoidance of interspecifics
will exceed that of conspecifics and (4) carnivores display diet-
ary segregation. We also investigated the effect of season and
biomes on the ecology of leopards and caracals. We expected
less spatial and temporal avoidance during the summer when
food may be limited thus increasing the likelihood of inter-
species competition. Greater spatial and temporal avoidance
(a)
Figure 1 Map of the camera trap sites (n = 73) and the presence of leopards, caracals or both carnivores at each site (a) and scat locations for
leopards and caracals (b) in the Cederberg study site. Inset: box indicates the study site (black square) in the Western Cape Province (grey
shade) of South Africa.
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Leopard and caracal coexistence
was expected in the fynbos biome due to greater landscape
heterogeneity making it easier to coexist. Since the need for
fine-scale interactions relies on competitors being relatively
close together, we expect fine-scale avoidance to be higher in
summer when resources are limited and in the karoo biome
which has less heterogeneity. To test these predictions, we used
camera trapping for spatial, temporal and fine-scale interaction
analyses and scat sampling for dietary analyses.
Materials and methods
Study area
The Cederberg (32°27’S; 19°25’E) is located 200 km north of
Cape Town and extends from Pakhuis Pass to Grootrivier in
the Western Cape Province, South Africa, (Martins & Harris,
2013). The study area covers approximately 1700 km2 of
rugged mountainous terrain, which includes CapeNature
Reserves (Cederberg Wilderness Area and Matjiesrivier Nature
Reserve), Bushmans Kloof Private Reserve, Cederberg Conser-
vancy (an array of privately-owned farms where landowners
agreed not to kill leopards or caracals) and farmland (Fig. 1).
Livestock farming was the dominant land use within the
Cederberg until the 1990s, but other agricultural practices such
as citrus, olive and rooibos tea farming have become more
common. Private reserves within the Cederberg area have rein-
troduced previously extirpated herbivores such as gemsbok
(Oryx gazella), red hartebeest (Alcelaphus buselaphus caama),
springbok (Antidorcas marsupialis) and Cape mountain zebra
(Equus zebra zebra, Martins & Harris, 2013). The carnivore
community in the Cederberg consists of a variety of species
such as bat-eared fox (Otocyon megalotis), Cape fox (Vulpes
chama), small-spotted genet (Genetta genetta), large-spotted
genet (Genetta tigrina), striped polecat (Ictonyx striatus),
(b)
3
Leopard and caracal coexistence
black-backed jackal (Canis mesomelas), aardwolf (Proteles
cristata), African wildcat (Felis silvestris), caracal and leopard.
The climate in the Cederberg is classified as semi-arid and
the area has two distinct seasons: a cool-wet winter between
April and September and hot-dry summer between October
and March (Martins & Harris, 2013). Temperatures range from
a minimum of –7°C in winter to a maximum of 47°C in sum-
mer (Martins & Harris, 2013). There are two main biomes:
fynbos, consisting of both fynbos (restioids, ericoids and pro-
teoids) and renosterveld vegetation (Renosterbos spp.), and the
succulent karoo comprising of small shrubs and succulents
(Martins et al., 2011). Mean annual rainfall is 669 mm in the
fynbos and 179 mm in the karoo (Martins & Harris, 2013).
The rugged and mountainous topography is divided by valleys
and ravines that are either densely wooded or open, with fyn-
bos having larger mountains and karoo having larger, flat open
areas. Altitudes range from 200 to 2026 m in the fynbos and
258 to 1446 m in the karoo (Martins & Harris, 2013).
Camera trapping
Leopard and caracal presence data were collected from 73 cam-
era trap stations distributed across the study area continuously
from October 2017 to September 2018 (Fig. 1). The camera trap
survey area was divided into grid cells of 50 km2 based on the
minimum home range size of female leopards in the Cederberg
(Martins, 2010). Each grid cell contained two camera trap sta-
tions with a mean intercamera station distance of 2.78 km
(range = 0.5–6 km) to maximise the chance of capturing indi-
viduals within the grid cells (Balme et al., 2009). Camera sites
were placed on trails, jeep tracks or along natural features such
as drainage lines where focal carnivores were likely to move
(Mann et al., 2015). Each camera trap station consisted of two
white-flash camera traps (Cuddeback X-Change Color Model
1279) which were placed about 2–3 m from the path. Cameras
were placed perpendicular to the path at ~40 cm above the
ground to obtain a full lateral body image of a passing animal.
All camera traps were set to operate for 24 h per day and to take
three photo-bursts every time the sensor was triggered, with a
delay of 1-s between successive triggers. Camera trap images
were processed in Camera Base version 1.3 (Tobler, 2007) and
manually identified to species level.
Scat collection
Scat samples were collected opportunistically along footpaths
and trails between May 2017 and February 2018. Due to most
felid species also defecating for territorial markings, a small
amount of scat was left behind (Martins et al., 2011). Scats
were identified as felid scat in the field following Walker
(1996). These scats were then differentiated between leopard
and caracal based on the size, shape and appearance of each
scat following methods described by Drouilly, Nattrass et al.
(2018), and later confirmed in the lab by the presence of hairs
from self-grooming (Mann et al., 2019). Carnivore scats of
doubtful identity were excluded from the analysis.
All scat samples were washed in water and air-dried at 30–
40°C in preparation for hair analysis. We randomly sampled
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L. Müller et al.
15–20 hairs from each scat sample (Wang & Macdonald,
2009) to create hair cross-sections following the methods
described by Douglas (1989). Cross-sections were analysed
under a Leica DM 2000 light microscope at 20–40× magnifi-
cation, and photographs and measurements of cross-sections
were made using the LAS Core V4.0 software (Leica
Microsystems Ltd, Wetzlar, Germany). Prey items were identi-
fied by comparing hair cross-sections to reference collections
from Rhodes University and published literature (Keogh, 1979,
1983, 1985). Cross-section analysis was aided by the macro-
scopic appearance of hairs as well as the presence of other
remains such as bones, footpads, hooves, teeth and claws (Nor-
ton et al., 1986). All hairs were sorted to species-level, except
for rabbits and hares (Lepus capensis, Lepus saxatilis and
Pronolagus saundersiae) and species from the genus Otomys
(Otomys irroratus and Otomys saundersiae) which were
grouped together due to similarities in hairs of individual spe-
cies (Mann et al., 2019). Isolated leopard and caracal hairs
within their own scats were assumed to be as a result of self-
grooming (Norton et al., 1986). Remains of birds, reptiles and
invertebrates were identified but not classified into lower taxo-
nomic groups.
Data analysis
Spatial
We had insufficient data to conduct two-species occupancy mod-
elling as there were too few sites where only caracal was
detected. So to investigate the site-specific association between
leopards and caracals, we first calculated the relative abundance
index (RAI, O’Brien et al., 2003) at the camera trap station by
dividing the independent number of captures by the total trap
nights at any given station (Ramesh et al., 2012). A capture was
considered independent when there was at least a 30 min interval
between the individuals of the same species at the same site
(O’Brien et al., 2003). A Spearman’s rank correlation test (Zar,
1999) was then conducted between RAI of leopard and caracal at
each station to assess the interpredator spatial association
(Ramesh et al., 2012). Each camera trap station was considered
spatially independent (Zhao et al., 2019) and we used the RAI for
each camera station to compute the spatial overlap index which is
used extensively to assess niche overlap between

1=2 species (Pianka,
1973): Oab ¼ ð∑nPia Pib Þ= ∑nP2ia ∑nP2ib , where Oab is spa-
tial overlap between species a and b; Pia and Pib are the propor-
tions of item i used by species a and b, respectively. Pianka’s
overlap index values range from 0 (no spatial overlap) to 1 (com-
plete spatial overlap). The analysis was done in R using the pack-
age spaa version 0.2.2 (Zhang, 2016). We used this index merely
as a measure of niche overlap as opposed to automatically imply-
ing competition from these values (Tsafack et al., 2021).
Temporal activity patterns
To estimate the temporal overlap between leopards and cara-
cals, we determined the diel activity patterns of the species’
using the time of detection on the camera trap photographs.
The activity time data were transformed to daylight, that is,
L. Müller et al.
sunrise and sunset using the dates and spatial locations of the
observations (Nouveliet et al., 2012). The analysis was per-
formed in the overlap package (version 0.3.2) in the R soft-
ware (Ridout & Linkie, 2009). The Δ4 overlap coefficient,
which is recommended for sample sizes >75, was calculated
for the summer and winter seasons and the two biomes
(Meredith & Ridout, 2014; Ridout & Linkie, 2009). Values
from the Δ4 overlap coefficient range from 0 (no overlap) to 1
(complete overlap). The estimated 95% confidence intervals
were obtained from 10 000 bootstrap samples. We followed
Monterroso et al. (2014) and defined low overlap when Δ4
was <0.5, moderate when Δ4 was between 0.5 and 0.75 and
high overlap when Δ4 was >0.75.
Fine-scale behavioural interactions
To assess fine-scale behavioural adaptations, we calculated
time-to-encounters, in decimal days, between consecutive
‘caracal-caracal (CC)’, ‘leopard-leopard (LL)’, ‘caracal-leopard
(CL)’ and ‘leopard-caracal (LC)’ capture events. We tested for
interspecific time-to-encounter exceeding intraspecific time-to-
encounter, as we expected caracals (subordinate carnivore) to
display fine-scale temporal avoidance of leopards (dominant
carnivore). We fitted a linear mixed-effects model with cross
factors ‘capture 1’ as the initial capture either caracal or leop-
ard, and ‘capture 2’ the subsequent capture as either caracal or
leopard in R statistical package lme4 (version 1.1-26, Bates
et al., 2015). Camera location was added as a random-effect
(Harmsen et al., 2009). The model ‘time-to-encounter’
response variable was log10-transformed to approximate
normal distribution of the residuals and equal variances. We
calculated the differences between model predicted time-to-
encounters for (1) LC and CC events and (2) CL and LL
events, and the 95% confidence intervals of the differences
using a bootstrap. A significant difference was inferred by its
95% confidence interval excluding zero.
Dietary
We followed Glen and Dickman (2006) in calculating the ade-
quacy of the dietary sampling effort using a Brillouin index:
H b ¼ ðlnN !  ∑lnni !Þ=N, where Hb is the diversity of prey, N
is the total number of prey items in all samples and ni is the
number of individual prey items in the ith category (Brillouin,
1956). An Hb curve was generated by bootstrapping the sam-
ple 10 000 times with replacement to obtain a mean Hb, vary-
ing the sample size from three to n, in increments of two.
Additionally, we calculated a curve using the percentage incre-
mental change of Hb. Scat sampling effort for each carnivore
was considered adequate if the diversity curve reached an
asymptote and the incremental change declined below 1%
(Hass, 2009).
Frequency of occurrence (FO) was calculated as the percent-
age of scats containing a particular prey item (Klare et al.,
2011). A corrected frequency of occurrence (CFO), which
accounts for multiple prey items per scat, was calculated by
designating a weighting value of 1 per scat, and each prey
item as a proportion of that scat, for example, two prey items
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Leopard and caracal coexistence
will each have a value of 0.5 (Klare et al., 2011). Both FO
and CFO account for rare prey species, and while CFO is the
preferred qualitative method for dietary analysis, FO was
included here for comparative purposes (Klare et al., 2011).
Dietary niche breadth, as a measure of diet specialisation for
leopards and caracals, was calculated using Levin’s index
(Levins, 1968): B ¼ 1=∑P2i , where Pi represents the frequency
of occurrence of the prey item in the scat. To allow for com-
parison, we standardised dietary niche breadth as a proportion
using the equation: BA ¼ B  1=n  1 (Levins, 1968), where
BA represents Levin’s standardised niche breadth and n the
number of prey species in carnivore diets. The values range
from 0 (specialist diet) to 1 (generalist diet). To determine diet-
ary overlap between leopards and caracals we used Pianka’s
overlap index (Pianka, 1973).
Biomass calculation models provide the most accurate esti-
mate of true carnivore diet and are the most relevant parame-
ters in dietary analysis because of their application in ecology
such as the impact of predation on prey populations (Klare
et al., 2011). To calculate biomass consumed, we used an
asymptotic regression model developed by Chakrabarti et al.
(2016) for obligate carnivores: Y = (0.033–0.024exp–4.284X/Z),
where Y is the mass of prey consumed per collectable scat, X
is prey body mass and Z is predator body mass. A mean body
mass of 35 kg was used for leopards based on Martins (2010),
which was chosen for comparative purposes with other leopard
populations in the Western Cape (e.g. Mann et al., 2019). For
caracal and prey species, we obtained mean adult body mass
from Skinner and Chimimba (2005), while for feral pigs (Sus
scrofa), we based this on recently published literature (Mann
et al., 2019). For larger ungulate species (gemsbok), we multi-
plied adult mass by 0.3 (Radloff & du Toit, 2004) due to the
assumption that leopards would typically prey on individuals
closer to their optimal prey size (Hayward et al., 2006). Mam-
malian prey were grouped into large (40–63 kg), medium (10–
40 kg), small (1–10 kg), very small (<1 kg) species and live-
stock categories, to compare the importance of each class to
carnivore diets. Non-mammalian prey items were excluded
from biomass calculations due to difficulties in species identifi-
cation. We used chi-square analysis to compare the frequency
of occurrence of mammalian prey size categories between car-
nivore diets. All statistical analyses were conducted in R ver-
sion 3.6.3 (R Development Core Team, 2019).
Results
Spatial
We recorded 741 independent leopard captures at 69 (95.00%)
sites and 153 independent caracal captures at 33 (45.00%)
sites. Leopards were found exclusively at 54.79% of sites and
caracals were found exclusively at only 5.48% of sites (Fig. 1).
Sites where both predators occurred totalled 39.73% and leop-
ards used these sites more often than caracals with a ratio of
3:1 based on trap rate. Predator co-occurrence at the same site
was more common in winter (30.00%) than in summer
(18.57%), and the percentage of carnivore-exclusive sites was
marginally higher in summer (81.43%) than in winter
5
Leopard and caracal coexistence
(71.43%). While all sites used by caracals in the karoo were
also used by leopards, 8.89% of the sites in fynbos were
exclusively used by caracal. Despite caracals co-occurring with
leopards at many camera trap sites, the spatial overlap based
on Pianka’s index (which accounts for the proportion of use)
between leopard and caracal was relatively low (0.11) and
caracal space use was negatively associated with leopard space
use (rs = –0.37, P < 0.01).
Temporal activity patterns
Overall, leopard and caracal were both crepuscular and noctur-
nal. In summer, leopards displayed a bimodal pattern of activ-
ity with peaks around sunset and sunrise, whereas caracals
displayed a unimodal pattern of activity with a peak around
Figure 2 Overlap (grey area) in daily activity patterns between leopard and caracal between summer and winter, as well as between fynbos and
karoo biomes.
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L. Müller et al.
midnight (Fig. 2). In winter, leopards displayed a bimodal
activity pattern with peaks in activity at sunset and between
midnight and sunrise (Fig. 2). Caracals showed a trimodal
activity pattern with two main peaks close to midnight and
sunrise and an additional slight peak around noon. Temporal
overlap between leopard and caracal was high in summer
(0.77; 95% CI: 0.68–0.85) and winter (0.77; 95% CI: 0.68–
0.86). Similarly, temporal overlap was high between fynbos
(0.79; 95% CI: 0.71–0.87) and karoo (0.79; 95% CI: 0.70–
0.88; Fig. 2).
Fine-scale behavioural interactions
The number of intraspecific and interspecific photo-capture
events were 139 (CC), 47 (CL), 46 (LC) and 724 (LL). Our
L. Müller et al.
model revealed the time-to-encounters (in log10 scale)
between LC captures (1.25) and CL capture (1.38) were sig-
nificantly longer than those between consecutive same-species
captures, CC (0.85) and LL (1.11). The predicted difference
between interspecific and intraspecific time-to-encounter events
were (1) LC and CC (0.40, 95% CI: 0.18–0.63) and (2) CL
and LL (0.27, 95% CI: 0.08–0.47). As expected, the LC–CC
difference was larger than CL–LL. Time-to-encounters varied
by season and biome, with greater LC and CC differences
compared to CL and LL in summer and in the karoo biome
(Appendix S1).
Dietary
A total of 547 prey items were recorded in leopard scats
(n = 469), representing 27 different prey species, while 133
prey items were recorded in caracal scats (n = 96), representing
20 different prey species (Appendix S2). The mean number of
prey items per scat was 1.17 for leopards and 1.39 for cara-
cals, while the majority of scats contained single prey items
Figure 3 Brillouin diversity curves (black triangles) and percentage (incremental) change curves (grey dots) for leopard and caracal scat samples.
Mean values were obtained by resampling with replacement 10 000 times.
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Leopard and caracal coexistence
for leopards (83.09%) and caracals (70.83%). Our sampling
effort was adequate for both species, with diversity curves
reaching an asymptote and the incremental change decreasing
to <1% at ≥43 and ≥37 samples, respectively (Fig. 3).
Based on FO, the most frequently consumed prey items for
leopards were rock hyrax (49.04%), klipspringer (Oreotragus
oreotragus, 29.64%) and common duiker (Sylvicapra grimmia,
6.82%, Table 1). For caracals, rock hyrax (39.58%), Namaqua
rock mouse (Micaelamys namaquensis, 23.96%) and Karoo or
bush rats (Otomys spp., 22.92%) were most frequently con-
sumed. Mean prey weight was higher for leopards
(12.38  3.57 [SE] kg) compared to caracals (4.46  3.86
[SE] kg), based on the five top contributing species. Based on
biomass consumed, rock hyrax and klipspringer remained the
two most important species for leopards, although grey rhebok
(Pelea capreolus) contributed the next highest proportion to
total biomass consumed (7.72%). For caracals, rock hyrax
(50.27%), rabbits and hares (Lepus spp. and Pronolagus saun-
dersiae, 10.23%) and Namaqua rock mouse (8.27%) repre-
sented the highest contributions to overall biomass consumed.
7
Leopard and caracal coexistence L. Müller et al.

Table 1 Frequency of occurrence per scat (FO, %), corrected frequency of occurrence (CFO, %), mean prey body mass (kg), corrected biomass
consumed (kg) and relative biomass consumed (%) of prey species in leopard and caracal scat in the Cederberg, South Africa

Mean Corrected Relative

CFO mass biomass biomass
FO (%) (%) (kg) (kg) (%)
Prey species Leopard Caracal Leopard Caracal Leopard Caracal Leopard Caracal
Aardwolf Proteles cristatus 0.21 0.00 0.21 0.00 9.50 0.88 0.00 0.24 0.00
African wild cat Felis silvestris 0.43 0.00 0.43 0.00 4.30 1.28 0.00 0.34 0.00
Cape fox Vulpes chama 0.21 1.04 0.21 0.52 2.65 0.52 0.15 0.14 0.67
Cape grey mongoose Galerella pulverulenta 0.00 1.04 0.00 0.35 0.80 0.00 0.06 0.00 0.27
Cape grysbok Raphicerus melanotis 4.05 1.04 3.59 1.04 10.25 15.24 0.41 4.11 1.91
Caracal Caracal caracal 0.21 0.00 0.21 0.00 8.70 0.85 0.00 0.23 0.00
Chacma baboon Papio ursinus ursinus 2.13 1.04 2.03 1.04 23.60 10.51 0.43 2.84 1.96
Common duiker Sylvicapra grimmia 6.82 4.17 5.86 3.65 16.10 28.41 1.48 7.67 6.83
Common mole-rat Cryptomys hottentotus 0.00 2.08 0.00 1.56 0.00 0.00 0.17 0.00 0.80
Domestic pig Sus scrofa 0.21 0.00 0.21 0.00 130.00 1.15 0.00 0.31 0.00
Elephant shrew Elephantulus edwardii 0.00 2.08 0.00 1.30 0.00 0.00 0.14 0.00 0.64
Forest shrew Myosorex varius 0.00 1.04 0.00 0.52 0.00 0.00 0.05 0.00 0.24
Gemsbok Oryx gazella 0.85 0.00 0.75 0.00 63.00a 4.04 0.00 1.09 0.00
Goat Capra hircus 1.49 3.13 1.39 3.13 50.00 7.49 1.28 2.02 5.87
Grey climbing mouse Dendromus melanotis 0.00 1.04 0.00 0.35 0.00 0.00 0.02 0.00 0.16
Grey rhebuck Pelea capensis 6.18 0.00 5.65 0.00 20.00 28.60 0.00 7.72 0.00
Hairy-footed gerbil Gerbillurus paeba 0.43 2.08 0.32 0.69 0.03 0.42 0.07 0.11 0.32
Klipspringer Oreotragus oreotragus 29.64 1.04 23.53 0.52 11.90 104.94 0.21 28.32 0.96
Hares & rabbits Lepus/Pronolagus spp. 2.77 9.38 2.56 7.81 2.35 5.98 1.67 1.61 9.56
Marsh mongoose Atilax paludinosus 0.21 0.00 0.11 0.00 2.80 0.27 0.00 0.07 0.00
Namaqua rock mouse Micaelamys 0.64 23.96 0.64 18.40 0.05 0.86 1.91 0.23 8.79
namaquensis
Karoo/Bush rat Otomys spp. 1.07 22.92 0.96 14.84 0.13 1.32 1.67 0.36 7.66
Porcupine Hystrix africaeaustralis 2.99 0.00 2.20 0.00 12.15 9.89 0.00 2.67 0.00
Rock hyrax Procavia capensis 49.04 39.58 43.00 33.33 3.66 120.18 10.56 32.43 48.57
Sheep Ovis aries 2.77 2.08 2.56 2.08 40.00 13.78 0.85 3.72 3.92
Small-spotted genet Genetta genetta 0.21 0.00 0.21 0.00 1.90 0.46 0.00 0.12 0.00
Springbok Antidorcas marsupialis 1.71 0.00 1.71 0.00 31.50 9.09 0.00 2.45 0.00
Steenbok Raphicerus campestris 0.85 0.00 0.85 0.00 11.10 3.72 0.00 1.00 0.00
Striped field mouse Rhabdomys pumilio 0.21 0.00 0.11 0.00 0.04 0.14 0.00 0.04 0.00
Striped polecat Ictonyx striatus 0.21 0.00 0.21 0.00 0.68 0.35 0.00 0.09 0.00
Yellow mongoose Cynictic pencillata 0.21 1.04 0.11 1.04 0.83 0.18 0.18 0.05 0.83
Bird 0.85 7.29 0.39 3.30 – – – – –
Invertebrates 0.00 7.29 0.00 2.86 – – – – –
Squamates 0.00 4.17 0.00 1.65 – – – – –

Boldface indicates the most frequently consumed (>5%) prey items for both carnivores.
a
Is the juvenile mass for larger ungulate species.

Prey size categories differed significantly between the two
species (χ2 = 86.36, d.f. = 3, P < 0.05). Leopards consumed
larger prey, with medium-sized mammals (10–40 kg) making
up 56.78% of their diet, while caracals consumed relatively
smaller prey with small mammals (1–10 kg) making up
58.83% of their diet (Fig. 4). Livestock contributed to both
leopard and caracal diets, but the total biomass consumed was
<10% for both carnivores.
Niche dietary breadth was 3.97 for leopard and 6.59 for
caracal and standardisation revealed that dietary breadth was
low for leopard (0.11) and caracal (0.29), representing spe-
cialised diets for both carnivores. A relatively high degree of
dietary overlap (0.66) was recorded between the two carnivore
species, mostly owing to the substantial contribution of rock
hyrax in both carnivore diets.
Discussion
Effectively conserving carnivores in their natural environment
requires an understanding of how these carnivores coexist
without competitively excluding one another. Sympatric carni-
vores in this study did not segregate along the temporal axis.
However, we found these carnivores displayed some degree of
spatial and dietary niche partitioning as well as fine-scale beha-
vioural avoidance which likely facilitates carnivore coexistence
in this semi-arid landscape.

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L. Müller et al.
Figure 4 Biomass consumed (%) for each of the prey weight classes found in the leopard and caracal diet in the Cederberg.
Spatial
As expected, our study revealed some level of spatial segrega-
tion between leopards and caracals. In the Cederberg, the like-
lihood of encountering a leopard may be relatively low for a
caracal as leopards maintain large home ranges and occur at
low densities (Martins, 2010), in contrast to the comparatively
higher densities and smaller ranges of caracals in the region
(Avenant & Nel, 1998). Resource availability is a strong pre-
dictor of carnivore spatial distribution (Rich et al., 2017; Ver-
schueren et al., 2021) and spatial overlap between is usually
higher when prey densities are lower to maximise resource
acquisition (Karanth et al., 2017). Thus, given the spatial seg-
regation found here, it is likely that prey densities are suffi-
cient to support current carnivore densities and reduce
competition between carnivores. However, contrary to our pre-
diction, spatial avoidance was highest in summer. One hypoth-
esis is that caracals can spatially avoid leopards more in
summer due to density peaks in rodents (Avenant, 1993),
which contribute substantially to their diet, resulting in less
direct competition with leopards. However, we acknowledge
that spatial analyses were not based on robust two-species
occupancy analyses.
Spatial heterogeneity in the landscape may also play a key
role in facilitating carnivore coexistence through the availabil-
ity of different habitats and other physical features, as well as
uneven resource distribution (Chesson, 2000; Stein et al.,
2014) which can provide vital refuges for subordinate species
to reduce encounters with dominant carnivores (Davies et al.,
2021; Durant, 1998). Our results indicated that spatial avoid-
ance was slightly higher in the fynbos biome compared to the
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Leopard and caracal coexistence
karoo which is likely due to the landscape heterogeneity which
provides more refugia (e.g. vegetation cover) for caracals, to
which they may be positively associated (Verschueren et al.,
2021). This emphasises the importance of conserving natural
habitat heterogeneity in human-dominated landscapes and sup-
porting land-use types that are conducive to carnivore conser-
vation.
Temporal activity patterns
Carnivores exhibited a high degree of temporal overlap in our
study with no differences between seasons or biomes, which is
likely due to relatively low carnivore densities minimising the
likelihood of competitive or agnostic interactions (Hayward &
Hayward, 2007). Romero-Muñoz et al. (2010) also suggested
that low carnivore densities may reduce the probability of
competitor encounters, and resource partitioning may not even
be required in such cases. As a result, subordinate species do
not necessarily need population-level modifications of their
activity patterns to facilitate carnivore coexistence (Lahkar
et al., 2020). However, subtle variations in activity peaks did
exist in our study. Caracal activity peaked around midnight,
while leopard activity peaked around dawn and dusk, these dif-
ferences were more pronounced during summer. Although it is
clear that carnivore temporal overlap is high, given that tempo-
ral activity patterns have evolved to satisfy a variety of selec-
tion forces that differ amongst species to minimise interactions
with competitors, while increasing chances of hunting success
(Hayward & Slotow, 2009; Karanth et al., 2017), it is plausible
that caracals could alter their peak activity to optimise this
trade-off.
9
Leopard and caracal coexistence
Fine-scale behavioural interactions
Resource partitioning is not always distributed along clear
space and time axes, but could also be ‘hidden’ in finer-scale
behavioural interactions between carnivores (Karanth et al.,
2017; Lahkar et al., 2020). Karanth et al. (2017) found that
fine-scale spatio–temporal interactions facilitated coexistence
among tigers (Panthera tigris), leopards and dholes (Cuon
alpinus) in India. Similarly, Swanson et al. (2016) found that
cheetahs avoided dominant lions on a moment-to-moment basis
and suggested that fine-scale avoidance strategies may prove
less costly for subordinate predators compared with long-term
avoidance of suitable habitats. Furthermore, Broekhuis et al.
(2013) stated that carnivore responses to predation risk may be
reactive rather than predictive, with subordinate predators
adjusting their behaviour to the nearest position of dominant
predators. Our study found that LC and CC differences were
greater than CL and LL differences, consistent with our
hypothesis and this literature. The fine-scale avoidance found
in our study (i.e. LC and CC > CL and LL) was higher in
summer, as expected, which is likely when carnivores are
attracted to limited resource hotspots. Fine-scale avoidance was
also higher in the karoo biome which supports less landscape
heterogeneity compared to fynbos, and therefore caracals likely
have to respond reactively to reduce predation risk by leopards
in this biome. This suggests that fine-scale avoidance responses
play an important role in shaping carnivore assemblages both
seasonally and across habitats and we recommend the inclusion
of these analyses in future studies.
Dietary
Both carnivores displayed specialised diets, which could be
explained by the lack of large-bodied prey and limited prey
diversity in the study area (Martins et al., 2011). Previous
studies suggest that leopards have generalised diets (e.g. Hay-
ward & Kerley, 2008), however, the leopard diet may be more
specialised than previously thought (Balme et al., 2007; Pitman
et al., 2013). Interestingly, the leopard diet in the Cederberg
was more specialised than those found in the Boland and Little
Karoo regions of the Western Cape, with the Boland being a
more mesic region dominated by fynbos and the Little Karoo
having similar climate, rainfall and topography to the Ceder-
berg (Mann et al., 2019). This variation in feeding patterns
across sites concurs with a previous comparative study (Norton
et al., 1986). Balme et al. (2020) found that leopard popula-
tions may consist of a heterogeneous mix of specialist and
generalist individuals with the primary driver of dietary spe-
cialisation being ecological opportunity which is influenced by
phenotypic constraints (e.g. sex of individuals or experience)
and environmental conditions (e.g. prey diversity), as predicted
by the optimal foraging theory (Stephens & Krebs, 1986).
Therefore, we hypothesise that variations in the types and
amount of prey available to leopards as well as individual
traits may be influencing the degree of dietary specialisation
between leopards in these different regions. Our study found
that the caracal diet was specialised and consisted mostly of
rodents. Caracals typically have a broad dietary range
10
L. Müller et al.
constituting mostly mammals, but the importance of prey
items, like rodents and antelope, varies widely between studies
(Avenant et al., 2016). Thus, these findings highlight the
importance of area-specific studies to improve the understand-
ing of carnivore feeding behaviour at a finer scale (Briers-
Louw & Leslie, 2020).
Despite the smaller gap between carnivore body sizes in the
Western Cape, leopards still consumed significantly larger-sized
prey groups compared to caracals, with leopards feeding pre-
dominantly on medium-sized prey (10–40 kg) and caracals on
small-sized prey (1–10 kg), which coincides with other studies
(Avenant & Nel, 1998; Drouilly, Nattrass et al., 2018; Hay-
ward et al., 2006). Although carnivores displayed selective pre-
dation of different sized prey groups which may facilitate
carnivore coexistence (Karanth & Sunquist, 1995), we found a
high dietary overlap between the two sympatric carnivores,
which was attributed to the contribution of rock hyrax. The
continued utilisation of rock hyrax by leopards in the Western
Cape is certainly interesting and its importance has been docu-
mented for over 35 years (Norton et al., 1986). This could be
related to density-dependent processes as the rock hyrax is the
most abundant prey species within the study site (Drouilly,
Nattrass et al., 2018b; Martins & Harris, 2013; Palmer & Fair-
all, 1988). High prey density has also been highlighted as a
potential mediator of carnivore coexistence (Marneweck et al.,
2019). Therefore, the high abundance of rock hyrax in the
Cederberg could be facilitating coexistence between leopards
and caracals. In conjunction with previous studies (Fröhlich
et al., 2012; Jansen et al., 2019; Mann et al., 2019; Martins
et al., 2011; Norton et al., 1986), our findings suggest that this
prey species contributes to a fundamental part of both leopard
and caracal diet in the Western Cape and is therefore a crucial
species to manage and conserve.
A contentious issue in the farmland surrounding the Ceder-
berg is the depredation of livestock by leopard and caracal,
and the subsequent retaliatory killings of these carnivores by
landowners. Lethal control of leopards (and likely caracals)
appears to have decreased over time due to long-term conser-
vation efforts (Martins, 2010), but human-carnivore conflict
still occurs today. It has been suggested that livestock preda-
tion can be predicted from the biomass of wild prey, with live-
stock predation rates increasing significantly when prey
biomass decreases below 540 kg/km2 (Khorozyan et al., 2015).
Another study found that carnivores consumed less livestock
than expected due to the high biomass of preferred prey (Wang
& Macdonald, 2009). Findings from this and other studies
(Martins et al., 2011; Norton et al., 1986) show that livestock
may provide an alternative food resource for leopard and cara-
cal, but the contribution remains less than 10% of their overall
diets. Therefore, it is likely that current wild prey populations
may sufficiently support leopard and caracal populations that
coexist in the Cederberg landscape, reducing the need for car-
nivores to find alternative food sources.
Interestingly, in a range-wide study of leopards (which
excluded leopards from the Cape), the mean body mass of pre-
ferred prey was ~43% of their body mass (Hayward et al.,
2006), whereas in our study, the mean prey body mass of leop-
ard selected prey was ~35% of their body mass. This suggests
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L. Müller et al.
that leopard body size may influence prey size selection,
although the availability of medium- and large-bodied prey
which make up their diets may also play an important role.
Meanwhile, for caracals, the absence of a dominant apex preda-
tor may influence their diet selection with caracals potentially
taking down larger-bodied prey typically associated with larger
carnivore diets (Palmer & Fairall, 1988). However, rodents are
still reported as their main prey group across most studies both
with and without more dominant competitors (e.g. Avenant &
Nel, 2002; Jansen et al., 2019; Melville et al., 2004).
Throughout Africa, leopards and caracals naturally co-occur
within systems that support intact carnivore guilds, including
large-bodied and abundant prey as well as larger-bodied leop-
ards (e.g. Melville et al., 2004). In these systems, one would
expect a broader ecological niche gap to exist based on the fol-
lowing factors. Firstly, the body size difference between these
two carnivores is greater compared to our scenario, which will
result in different energetic requirements (Carbone et al., 1999)
and species may respond differently along space, time and diet
axes. For example, a study from Welgevonden Game Reserve (a
fenced system with an intact carnivore guild) found that sym-
patric carnivore activity overlap with dominant lions decreased
as the body mass of sympatric carnivores decreased (Greco
et al., 2021). Secondly, the availability of larger-bodied prey
may reduce the need for leopards to consume smaller-bodied
prey, that is naturally consumed by caracals, according to ener-
getic expenditure versus energetic intake rates (Carbone et al.,
2007), resulting in lower levels of direct competition. For exam-
ple, in the Kgalagadi Transfrontier Park (an intact, semi-arid sys-
tem), the leopard diet consisted largely of springbok and other
medium-to-large-sized mammals (Mills, 1984), while the caracal
diet consisted mostly of rodents (Melville et al., 2004). Based
on our results, there was evidence that leopards and caracals
operated in different ecological niches, although the niche gap
was not exceptionally broad and resource overlap did occur.
This could be explained by a lack of large prey available to
leopards, hyper abundance of rock hyrax providing plenty of
food for both carnivores, low densities of the apex carnivore and
both carnivores occurring relatively close to the 21.5 kg weight
threshold between small and large carnivores (Carbone et al.,
1999). Ultimately, despite a narrower ecological gap, caracals
are still able to coexist alongside leopards in the Cederberg land-
scape. However, quantitative evidence comparing ecological
niche gaps among carnivore species is lacking and studies inves-
tigating this could provide important insights into carnivore
competition across various systems. Today, intact large carnivore
guilds only cover 8% of their former range due to human popu-
lation growth and agricultural development (Wolf & Ripple,
2017). Therefore, systems with incomplete carnivore guilds (like
the Cederberg) are widespread across the continent and carni-
vores have adapted to coexist within these landscapes. Our find-
ings emphasise the importance of studying competition and
coexistence mechanisms between sympatric carnivores across
their ranges to better understand the ecological processes that
govern carnivore community structure and function, particularly
since carnivore populations are threatened by habitat loss and
fragmentation, prey loss and direct poaching (Rayan & Linkie,
2016).
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Leopard and caracal coexistence
Acknowledgements
We thank Ewan Brennan, Hannes de Kok, Barbara Seele,
Ismail Wambi and Grant Baker, for assisting with the camera
trap survey. A special thanks also to Rika du Plessis from
CapeNature and all the Cederberg landowners for their support
and for giving us access to their properties. We thank Ford
Wildlife Foundation for providing a vehicle to the research
team. We thank Mikaela Liltved and the Department of Con-
servation Ecology & Entomology at Stellenbosch University
for assisting with the caracal scat analysis, as well as Margaret
and Graham Avery from the Iziko South African Museum for
osteological reference collections. We acknowledge the Cape
Leopard Trust for providing the resources to enable this
research. We are also very grateful to our donors, Abax Foun-
dation, Bushmans Kloofs Wilderness Reserve, Lomas Wildlife
Protection Trust and the Rolf Stephan Nussbaum Foundation.
Without their support this work would not have been possible.
Finally, we want to thank Professor Dan Parker for reviewing
this paper.
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Leopard and caracal coexistence
Zhao, G., Yang, H., Xie, B., Gong, Y., Ge, J., & Feng, L.
(2019). Spatio-temporal coexistence of sympatric
mesocarnivores with a single apex carnivore in a fine-scale
landscape. Global Ecology and Conservation, 21, e00897.
Supporting Information
Additional Supporting Information may be found in the online
version of this article:
Appendix S1. Model results for predicted time-to-encounters
for (1) leopard-caracal (LC) and caracal-caracal (CC) events
and caracal-leopard (CL) and leopard-leopard (LL) events.
Appendix S2. Details of leopard and caracal scats collected in
the Cederberg study area between May 2017 and February
2018.
15