Download Prey morphology and predator sociality drive predator prey

Journal of Mammalogy, 97(3):919–927, 2016
DOI:10.1093/jmammal/gyw017
Published online February 22, 2016
Prey morphology and predator sociality drive predator prey
preferences
Hayley S. Clements,* Craig J. Tambling, and Graham I. H. Kerley
Centre for African Conservation Ecology, Department of Zoology, Nelson Mandela Metropolitan University, Port Elizabeth 6031,
South Africa
* Correspondent: [email protected]
Predator prey preferences shape the dynamics of predator–prey assemblages. Understanding the determinants
of a predator’s prey preferences is therefore important. Trends in prey preferences of the large African predators
have been described at a species scale, limiting our ability to assess the influence of prey morphology (size and
horns) and predator social structure (sex and sociality) on prey preferences. An analysis of cheetah Acinonyx
jubatus kill and prey abundance information from throughout South Africa shows that the presence of prey
horns and the type of cheetah social group interact with prey size to influence cheetah prey preference. The size
threshold above which prey is avoided by cheetah is lower for horned prey than non-horned prey, providing
evidence that horns are a predation deterrent in medium-sized prey. Horned females occur significantly more
frequently in antelope species on the cusp of being too large for cheetah predation, supporting the hypothesis that
horns evolved as an antipredator defense in the females of medium-sized prey. Male coalition cheetah have access
to a broader weight range of prey than solitary cheetah, which may infer fitness benefits by way of expanded
resource options. The prey weight range accessible to solitary male cheetah is similar to that accessible to solitary
female cheetah, suggesting that, in the absence of cooperative hunting, the slightly larger size of the male cheetah
infers no hunting advantage. These findings provide insight into the predation pressures driving the evolutionary
selection for large body size and horns in prey, and expanded resource access leading to predator sociality.
Key words: cheetah, horns, large carnivore, predator sociality, prey preference, prey size
© 2016 American Society of Mammalogists, www.mammalogy.org
Predators display prey preferences that in turn influence ecosystem patterns and processes such as biomass fluxes (OwenSmith and Mills 2008), the abundance of predators relative
to prey (Carbone and Gittleman 2002), and prey population
composition and dynamics (Sinclair et al. 2003; Gervasi et al.
2015). Across a myriad of carnivore species, these prey preferences are influenced by the size of the prey relative to the
size of the predator (Gittleman 1985; Sinclair et al. 2003;
Owen-Smith and Mills 2008; Gervasi et al. 2015). Among terrestrial carnivores, there is a body mass limit (21.5 kg) above
which a carnivore’s energy requirements necessitate predation on prey weighing more than 45% of the carnivore’s body
mass (Carbone et al. 1999). The relationship between predator size and prey size is perhaps most critical for these larger
predators, due to the challenges of capturing and subduing
large prey (Gittleman 1985). Large African predators regularly predate ungulates double their mass (Gittleman 1985;
Owen-Smith and Mills 2008), with the possibility of injury
or death to the predator during prey capture (Hayward and
Kerley 2005).
According to optimal foraging theory, a predator should
select prey that offers maximum energetic benefits in terms of
size, with minimum energetic costs and risks incurred during
prey capture (Pyke et al. 1977). Risk imposed on the predator
during prey capture is likely influenced not only by relative prey
size but also by other prey and predator life history attributes,
such as prey defense morphology (e.g., the presence of horns,
spines, or plates) and behavior (e.g., grouping) that may repel
predator attacks (Packer 1983; Caro 2005), and predator social
structure (e.g., cooperative hunting) that may improve hunting
success rates (Kruuk 1975; Fanshawe and FitzGibbon 1993).
Stankowich and Caro (2009) predict that larger prey species, by
being better able to defend themselves against predators as well
as by being more exposed, should benefit more from defensive
weaponry (e.g., horns) than smaller species. This suggests that
predation risk is a function of the interaction between prey size
and weaponry. Furthermore, predators that hunt cooperatively,
at least to the extent that all group members hunt simultaneously, can kill prey that is larger relative to their own size than
solitary predators (Kruuk 1975; Fanshawe and FitzGibbon
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1993). Males of sexually dimorphic predators also kill larger
prey than females (Radloff and du Toit 2004).
Prey size is an important determinant of prey preference of
the large African predators: cheetah Acinonyx jubatus, leopard
Panthera pardus, lion Panthera leo, spotted hyaena Crocuta
crocuta, and African wild dog Lycaon pictus (Hayward and
Kerley 2005; Hayward 2006; Hayward et al. 2006a, 2006b,
2006c; Clements et al. 2014). Risk presented by prey species
is a further determinant of prey preference in cheetah, leopard,
and wild dog (Hayward et al. 2006a, 2006b, 2006c). Hayward
and colleagues classed these risks a priori according to documented predator–prey interactions, on a scale from 0 (no threat)
to 2 (severe threat; known deaths of predators caused by the
species). The mechanism behind this threat level is unknown,
with interspecies analyses preventing a finer assessment of the
influence of weaponry on prey preference, since weaponry can
differ between age and sex classes within species. The implications of differences in preference between prey age and sex
classes on prey population dynamics (FitzGibbon 1990a, 1990b;
Gervasi et al. 2015) are therefore overlooked. Furthermore, by
pooling predator sexes and hunting group sizes, these broadscale studies do not account for differences in size and hunting
behavior between and within predator sexes, despite the fact
that several single-site studies have shown predator hunting
group size to be an important determinant of prey size for lion,
spotted hyaena, and wild dog (Mills 1990; Scheel and Packer
1991; Creel and Creel 2002). The influence of the interaction
between prey morphology and predator social structure on the
prey preferences of large predators has yet to be accounted for
in multisite predator prey preference reviews.
The cheetah is a suitable study species with which to assess
the relationship between prey morphology and predator social
structure in determining prey preference. It is a highly specialized predator evolved for rapid pursuit hunting (Mills and
Harvey 2001), which is believed to impose morphological limitations on the size of prey that can be successfully captured
without injury (Hayward et al. 2006b). The high energy expenditure during such hunts, penalizing unsuccessful attempts,
is reflected by the high hunting success rate (Bertram 1979).
These findings suggest that the cheetah is a highly selective
predator, targeting prey that offer the greatest likelihood of
successful capture without injury. Following optimal foraging
theory (Pyke et al. 1977), we predict that the risk imposed by
horns will lower the upper body size threshold of horned prey
compared to non-horned prey, which is preferred by cheetah.
Furthermore, the cheetah displays a social structure varying
both between and within the sexes (Caro 1994). Female cheetah are solitary except when rearing cubs, while male cheetah
are either solitary or form stable coalitions (Caro 1994). Male
cheetah, being 25% larger than females, have been shown to
hunt more large prey than females (Radloff and du Toit 2004)
and male coalitions hunt more large prey than solitary male
cheetah (Caro 1994). Consistent with these patterns described
at single sites, when assessed across multiple sites and measured in terms of prey preference, we predict that (1) the size
dimorphism between cheetah sexes will result in solitary male
cheetah preferring larger prey and a broader weight range of
prey than female cheetah and (2) a cooperative hunting advantage will result in male coalition cheetah preferring larger prey
and a broader weight range of prey than solitary cheetah of
either sex.
In intact African ecosystems, cheetah coexist with other competitively dominant predators, such as lion and spotted hyaena,
which kleptoparasitize and kill them (Caro 1994). Intraguild
competition has been predicted to promote cheetah preference
for medium-sized prey, which can be consumed before kleptoparasites arrive (Radloff and du Toit 2004; Hayward et al.
2006b). Where the risk of kleptoparasitism is low, cheetah preferred prey weight range has been shown to expand (Bissett and
Bernard 2007), though cheetah in denser habitats that afford
refuge from kleptoparasitism do not prefer larger prey than
those in more open areas (Hayward et al. 2006b). Given these
conflicting findings, it is necessary to account for the influence
of dominant predators in the system when assessing cheetah
prey preference. Using 1,290 cheetah kills from multiple sites
throughout South Africa, we test our predictions by (1) assessing the influence of prey size, prey weaponry, cheetah social
structure, and the density of dominant predators on cheetah
prey preference, and (2) using a novel approach to quantify and
compare the degree of preference displayed by cheetah for different prey sizes. This study is unique in its integrated assessment of the influence of prey morphology (size and horns),
predator social structure (sex and solitary/coalition hunting),
and dominant predator density on cheetah prey preferences
across multiple sites in South Africa.
Materials and Methods
Data sourcing.—The literature was reviewed for publications and dissertations detailing cheetah kill, prey abundance
(census) and, if possible, prey demographic (sex and age ratio)
data from sites in Africa. Unpublished data were sourced from
additional sites. Kill data were derived from incidental observations, observations from tracking cheetah using VHF collars
and continuous follows (Hayward et al. 2006b). Continuous
follows are widely regarded as the superior method of ascertaining the diet of a predator, minimizing the undercounting of
small prey and the inclusion of scavenged prey (Bertram 1979;
Mills 1992). However, because cheetah rarely scavenge and
spend a relatively brief period of time on kills (regardless of
size), there is effectively no difference between the 2 methods
in measuring cheetah diet (Mills 1992). Published data were
augmented with those from the gray literature because few published studies included data in the detail required by this study.
All unpublished and dissertation data were derived from standard, widely used methods (incidental observations and continuous follows—Mills 1992). Data from 9 South African sites,
which varied in rainfall from 315 mm·yr−1 to 875 mm·yr−1, were
obtained (Clements 2013; Supporting Information S1). Limited
availability/access to complete datasets from elsewhere in
Africa prevented a broader geographical scope. Kill data were
separated into 3 cheetah social class categories: female, solitary
CLEMENTS ET AL.—CHEETAH PREY PREFERENCES921
male, and male coalition cheetah according to the sex and number of cheetah observed either making the kill or feeding from
it (Supporting Information S1). As a result of insufficient data
classification at sites with both solitary female cheetah and those
rearing cubs, female cheetah kill data were pooled. At 3 sites,
distinct changes in prey abundance (see Bissett 2007; Clements
2013) necessitated the division of data into 2 time periods
(Supporting Information S1). Temporal partitioning of kill data
is common practice in studies of carnivore feeding ecology, and
is not believed to result in autocorrelation since a fundamental
determinant of whether a prey item is captured is the probability
of the predator encountering that prey item, which varies with
temporal changes in prey abundance (Creel and Creel 2002;
Hayward and Kerley 2005; Hayward et al. 2006b). Prey abundance data were obtained from aerial census data or road count
data. Standard visibility correction factors, used previously in
thicket and savanna ecosystems, were applied to aerial counts
(Rapson and Bernard 2007; Owen-Smith and Mills 2008). No
visibility corrections were applied to road counts (performed
at just 1 site), since information on the density of habitats in
which prey were counted was not available. For 3 sites, prey
demographic data (the ratio of adult males to adult females to
juveniles) could not be obtained and ratios were inferred from
directly adjacent sites in 2 instances and from a site 58 km away
in the 3rd instance. We ensured sites were directly comparable
both in terms of vegetation type and in terms of management
history in order to minimize the influence of these factors on
prey demographic ratios (Supporting Information S2).
Allocating prey masses and determining prey abundances.—
For each listed potential prey species, adult males, adult
females, and juveniles (hereafter referred to as species-demographic-classes) were allocated a standard “species-classmass”, assuming juvenile mass to be 30% of the adult female
mass (Skinner and Chimimba 2005; Supporting Information
S3). Juveniles were considered to be individuals less than a year
old. For warthogs Phacochoerus africanus, adult kills were
rarely sexed, and so all adults were pooled, calculating species-class-mass as an average between adult male and female
body mass (Supporting Information S3). Within each species,
males and females were categorized as horned or non-horned
(Skinner and Chimimba 2005), with all juveniles categorized
as non-horned. Warthogs of both sexes carry tusks and hence
adults were included in the “horned” category. Abundance
of each prey species-demographic-class at each site was calculated using species abundance and demographic data. The
total abundance of censused prey at each site was calculated by
summing the census data for all prey species at that site. Prey
weighing more than 1,200 kg were omitted, since giraffes are
the largest prey species recorded to have been killed (Hayward
et al. 2006b). Carnivores occasionally appear in the kill records
but are rarely consumed (Radloff and du Toit 2004) and were
therefore omitted.
Calculating preferences for prey species-demographicclasses.—To determine how and why a predator selects its
prey, cognizance of prey availability is imperative. If a predator
is presented with 2 (or more) prey items in equal abundance
and selects the 1 more frequently than expected by chance, it
is referred to as a preferred prey item (Johnson 1980). While in
many field studies measuring preference for equally available
food items is not possible, the term preferred prey has been
used to refer to a prey item that is selected (killed) by a predator more frequently than expected based on the prey item’s
relative availability (Hayward and Kerley 2005). If the predator
selects proportionally fewer prey than expected based on the
prey item’s availability, then it is referred to as an avoided prey
item. Prey preference was calculated following previous prey
preference studies (Hayward and Kerley 2005; Hayward et al.
2006b), using the Jacobs’ Index (JI—Jacobs 1974):
JI i =
(ri − pi )
(ri + pi − 2ri pi )
JI standardizes the relationship between prey relative abundance pi (i.e., the proportion p that prey item i makes up of the
total abundance of censused prey at a site) and the proportion
of cheetah kills that prey item i comprises ri, to a value ranging
between +1 and −1, where +1 indicates complete preference
and −1 indicates complete avoidance. For each cheetah social
class, JI values were calculated for each prey species-demographic-class at each site.
Assessing drivers of prey preference.—We used generalized
linear mixed models (GLMMs) to assess whether prey size,
cheetah social class, prey weaponry, and the density of dominant predators influenced cheetah preference for each prey species-demographic-class. JI values are bounded, non-normal,
and overdispersed; we therefore fitted the GLMMs using a
negative binomial distribution (Zuur et al. 2009). Models based
on this distribution require an integer predictor variable, and
so we allocated JI values into 0.1 interval bins and allocated
each bin an integer value representing degree of preference,
commencing at 1 for maximum prey avoidance (bin −1 ≤ JI <
−0.9) and terminating with 20 for maximum prey preference
(bin 0.9 ≤ JI < 1). We combined data from all sites and timeperiods; including site, and sample-period nested within site,
as random effects. We developed a global model that included
prey mass, prey weaponry, cheetah social class, and the combined density of lion and spotted hyaena at the site as fixed
effects. Since we predicted prey weaponry, cheetah social class
and the density of other large predators would interact with
prey mass to influence prey preference, these 2-way interactions were included in the global model. Given the potential
biases arising from applying visibility correction factors to
aerial but not road census data, we further included census
method as a methodological predictor. We generated 12 nested
models by removing combinations of fixed effects and interactions from the global model, while keeping the biological
relevance of the model in mind and always including the methodological predictor. Akaike’s Information Criterion (AIC) was
used for model selection, where models with a change in AIC
greater than 2 (when compared to the best model) were considered to be less informative than the best model (Akaike 1974;
Burnham and Anderson 2002). The best model was compared
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to the null (intercept only) model using a likelihood ratio test
in order to assess whether the predictor variables significantly
increased model fit. Prior to model fitting, we examined the
fixed effects for multicollinearity to avoid correlation among
covariates. Plots of fitted and observed values and residuals
were examined for deviations from the assumptions regarding
homogeneity and normality (Zuur et al. 2009), and as a result
prey mass was log-transformed. Models were run using the R
package “lme4” (Bates et al. 2014).
Quantifying preferred prey weight ranges.—Prey weaponry
and predator sociality were significant predictors of cheetah
prey preference (see “Results”). We therefore assessed cheetah prey weight preferences by distinguishing between horned
and non-horned prey and solitary and coalition cheetah (pooling solitary male and female cheetah kills). As the density of
dominant predators influenced cheetah prey preference (see
“Results”), we excluded sites in our subsequent analyses where
dominant predators were absent (resulting in 879 kill records
for the subsequent analyses).
A mean JI value across sites was calculated for each prey
species-demographic-class with 2 or more site-specific JI
values. These mean JI values (Supporting Information S3)
were standardized (+1 to ensure non-negative values) and
used as an index of prey preference. To determine solitary
and coalition cheetah prey size preference for horned and
non-horned prey, segmented generalized linear models were
used (Hudson 1966; Muggeo 2008) as they provide a statistically robust means of detecting changes in prey preference
as a function of prey mass. Following Clements et al. (2014),
prey species-class-masses were ranked from the lightest to
the heaviest and allocated corresponding incremental integer values (mass-ranks; Supporting Information S3) in order
to control for uneven size distribution of prey species. For
each prey species-class-mass, a corresponding cumulative
JI+1 value was calculated, commencing at the prey speciesclass-mass with a mass-rank of 1. Mass-ranks were plotted
against cumulative JI+1 values and break-points were estimated using segmented models (Muggeo 2008). Starting
with a linear model, we incrementally increased the number
of break-points in each segmented model, and selected the
optimum number of break-points (if any) using AIC (Akaike
1974). Mass-ranks, at which the best-fit segmented model
detected break-points in the relationship between mass and
preference, were converted back into corresponding prey
species-class-masses in order to identify prey weight ranges
of differing preference.
Prey weight ranges of differing preference were thereafter assessed for prey preference/avoidance by calculating the
JI of each prey weight range at each site listed in Supporting
Information S1 (Clements et al. 2014). The mean JI value of
each prey weight range across sites was tested for significant
preference or avoidance using a single sample t-test against
a mean of zero where data conformed to the assumptions of
normality, and a Wilcoxon signed-rank test where data did
not. Prey weight ranges found to be either preferred (mean
JI significantly greater than 0) or killed relative to their abundance (mean JI not significantly different from 0) are together
referred to as “accessible” weight ranges. A mean JI value
significantly less than zero indicated an avoided prey weight
range. Segmented models were performed using the R package
“segmented” (Muggeo 2008).
Female size and the presence of horns in South African
antelope species.—We generated a list of the antelope species (family Bovidae) indigenous to South Africa and recorded
the mass and presence/absence of horns for the adult female
of each species (Supporting Information S4; Skinner and
Chimimba 2005). For each mass, we determined, according
to our preference results, whether a prey individual with such
a mass would be avoided by cheetah if it (1) had horns and
(2) did not have horns. We then allocated antelope into 1 of
2 categories: (1) antelope with adult females of a mass where
only non-horned prey are accessible to solitary or coalition
cheetah and (2) antelope with females of a mass where both
horned and non-horned prey are accessible to solitary and
coalition cheetah. The number of antelope species with horned
and non-horned adult females in each category was summed.
We excluded antelope with horned adult females weighing
more than 313 kg, since no non-horned prey weigh more than
this (Supporting Information S3), thus preventing comparison. Difference in the number of species with horned versus
non-horned females in each category was assessed using a chisquare test. Statistical analyses were performed in the statistical programme R (R Development Core Team 2013), at a
significance level of 0.05.
Results
The best model predicting cheetah prey preference (see
Supporting Information S5 for the top 4 candidate models)
had a significantly improved fit when compared with the null
model (χ2 = 215.04, d.f. = 10, P < 0.001). The best model
included a significant negative relationship between prey
mass and prey preference (Table 1). This relationship was
stronger when prey had horns, depicted by a significant negative interaction between prey mass and the presence (compared with absence) of horns (Table 1). The relationship
between prey mass and prey preference was weaker for male
coalition cheetah, compared with female cheetah, depicted
by a significant positive interaction between prey mass and
male coalition (compared with female) cheetah (Table 1).
There was no difference in the relationship between prey
mass and prey preference for female and solitary male cheetah, evidenced by the nonsignificant interaction between
prey mass and solitary male (compared with female) cheetah (Table 1). Finally, there was a significant negative relationship between the density of dominant predators and prey
preference, and census method did not influence prey preference (Table 1).
Segmented models revealed changes in the relationship
between prey weight and degree of cheetah prey preference
at sites where dominant predators were present (Fig. 1). For
solitary and male coalition cheetah, preferred weight ranges
of prey were only evident in non-horned prey, whereas horned
prey were killed relative to their abundance or avoided (Fig. 2;
CLEMENTS ET AL.—CHEETAH PREY PREFERENCES923
Table 1.—Best generalized linear mixed model (AIC = 3602.9) of cheetah prey preference, as a function of prey mass, prey weaponry, cheetah
social class, and density of lion and spotted hyaena. (: represents an interaction between 2 fixed effects.) Results include coefficient estimate β,
standard error SE(β), associated Wald’s z-score β/SE(β), and significance level P for all predictors. AIC = Akaike’s Information Criterion.
β
SE(β)
z
P
4.146
−1.228
1.310
−0.602
−1.524
−1.956
−0.804
0.319
1.023
0.051
0.328
0.169
0.418
0.461
0.503
0.573
0.213
0.242
0.262
0.144
12.642
−7.252
3.126
−1.305
−3.029
−3.411
−3.765
1.318
3.915
0.355
< 0.001*
< 0.001*
0.002*
0.19
0.002*
< 0.001*
< 0.001*
0.19
< 0.001*
0.723
Fixed effect
Intercept
log(prey_mass)
prey_horned versus prey_not_horned
solitary_male_cheetah versus female_cheetah
coalition_cheetah versus female_cheetah
density_dominant_predators
log(prey_mass):prey_horned versus log(prey_mass):prey_not_horned
log(prey_mass): solitary_male_cheetah versus log(prey_mass): female_cheetah
log(prey_mass): coalition_cheetah versus log(prey_mass): female_cheetah
census_method_road versus census_method_aerial
* Significant.
Cumulative Jacobs Index + 1
Prey mass (kg)
10
9
8
7
6
5
4
3
2
1
0
14
12
10
8
6
4
2
0
11
62
0
5
16
150
Solitary cheetah - horned prey
AIC = 13, n = 26
15
20
25
30
10
42
1192
179
365
1192
Coalition cheetah - horned prey
AIC = 10, n = 21
0
5
10
15
20
25
20
18
16
14
12
10
8
6
4
2
0
20
18
16
14
12
10
8
6
4
2
0
4
8
0
145
313
Solitary cheetah - non-horned prey
AIC = 19, n = 28
10
15
20
25
30
5
0
48
31
18
5
62
119
313
Coalition cheetah - non-horned prey
AIC = 10, n = 22
10
15
20
25
Prey mass rank
Fig. 1.—Segmented relationship between the mass-rank of each prey species-demographic-class and predator preference, for solitary and male
coalition cheetah. Preference is indicated by cumulative Jacobs’ Index +1 value. Actual prey masses that correspond to the lowest, break-point,
and highest prey mass-ranks are indicated above the figures.
Table 2). For solitary cheetah, the presence of horns decreased
the weight threshold above which prey are avoided from
145 kg for non-horned prey (JI>145 kg = −0.91 ± 0.05, P < 0.001)
to 62 kg for horned prey (JI62–150 kg = −0.85 ± 0.10, P = 0.02;
JI>150 kg = −0.96 ± 0.02, P = 0.02; Fig. 2; Table 2).
Male coalition cheetah did not exhibit a weight threshold above which non-horned prey are avoided (Fig. 2). Adult
male zebra, weighing 313 kg, were the largest non-horned
prey present at any of the study sites and male coalition cheetah killed prey up to this weight relative to prey abundance
(JI119–313 kg = −0.22 ± 0.23, P = 0.41; Fig. 2; Table 2). This translated into male coalitions killing non-horned prey relative to their
abundance at weights up to 168 kg greater than solitary cheetah
(Fig. 2; Table 2). Male coalition cheetah avoided horned prey
above a weight threshold of 179 kg (JI179–365 kg = −0.85 ± 0.09,
P < 0.001; JI>365 kg = −1 ± 0; Fig. 2; Table 2), thereby killing
horned prey relative to their abundance at weights up to 117 kg
greater than solitary cheetah (Fig. 2; Table 2).
There were significantly more antelope species with horned
adult females in the weight range where horns result in avoidance by cheetah, than there were antelope species with horned
adult females in the weight range where the females are accessible to cheetah irrespective of horn presence/absence (χ2=
8.27, d.f. = 1, P < 0.01).
Discussion
This study highlights the influence of prey morphological
traits (size and weaponry), predator behavioral traits (sociality), as well as the density of dominant predators on a large
predator’s prey preference. Site-specific prey preferences
may be further influenced by prey species composition and
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JOURNAL OF MAMMALOGY
abundance, ecology (e.g., prey scarcity), behavior, and its
relation to sex (e.g., group defense; males tending to be more
solitary with reduced group vigilance), and how the prey
individual responds to the landscape of fear, which can also
depend on available habitat (Laundré et al. 2001; Hayward
2011). Similarly, measures of prey preference can be influenced by detectability of both kills and prey communities
during census, which may vary as a function of sampling
technique, herd size, and habitat (which varies seasonally).
As this study is based on a multisite, multispecies analysis,
for a prey weight range to be found to be preferred or avoided,
it must be so across a diversity of prey communities and habitats. This study therefore presents patterns of the influence of
prey morphology and predator social structure on predator
prey preference that are robust across a multitude of habitats,
climates, and prey communities. These trends should serve
as a useful departure point from which hypotheses regarding
predator–prey interactions at a finer scale can be formulated.
Preferred
320
Relative
Avoided
Prey mass (kg)
280
240
200
160
120
80
40
0
Horned
Non-horned
Solitary cheetah
Horned
Non-horned
Coalition cheetah
Fig. 2.—The weight ranges of horned and non-horned prey that are
preferred, killed relative to their abundance, and avoided by solitary
and male coalition cheetah. (Weight ranges preferred and killed relative to their abundance are together referred to as “accessible prey
weight ranges.”)
The influence of prey morphology on cheetah prey
preference.—Upper prey size thresholds were identified above
which large body size serves to provide protection to prey from
cheetah predation. This supports previous studies on predator–prey size relationships (Sinclair et al. 2003). Notably, this
study further shows that the influence of prey size and the
presence of horns interact, lowering the mass threshold above
which prey is avoided. Our findings therefore provide quantitative evidence that horns serve as a successful antipredatory
mechanism, particularly in prey that are on the cusp of being
too large to be predated. This further provides support for the
prediction that larger species, by being better able to defend
themselves against predators as well as by being more exposed,
should benefit more from having defensive weaponry than
smaller species (Packer 1983; Stankowich and Caro 2009).
In all antelope species, males possess horns that are widely
thought to have evolved for territorial disputes or mate acquisition (Geist 1966; Janis 1982). In contrast, the presence of horns
in females is highly variable across antelope species and its
evolution has been attributed to an antipredatory mechanism,
the defense of territories against other females, and as a buffer
against aggression toward male offspring by dominant males
(Packer 1983; Estes 1991; Stankowich and Caro 2009). The
occurrence of horned females is significantly greater in antelope species where females are large enough to escape into the
avoided weight range by having horns, supporting the prediction that predation is an evolutionary driver of horns in large
female antelope.
Small prey also benefit from horns. While not influencing
the accessibility of smaller prey to cheetah, horns do influence
preference within this accessible prey weight range. Small prey
size, independent of horn presence/absence, limits absolute
protection from cheetah predation, but the presence of horns
reduces predation below levels experienced by non-horned prey
of similar size. Furthermore, horns in small-sized prey may
serve to reduce predation by predators smaller than cheetah,
such as black-backed jackal Canis mesomelas. The influence
of prey size and horns on cheetah prey preference shows that,
Table 2.—The prey mass-ranks at which segmented models revealed break-points in cheetah prey preference, with corresponding prey weight
ranges and preference statistics. JI = Jacobs’ Index.
Cheetah
Prey
weaponry
Preference
Mass-rank
range
Corresponding
weight range (kg)
JI
Significance
Solitary
Horned
Relative
Avoided
Avoided
Preferred
Relative
Relative
Avoided
Relative
Relative
Avoided
Avoided
Relative
Relative
Preferred
Relative
≤ 8.3
8.3–15.1
> 15.1
≤ 11.7
11.7–17.2
17.2–23.5
> 23.5
≤ 3.4
3.4–11.5
11.5–17.5
> 17.5
≤ 5.9
5.9–12.2
12.2–16.6
> 16.6
≤ 62
62–150
> 150
≤ 31
31–48
48–145
> 145
≤ 42
42–179
179–365
> 365
≤ 18
18–62
62–119
> 119
−0.19 ± 0.14
−0.85 ± 0.10
−0.96 ± 0.02
0.35 ± 0.14
0.12 ± 0.22
0.21 ± 0.12
−0.91 ± 0.05
−0.17 ± 0.42
0.03 ± 0.14
−0.85 ± 0.09
−1 ± 0
0.00 ± 0.27
−0.15 ± 0.12
0.87 ± 0.01
−0.22 ± 0.23
t = 1.32, d.f. = 6, P = 0.24
W = 0, n = 7, P = 0.02
W = 0, n = 7, P = 0.02
t = 2.46, d.f. = 6, P = 0.049
t = 0.54, d.f. = 6, P = 0.61
t = 1.69, d.f. = 6, P = 0.14
t = −17.65, d.f. = 6, P < 0.001
t = −0.41, d.f. = 4, P = 0.72
t = 0.21, d.f. = 4, P = 0.85
t = −9.25, d.f. = 4, P < 0.001
n = 6
t = 0.00, d.f. = 4, P = 0.99
t = −1.26, d.f. = 4, P = 0.28
t = 162.03, d.f. = 4, P < 0.001
t = −0.92, d.f. = 4, P = 0.41
Non-horned
Male coalition
Horned
Non-horned
CLEMENTS ET AL.—CHEETAH PREY PREFERENCES925
in the face of predation by cheetah, it is better for a prey individual to be big and horned. In multipredator systems, size- and
horn-derived protection from smaller predators such as cheetah
would not necessarily provide protection from predation by
larger predators that hunt larger prey (e.g., lion—Radloff and
du Toit 2004; Owen-Smith and Mills 2008). However, while
a large body size and the presence of horns may not eliminate
the risk of predation for most prey species, it will determine
the suite of predators that the species is vulnerable to, with a
bigger size and the presence of horns reducing total predation
pressure. Therefore, predation pressure, even in multipredator
ecosystems, could have contributed to the selection for large
body size and the presence of horns in prey species.
The influence of cheetah sex and social structure on
cheetah prey preference.—Cheetah preference for prey of a
given mass did not differ between female and solitary male
cheetah, suggesting that sexual dimorphism in cheetah is not
sufficient to facilitate a clear hunting advantage to the slightly
larger males when the latter are solitary. While this is contrary to
the finding of Radloff and du Toit (2004), the majority of male
cheetah data used in their study were from coalitions of cheetah, not solitary males (F. Radloff, Cape Peninsula University of
Technology, pers. comm.). Therefore, while Radloff and du Toit
(2004) only compared cheetah sexes and not group sizes, their
results may have been biased by group hunting in males, since
we show that male coalition cheetah have a larger weight range
of prey accessible to them than solitary cheetah.
Drivers of sociality within the order Carnivora have been
debated, including the benefits of strength in numbers for
defense of cubs, kills, and territories and the ability to hunt and
kill larger prey cooperatively (Macdonald 1983; Packer et al.
1990; Caro 1994). For cooperative hunting to be a driver of
sociality, groups members must accrue greater per capita forage returns by hunting as a group than alone, and food intake
must be a key factor affecting fitness (Caro 1994). Ultimately,
the costs of sociality, such as food and mate sharing (Kruuk
1975; Caro and Collins 1986; Packer et al. 1990; Caro 1994),
need to be outweighed by the benefits. Costs and benefits will
vary, depending for example on the availability and density of
food and the risks of accessing, capturing, and defending it
(Macdonald 1983; Radloff and du Toit 2004). While acknowledging that sociality in predators is therefore likely to be the
result of several interacting variables, this study shows that
coalition males derive increased resource access as a direct
benefit of their sociality.
Female cheetah with cubs will require more food to meet
increased energetic demands, and may accomplish this by
increasing their kill rate, as seen in leopard and puma Puma
concolor (Bothma and Coertze 2004; Laundré 2008), or hunting more prey in the upper prey size limits imposed on solitary hunters (Laurenson 1995). We did not investigate this, but
with the accumulation of datasets distinguishing between kills
of solitary and cub-rearing females, these predictions can be
tested.
The influence of dominant predators on cheetah prey
preference.—It has been predicted that a reduction in
kleptoparasitism may result in an expansion of a cheetah’s
prey weight preferences (Radloff and du Toit 2004; Bissett
and Bernard 2007). Contrary to this prediction, we show that
the density of lion and spotted hyaena does not influence
prey weight preferences of cheetah. The density of dominant
predators does, however, influence the number of prey speciesdemographic-classes that are preferred. The reduction in prey
preference with increasing dominant predator density, independent of prey mass, suggests that at higher densities of dominant
predators, cheetah diet becomes more specialized. This functional response may be as a result of cheetah avoiding certain
habitats where dominant predators more commonly occur,
or within which cheetah are more visible to dominant predators (Durant 1998; Vanak et al. 2013). This would represent a
spatially focused mechanism for mesopredator release in the
absence of lion and spotted hyaena (Prugh et al. 2009). We did
not quantify the cheetah’s preferred and accessible prey weight
ranges at sites devoid of dominant predators, since no data at
such sites were available for male coalition cheetah. However,
as the density of dominant predators does not influence cheetah
prey mass preference or avoidance, the preferred and accessible
prey weight ranges of cheetah, quantified in this paper, should
be reliable independent of the presence or absence of dominant
predators.
Our findings provide support for the influence of selective
predation on the evolution of horns and body size in prey species, and the influence of expanded resource access on the evolution of sociality in predator species. With the diverse range of
social systems found in large predator species, and the varied
size and weaponry array found in prey species, these findings
should allow for hypotheses to be developed and tested regarding predator prey preferences, and thereby predator–prey interactions and their evolutionary drivers, in other predator–prey
communities.
Acknowledgments
We thank T. Caro, N. Owen-Smith, M. Hayward, and 2 anonymous reviewers for their useful comments on an earlier version of this paper. We thank C. Bissett, T. Burke, M. Grover,
E. Larson, J. O’Brien, S. Razzaq, and R. Slater for providing
data. HSC was funded by Samara Private Game Reserve, the
National Research Foundation (NRF), and Nelson Mandela
Metropolitan University. CJT was funded by the NRF and a
Claude Leon Postdoctoral Fellowship.
Supporting Information
The Supporting Information documents are linked to this
manuscript and are available at Journal of Mammalogy online
(jmammal.oxfordjournals.org). The materials consist of data
provided by the author that are published to benefit the reader.
The posted materials are not copyedited. The contents of all
supporting data are the sole responsibility of the authors.
Questions or messages regarding errors should be addressed
to the author.
926
JOURNAL OF MAMMALOGY
Supporting Information S1.—Sites and sources of data used
in this study.
Supporting Information S2.—Habitat and management
details for sites for which prey demographic data were inferred.
Supporting Information S3.—Prey species-class-masses,
mass-ranks, and mean Jacob’s Index (JI) values of speciesdemographic-classes used in segmented model analyses,
for solitary and coalition cheetah, separated into horned and
non-horned prey.
Supporting Information S4.—South African antelope
(Bovidae) species and adult female masses.
Supporting Information S5.—Formulas and model comparison statistics for the 4 best-fit generalized linear mixed models
predicting the degree of cheetah prey preference for a given
prey species-demographic-class (Pr = degree of prey preference; M = log(prey mass); H = prey weaponry; C = cheetah
social group; D_LH = density of lion and spotted hyaena;
X = census method; : = interaction between 2 fixed effects).
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Submitted 1 June 2015. Accepted 26 January 2016.
Associate Editor was I. Suzanne Prange.