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Prey species may adjust their use of antipredator behaviours to counter the hunting strategies (e.g. ambush versus cursorial) and the level of risk imposed by different predators. Studies of suites of behaviours across well-defined contrasts of predation risk and type are rare, however. Here we explored the degree to which six herbivore species adjusted their antipredator behaviours to two predator treatments (lion, Panthera leo, versus cheetah, Acinonyx jubatus, and wild dogs, Lycaon pictus). We focused on prey behaviour (vigilance, grouping, temporal use) at waterholes. We predicted that if the hunting strategy of the predator was the key driver of antipredator behaviour, ambushing lions would elicit a greater response than cursorial cheetah and wild dogs. Alternatively, if predator preference was the main driver, then we expected prey species to adjust their antipredator behaviours in response to the predators that specifically target them (i.e. preferred prey of the different predators). Overall, we found that the herbivores maintained greater vigilance, generally moved in larger groups and used waterholes less at dawn, at dusk or at night (when lions are active) when exposed to the potential threat of ambushing lions. However, some species within the accessible prey range of cheetah and/or wild dogs (i.e. red hartebeest, warthog, gemsbok) moved in larger groups when exposed to these predators. Yet, the magnitude of the differences in group size for these herbivores were small. Thus, we suggest that, overall, the potential threat of ambushing lions was the main driver of antipredator behaviour around waterholes, probably determined by prey weight preference and the possibility of being ambushed.
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Herbivores employ a suite of antipredator behaviours to minimize risk
from ambush and cursorial predators
Douglas F. Makin
, Simon Chamaill
, Adrian M. Shrader
School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg, South Africa
Centre d'Ecologie Fonctionnelle et Evolutive, UMR 5175, CNRS, Universit
e de Montpellier, Universit
e Paul-Val
ery MontpelliereEPHE, Montpellier, France
article info
Article history:
Received 7 November 2016
Initial acceptance 11 January 2017
Final acceptance 2 March 2017
MS. number: 16-00973R
group size
hunting strategies
predatoreprey interactions
prey preferences
temporal activity
Prey species may adjust their use of antipredator behaviours to counter the hunting strategies (e.g.
ambush versus cursorial) and the level of risk imposed by different predators. Studies of suites of be-
haviours across well-dened contrasts of predation risk and type are rare, however. Here we explored
the degree to which six herbivore species adjusted their antipredator behaviours to two predator
treatments (lion, Panthera leo, versus cheetah, Acinonyx jubatus, and wild dogs, Lycaon pictus). We
focused on prey behaviour (vigilance, grouping, temporal use) at waterholes. We predicted that if the
hunting strategy of the predator was the key driver of antipredator behaviour, ambushing lions would
elicit a greater response than cursorial cheetah and wild dogs. Alternatively, if predator preference was
the main driver, then we expected prey species to adjust their antipredator behaviours in response to the
predators that specically target them (i.e. preferred prey of the different predators). Overall, we found
that the herbivores maintained greater vigilance, generally moved in larger groups and used waterholes
less at dawn, at dusk or at night (when lions are active) when exposed to the potential threat of
ambushing lions. However, some species within the accessible prey range of cheetah and/or wild dogs
(i.e. red hartebeest, warthog, gemsbok) moved in larger groups when exposed to these predators. Yet, the
magnitude of the differences in group size for these herbivores were small. Thus, we suggest that, overall,
the potential threat of ambushing lions was the main driver of antipredator behaviour around water-
holes, probably determined by prey weight preference and the possibility of being ambushed.
©2017 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Prey possess a whole suite of behaviours that they may employ
to reduce predation risk (Caro, 2005; Lima &Dill, 1990). In partic-
ular, vigilance and grouping are exible behaviours that can be
used to reduce risk, although they come with associated costs. For
example, increased vigilance allows individuals to detect attacks
earlier, providing a greater chance of escaping (Lima &Bednekoff,
1999), but often reduces food intake rate (Fortin, Boyce, Merrill, &
Fryxell, 2004). Living in larger groups allows individuals to poten-
tially benet from dilution, collective vigilance and/or deterrence
effects (Beauchamp, 2003; Schmitt, Stears, Wilmers, &Shrader,
2014), but could increase intragroup competition (Krause &
Ruxton, 2002). Because of these costs, prey are not expected to
always display a full suite of antipredator behaviours, but rather to
nely adjust antipredator behaviours to the level of risk, by prior-
itizing certain behaviours over others (e.g. vigilance, grouping,
temporal shifts; Creel, Schuette, &Christianson, 2014).
Predation risk varies both temporally and spatially across the
landscape. This translates into a landscape of fear(Laundr
andez, &Altendorf, 2001) that is shaped by differences in
the prey's perception of the likelihood of meeting a specic pred-
ator (e.g. predator density, similar landscape use between predator
and prey, shared time of activity), and of the likelihood of being
killed when attacked (i.e. threatof the predator). However, as not
all predators are the same, prey species probably adjust the extent
to which they utilize different antipredator behaviours (e.g. vigi-
lance levels, group size) in response to different predators or
predator combinations.
One factor that probably greatly inuences antipredator stra-
tegies is the hunting strategy of a predator. For instance, large
mammalian predators are usually classied as either cursorial or
stalking/ambush predators. Cursorial predators roam over large
areas looking for prey, and then approach prey rapidly and silently
when found (Creel &Creel, 2002; Pomilia, McNutt, &Jordan, 2015).
As a result, their distribution in the landscape is generally unpre-
dictable, and thus prey tend not to associate specic places with
predation risk from these species (see discussion in Preisser,
Orrock, &Schmitz, 2007). In contrast, ambush predators rely on
*Correspondence: D. F. Makin, School of Life Sciences, University of KwaZulu-
Natal, Private Bag X01, Scottsville 3209, Pietermaritzburg, South Africa.
E-mail address: (D. F. Makin).
Contents lists available at ScienceDirect
Animal Behaviour
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0003-3472/©2017 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Animal Behaviour 127 (2017) 225e231
places where the likelihood of meeting prey is high, relying on
small-scale vegetation cover, rather than speed, to approach prey
(Preisser et al., 2007). Thus, areas attracting prey usually also attract
ambush predators, and thus prey should increase their antipredator
behaviour when using these areas (Valeix, Fritz, et al., 2009). For
example, within the arid and semiarid environments that we
studied here, water sources attract both large mammalian herbi-
vores and their ambush predators such as lions, Panthera leo (Ogutu
et al., 2014; Thaker et al., 2011; Valeix et al., 2010; de Boer et al.,
In addition to a predator's hunting strategy, prey species prob-
ably also consider the degree of threat posed by a specic predator.
Predators tend to target prey species within specic body size
ranges (for lion: Clements, Tambling, Hayward, &Kerley, 2014;
Hayward, 2006; Hayward, Hayward, Tambling, &Kerley, 2011).
Thus, some predators will be more of a threat than others. For
example, lions are more likely to attack a 290e340 kg zebra, Equus
quagga, than a 40e70 kg impala, Aepyceros melampus (Hayward &
Kerley, 2005). As a result, prey species should increase the extent
to which they utilize specic behaviours (e.g. increase vigilance
levels) in response to their primary predators, compared to more
peripheral predators. Yet, an overarching factor that greatly in-
uences predation risk is the overlap in the activity patterns of
predators and prey (i.e. whether they are nocturnal or diurnal;
Kronfeld-Schor &Dayan, 2003). To minimize contact with preda-
tors, prey species can shift their temporal use of the landscape to
periods when predators are least active. For example, in Hwange
National Park, Zimbabwe, most ungulate species appear to avoid
coming to drink at night when lions are in the vicinity of the
waterholes (Valeix, Fritz, et al., 2009).
Here we explored the degree to which prey species adjust their
antipredator strategies in response to different predators. We
focused our observations at waterholes in a semiarid ecosystem as
a model of key interaction areas between predators and prey, and
studied the antipredator behaviour (grouping, vigilance, time of
use) of six large herbivore species (i.e. eland, Taurotragus oryx;
gemsbok, Oryx gazella; plains zebra, red hartebeest, Alcelaphus
buselaphus caama; warthog, Phacochoerus africanus; blue wilde-
beest, Connochaetes taurinus) at these waterholes. We did this in
two sections of the same reserve that were separated by fences, one
with only lions (ambush predators), the other with cheetah, Aci-
nonyx jubatus, and wild dogs, Lycaon pictus (both cursorial preda-
tors) and no lions.
In many ecosystems, lions select and kill in areas close to water
(Ogutu et al., 2014; Thaker et al., 2011; Valeix et al., 2010; de Boer
et al., 2010). Cheetah and wild dog may also do this, but their
presence near waterholes might be less predictable as their
cursorial hunting strategies probably increase their use of areas
away from water sources, more so than lions (e.g. Ndaimani,
Tagwireyi, Sebele, &Madzikanda, 2016). Thus, we predicted that
if hunting strategy was a key driver of prey a ntipredator behaviour,
lions would elicit a greater antipredator response from prey spe-
cies than the less spatially predictable cheetah and wild dogs. This
could be through all the prey species changing their antipredator
behaviours (e.g. increased vigilance and larger groups) and/or
adjusting their temporal activity patterns more in response to li-
ons than to cheetah and wild dogs. Alternatively, if antipredator
behaviours of prey species are driven more by prey preferences of
predators, then we would expect individual prey species to change
their antipredator behaviours more in response to the predators
that specically target them (i.e. prey falling within the predator's
preferred prey weight range) than if the prey species falls outside
the predator's prey weight range. This could then result in species-
specic differences both within and between the predator
Ethical Note
The University of KwaZulu-Natal approved all aspects of the
research design (Ethics code: 058/14/Animal).
Data Collection
We conducted our study in Tswalu Kalahari Reserve (Tswalu
hereafter) in the Northern Cape, South Africa (S 27
and E
) from October 2013 to April 2015. The fenced reserve
encompasses 1000 km
of restored farmland (Cromhout, 2007)
located in the southern Kalahari (Roxburgh, 2008). Tswalu has a
mean annual rainfall of 250 mm, with an extended dry season
lasting from May to September/October when there is less than
10 mm rainfall (Roxburgh, 2008). Large mammalian herbivores
found in the reserve include kudu, Tragelaphus strepsiceros,
springbok, Antidorcas marsupialis, gemsbok, eland, sable, Hippo-
tragus niger, zebra, red hartebeest, warthog and wildebeest.
Tswalu is divided into two adjacent sections which support
different large predator populations, but are separated by about
50 m comprising a road and two predator fences. The western
section of the reserve (200 km
) contains lion (N¼24), while the
eastern section (800 km
) contains populations of cheetah (N~10)
and wild dog (N¼14). Habitat types across both sections are
similar, made up of Digitaria polyphylla-dominated hills, Stipagrostis
uniplumis-dominated plains and valleys and Anthephora pubescens-
dominated sand dunes (see Van Rooyan, 1999). Likewise, both
sections have a similar mean annual rainfall (mm), with
326 ±40 mm falling within the western section compared to
345 ±42 mm within the eastern section recorded over a 9-year
period. We limited data collection to the herbivore species that
occurred in both sections of the reserve. These included eland,
gemsbok, zebra, red hartebeest, warthog and wildebeest. The her-
bivores living in the two sections face different levels of predation
risk due to the hunting strategy employed, their activity patterns
and the prey weight preferences of the different predator species
(Hayward &Slotow, 2009; Hayward et al., 2007). Lion are stalk and
ambush predators that are predominantly active at night, while
cheetah and wild dogs are mostly diurnal and hunt by chasing
down their prey (Hayward &Somers, 2009). Comparing prey
weight preferences from a multisite analysis, Clements et al. (2014)
determined that lion have an accessible prey weight class range of
32e632 kg and therefore all six herbivores species monitored in
our study fall within their prey weight range. However, they tend to
prefer prey weights of 92e632 kg (Clements et al., 2014) with
wildebeest and zebra often preferentially targeted over other prey
(Sinclair, Mduma, &Brashares, 2003). In contrast, cheetah and wild
dogs have smaller accessible prey weight ranges of 14e135 kg (with
a peak weight mode of 36 kg; Hayward, Hofmeyr, O'Brien, &Kerley,
2006) and 10e289 kg (peak weight modes of 16e32 kg and
120e40 kg; Hayward, Hofmeyr, et al., 2006), respectively. There-
fore, only warthog and red hartebeest fall within the accessible
range of cheetah, while all the herbivores, except eland, fall within
the accessible prey range of wild dogs (Clements et al., 2014).
However, although warthog fall within the accessible prey range of
both cheetah and wild dogs, they are generally avoided (Clements
et al., 2014;Hayward, Hofmeyr, et al., 2006). Despite discrep-
ancies in prey weight range preferences, cheetah and wild dogs
have the highest recorded dietary overlap (73.5%; Hayward &
Kerley, 2008) of the large African predator guild and therefore
present a signicant cumulative predation risk to shared prey
species. Within Tswalu, lion prey upon wildebeest and gemsbok
(Roxburgh, 2008), while cheetah prey on red hartebeest and
D. F. Makin et al. / Animal Behaviour 127 (2017) 225e231226
springbok, and wild dogs prey on kudu, red hartebeest and impala
(Makin, n.d).
Throughout the study, all three predators were observed uti-
lizing waterholes. Moreover, lions were active at waterholes pre-
dominantly at night and during crepuscular periods (80% of
observations). In contrast, cheetah and wild dogs were more
diurnal, visiting waterholes during the crepuscular periods and
during the day (65% and 70% of observations, respectively).
To assess the antipredator strategies used by the different prey
species in response to the different predators, we deployed Bush-
nell video camera traps with heat-motion sensors at ve water-
holes in the cheetah and wild dog section and three waterholes in
the lion section. Camera traps were attached to trees 1 m above the
ground. This ensured that each camera's eld of view extended
from the ground up to over 2.5 m. Camera traps were placed so that
they had a clear view of the entire waterhole. This enabled all in-
dividuals visiting the waterholes to be recorded. Only videos
showing clearly discernible individuals were included in the data
We limited the chances of collecting data from the same indi-
vidual multiple times within a single recording event, by rst
noting when individuals left the eld of view. We then waited
30 min before collecting data from groups of the same species
comprising the same number of individuals (i.e. potentially the
same group) that entered the eld of view (Linkie &Ridout, 2011;
Tambling et al., 2015). Previous studies have suggested that
30 min represents a sufcient trade-off between recording the
same individual multiple times and missing new individuals
(Rovero, Jones, &Sanderson, 2005; Tambling et al., 2015).
We analysed the video camera data recording for (1) herbi-
vores species, (2) time of day (day: 0600e1700; crepuscular:
0400e0600 and 1700e1900; night: 1900e0400), (3) typical group
size (i.e. the reection of the animal's rather than the human
observer's experience within the group; calculated as G¼(PNi
(N), where the sum of the squares of all individuals in all groups
) is divided by the total number of individuals seen (N);
Jarman, 1974; Reiczigel, Lang, R
ozsa, &T
esz, 2008), (4)
predator section (lion versus cheetah and wild dogs), and (5)
proportion of time individual herbivores within groups were
vigilant at waterholes. We followed the approach of P
eriquet et al.
(2010) where vigilance was monitored for a focal animal within
the centre of each group. We did this as central individuals are
less likely to be killed than individuals on the periphery; thus, any
increase in vigilance by central individuals is likely to reect an
increase in vigilance for all individuals within the group. We
considered an animal to be vigilant when it stood in an upright
position, head alert and actively scanning with ears held forward.
All individuals recorded were adult members of the group. As
females with juveniles will maintain higher levels of vigilance to
protect dependent offspring we focused on the vigilant responses
of females without juveniles (P
eriquet et al., 2010). Additionally,
the study was conducted following a severe drought year and
therefore there was little recruitment into the different herbivore
populations during this period, with most breeding groups con-
sisting of only adults and subadults from the previous year (Makin
Pers. Obs.).
We recorded the proportion of time each individual spent
vigilant at waterholes over a 10 min period or over the entire time
herbivore groups were drinking at a waterhole if it was less than
10 min. We dened both these time periods as an observation.
Vigilance was recorded for individuals within groups that were
close to the waterhole (i.e. drinking or standing on the water's
edge). Within the lion section, we recorded 85 wildebeest, 23
eland, 91 gemsbok, 147 zebra, 36 red hartebeest and 88 warthog
observations, while in the cheetah and wild dog section we
recorded 182 wildebeest, 76 eland, 222 gemsbok, 78 zebra, 187 red
hartebeest and 275 warthog observations.
Statistical Analysis
For each herbivore species, we compared the effect of predator
section (i.e. lion versus cheetah and wild dog) and the interaction
between predator section and herbivore species on changes in the
antipredator behaviours of typical group size and proportion of
time spent vigilant using generalized linear models (GLM) with
Poisson and binomial errors, respectively. To keep the model sim-
ple, we did not include group size as a predictor of the proportion of
time spent vigilant. Preliminary analyses showed that there was no
relationship for ve of the six species (all P>0.10), with only red
hartebeest showing a slight positive relationship between indi-
vidual vigilance and increasing group size (z¼3.86, P<0.01), but
this was of a very small magnitude (lion section: y¼0.03xþ0.33;
cheetah and wild dog section: y¼0.03xþ0.11). For each herbivore
species in each predator section, we visually displayed the diel
distribution of visits to waterholes using kernel-based density
plots. In addition, we tested for the statistical signicance of dif-
ferences between predator sections by tting a GLM with Poisson-
distributed errors with the number of herbivore observations
recorded at a waterhole within each time period (night, crepus-
cular, day) as the response variable, and time period and predator
section as explanatory variables, including interactions between
variables. Warthog were not recorded visiting waterholes at night
in the lion section and therefore could not be compared for this
period. All analysis was performed using R 3.21 (R Core Team, 2014)
using the lme4 package (Bates, Maechler, &Bolker, 2012), MASS
package (Venables &Ripley, 2002) and the multcomp package
(Hothorn, Bretz, &Westfall, 2008).
Typical group sizes varied signicantly between herbivore
species (x
¼732.7, P<0.01), between the predator sections
¼51.5, P<0.01) and for the interaction between herbivore
species and the different predator sections (x
¼51.4, P<0.01).
Overall, group size did not differ between the sections for eland
(z¼1.7 2 , P¼0.08; Fig. 1a). Zebra (z¼2.12, P¼0.03) and wilde-
beest (z¼5.05, P<0.01) maintained larger groups in response to
lion than to cheetah and wild dogs. In contrast, gemsbok (z¼2.18,
P¼0.03), red hartebeest (z¼2.37, P¼0.018) and warthog
(z¼3.45, P<0.01) maintained slightly larger groups in response
to cheetah and wild dogs than in response to lion (Fig. 1a).
All the herbivore species tended to be more vigilant at water-
holes within the lion section compared to within the cheetah and
wild dog section (Fig. 1b). Differences, however, were only statis-
tically signicant for gemsbok (z¼2.52, P¼0.01), red hartebeest
(z¼3.54, P<0.01) and warthog (z¼2.88, P<0.01) groups, and not
for eland (z¼1.69, P¼0.09), zebra (z¼1.92, P¼0.06) or wilde-
beest (z¼0.94, P¼0.35; Fig. 1b).
Gemsbok, zebra and wildebeest were predominantly diurnal at
waterholes in both predator sections (Fig. 2). However, when we
compared the differences in temporal waterhole use (day, crepus-
cular, night) for the same species across sections, we found statis-
tically signicant differences in the waterhole use of gemsbok
(z¼2.58, P¼0.01), zebra (z¼2.48, P¼0.02) and wildebeest
(z¼2.14, P¼0.03). Specically, in the lion section, these herbi-
vores visited the waterholes less during the night (z¼10.98,
z¼5.161, z¼3.63, all P<0.01, respectively) and during
crepuscular periods (z¼3.58, z¼3.59, z¼3.35, all P<0.01,
respectively) than they did in the cheetah and wild dog section.
There were no statistically signicant differences in temporal use of
D. F. Makin et al. / Animal Behaviour 127 (2017) 225e231 227
waterholes for eland (night: z¼0.12, P¼1.00; crepuscular:
z¼0.12, P¼1.0 0; d a y: z¼0.36, P¼0.998), red hartebeest
(night: z¼0.69, P¼0.982; crepuscular: z¼0.33, P¼0.999; day:
z¼0.29, P¼0.997) and warthog (crepuscular: z¼0.03, P¼1.0 0 ;
day: z¼0.26, P¼0.998; Fig. 2).
In response to predators, prey species can adjust their behaviour
in several ways to reduce risk (Caro, 2005; Creel et al., 2014; Lima &
Dill, 1990). However, as not all predators impose the same threat,
the behavioural strategies utilized by prey are likely to vary in
response to different predator hunting modes (i.e. ambush versus
cursorial), overlap in activity patterns (i.e. nocturnal versus diurnal)
and their prey preferences. We found that the antipredator
behavioural strategies of six herbivore species differed between the
lion and cheetah and wild dog sections. Overall, lions had the
greatest effect suggesting that the threat of this ambush predator
around waterholes was a key driver of the observed antipredator
behavioural adjustments of most of the herbivores.
It is possible, however, that the differences in antipredator be-
haviours we recorded were driven by landscape differences be-
tween the sections, although the two sections were only separated
by about 50 m, had identical history of land use, similar climates/
rainfall and similar topography (Cromhout, 2007; Van Rooyan,
1999). As a result, we believe that it is more likely that the
behavioural differences between the two sections were driven by
differences in predation risk posed by the two sets of predators.
Across African landscapes, lions are one of the most dangerous
predators that herbivores can encounter. The combination of their
large body size and group-hunting tactics mean that they can
successfully kill a number of species ranging from warthogs to large
herbivores including buffalo, Syncerus caffer (550e700 kg), giraffe,
Giraffa spp. (700e1400 kg) and in some cases even elephants,
Loxodonta africana (up to 7 years old; 700e900 kg; Hanks, 1972;
Loveridge, Hunt, Murindagomo, &Macdonald, 2006). Moreover,
lion actively select habitats close to waterholes and therefore pre-
sent a signicant risk to herbivores aggregated around these water
sources (Valeix, Fritz, et al., 2009; de Boer et al., 2010).
Comparing differences in the herbivore species' antipredator
behaviours between predator sections, we found that most
Lion Cheetah/wild dogs
Typical group sizes
Proportion of time spent vigilant
Eland Gemsbok Plains zebra Red hartebeest Warthog Wildebeest
Eland Gemsbok Plains zebra Red hartebeest Wartho
Figure 1. (a) Typical group sizes and (b) mean proportion of time herbivore groups were vigilant at waterholes in the two predator sections (lion versus cheetah and wild dogs).
Bars represent SE. *P<0.05.
D. F. Makin et al. / Animal Behaviour 127 (2017) 225e231228
herbivore species adjusted their behaviours so as to minimize the
risk of attack from ambushing lions. This was evident in that all the
herbivore species maintained greater vigilance in the lion section
(signicantly so for gemsbok, red hartebeest and warthog) than the
cheetah and wild dog section. This could also be partly because
vigilance may not be so necessary in the face of cursorial predators
that often testherds for vulnerable animals (Creel &Creel, 2002).
Moreover, all herbivores preferred to utilize waterholes during
midday when lions tended to be less active (Tambling et al., 2015;
Valeix, Loveridge, et al., 2009). The fact that zebra, wildebeest and
gemsbok (all preferred prey of lions) reduced their night-time us-
age of waterholes in the lion section indicates that these species
adjusted their activity patterns to reduce contact with lions. In
addition, both zebra and wildebeest moved in larger groups in the
lion section than in the cheetah and wild dog section. Thus, both
zebra and wildebeest increased the use of their range of anti-
predator behaviours against their main predator, lions. This was
similar to Valeix, Fritz, et al. (2009) and Valeix, Loveridge, et al.
(2009) who found that in Hwange National Park, wildebeest and
zebra increased their group sizes with the long-term risk of
encountering lion around waterholes.
As all the herbivore species in our study fall within the prey
weight range of lions, it is difcult to tease apart which factors are
driving the observed behavioural differences between the herbi-
vores in the two predator sections. However, as the main species
making these adjustments (i.e. zebra and wildebeest) are generally
preferred prey species of lions, we suggest that it is probably the
combination of prey preference of the lions (Sinclair et al., 2003)
and heightened predation risk at the waterholes (i.e. possibility of
being ambushed) that lead to adjustments to these and the other
species' antipredator strategies (de Boer et al., 2010).
In contrast to the general response towards lions, we found that
red hartebeest, warthog (accessible and avoided prey of cheetah and
wild dog, respectively; Hayward, O'Brien, Hofmeyr, &Kerley, 2006;
Marker, Dickman, Wilkinson, Schumann, &Fabiano, 20 07)and
gemsbok (within the prey range of wild dogs; Hayward, Hofmeyr,
et al., 2006) moved in larger groups at waterholes in the cheetah
and wild dog section. This suggests that these herbivores were
responding to the combined threat from cheetah and wild dog. Yet,
all three of these herbivore species also fall within the prey range of
lions. A potential reason for why these herbivores maintained larger
groups in the presence of cheetah and wild dogs is that it is possible
that the combined risk from these predators was greater than the
risk from lions alone. This may have been due to more frequent
contact with cheetah and wild dogs than lions. Within the lion
section, there were only two prides of lions. In contrast, in the
cheetah and wild dog section there were a minimum of 10 cheetahs,
each moving separately (D. F. Makin, personal observation), and one
pack of wild dogs (i.e. 11 potential encounters with predators).
Moreover, as cheetahand wild dogs are predominantly active during
the day (Hayward &Somers, 2009), and thus there is a greater
overlap in the activity patterns of these predators and their prey, it is
possible that by moving in larger groups these herbivores reduced
the combined risk from both predators (Clements et al., 2014).
Despite this, the differences in group size for all six herbivore
species were small with typical group sizes differing by only a few
individuals between the predator sections. This suggests that group
size may in fact not be a major adaptive response to increased
Cheetah and wild dogs
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Figure 2. Density kernel plots estimating the daily activity patterns of (a) eland, (b) gemsbok, (c) zebra, (d) red hartebeest, (e) warthog and (f) wildebeest at waterholes in the two
predator sections (cheetah and wild dog: dotted black line; lions: solid black line) and time periods (night: dark grey; crepuscular: light grey; day: white).
D. F. Makin et al. / Animal Behaviour 127 (2017) 225e231 229
predation risk from predators at waterholes in Tswalu. If this is the
case, then this suggests that all the herbivores in our study adjusted
their antipredator behaviours more in response to the potential
threat from the two prides of ambushing lions than to the cursorial
cheetah and wild dogs. Additional support for this comes from the
nding that herbivores preferred by cheetah and wild dogs did not
shift to utilizing water holes during the night when these predators
were less active (Ford et al., 2015; Hilborn, Pettorelli, Orme, &
Durant, 2012; but see Cozzi et al., 2012). One possible reason for
this is that there may have been costs that prevented these herbi-
vores from doing this, but it is unclear what these costs may be.
In conclusion, we found that the herbivores tended to display
stronger antipredator behaviour in response to lions (i.e. greater
vigilance, larger groups and temporal shift in water hole usage)
than when living with cheetah and wild dogs. This suggests that the
cursorial hunting strategy of cheetah and wild dogs imposed lower
perceived risk around waterholes than the stalk and ambush
strategy adopted by lions. Our study is one of the few that has
directly addressed the effect of hunting mode on prey behaviour,
using a powerful semiexperimental design. Moreover, our results
support the common assertion that ambush predators are likely to
induce stronger nonconsumptive effects on prey than cursorial
predators (Middleton et al., 2013; Preisser et al., 2007).
Yet, as predation risk varies across the landscape (Laundr
andez, &Ripple, 2010; Shrader, Brown, Kerley, &Kotler, 2008),
behavioural strategies utilized to reduce this risk probably also vary
spatially. As waterholes represent key interaction areas between
predators and prey, the suite of behaviours utilized by each species
we recorded probably reect those best suited against ambush
predators.However, as the possibility of ambush probablydeclines as
herbivores move away from waterholes, herbivores possibly adjust
their antipredator behaviours to reduce the use of behaviours that
decrease risk from ambush predators and increase those that are
better suited against roaming cursorial predators. Observations in
landscapes with multiple predators using contrasting hunting stra-
tegies will be required to test this hypothesis. However, in such a
landscape, Thaker et al. (2011) found that all prey species tended to
avoid the activity areas of ambush, but not of cursorial, predators.
They also found that prey responded more to habitat cues than to
actual predator distribution. See Schmitz (2007) for further discus-
sion on additive or substitutive effects in multipredator systems.
Despite focusing on a number of antipredator behaviours, there
are others we did not consider, for instance multiscale habitat use
(e.g. Padi
e et al., 2015) or reactive responses (e.g. Courbin et al.,
2016). Our study, however, highlights an important point, namely
that ecologists (including ourselves) need to move beyond focusing
on a limited set of behaviours (e.g. just vigilance) when studying
prey species' responses to predation risk. This will be difcult, but is
required, as our results highlight that animals do not reduce risk by
simply adjusting one or two behaviours, but rather exploit and
combine an array of antipredator behaviours.
We thank the Oppenheimer family and the Tswalu foundation
for allowing us to conduct the study in Tswalu. Funding for this
research was provided by UKZN, NRF (Research Grant 77582, AMS),
GreenMatter (DM) and the Tswalu Foundation. Two referees pro-
vided constructive comments on the manuscript.
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... Not all predatory species are the same and understanding how their characteristics may influence antipredator responses of prey may shed light on some of these variations. Indeed, predators differ in body size, sociality, speed, preferred prey size and hunting mode, which all have the potential to play a role in predatoreprey interactions, with larger, quicker, social forager and ambush predators perceived as the most dangerous (Thaker et al., 2011;Chamaill e-Jammes et al., 2014;Makin et al., 2017;Cuthbert et al., 2020;Hirt et al., 2020). In addition, a response that is efficient towards one predator may not be an efficient defence against another (Leblond et al., 2016). ...
... Most studies investigating the role of the predator species in prey responses in large mammals have considered proactive responses, that is, when prey modify their behaviour in response to an a priori assessment of the level of risk based on the cumulative knowledge a prey has of its environment (independently from the actual presence of the predator; e.g. Thaker et al., 2011;Makin et al., 2017). In this study, we assessed the much less studied reactive response, that is, when prey detect the presence of a predator that presents an immediate threat (either an attack, an impending attack or the mere presence of a predator that may launch an attack any time). ...
... The underlying mechanism would be that because sit-and-pursue predators tend to spend longer periods in the same area, cues of their presence should be more indicative of imminent predation risk, and therefore should elicit stronger prey responses. The idea that predator hunting mode can affect antipredator responses this way has started to appear in the literature on large mammals, with support for the above hypothesis at the scale of the proactive responses of prey (Thaker et al., 2011;Moll et al., 2016;Makin et al., 2017). Furthermore, the hunting success of ambush predators, such as lions, benefits from a surprise effect, as they can run at a very high speed but over short distances. ...
... Extending this logic, it could be expected that individual prey species will vary their spatial response to predators according to the context-dependent risk those predators afford (Chamaillé-Jammes et al., 2014;Sih et al., 1998). For example, stalking predators elicit different behavioral responses when compared to cursorial predators simply due to their hunting strategies (Makin et al., 2017;Miller et al., 2014;Thaker et al., 2011). Furthermore, the specific prey preferences of predators (Clements et al., 2014) that are reinforced throughout the predatory behavioral sequence (Hayward et al., 2011) indicates prey species are not equally at risk from each predator, and so prey responses may vary accordingly (Makin et al., 2017). ...
... For example, stalking predators elicit different behavioral responses when compared to cursorial predators simply due to their hunting strategies (Makin et al., 2017;Miller et al., 2014;Thaker et al., 2011). Furthermore, the specific prey preferences of predators (Clements et al., 2014) that are reinforced throughout the predatory behavioral sequence (Hayward et al., 2011) indicates prey species are not equally at risk from each predator, and so prey responses may vary accordingly (Makin et al., 2017). ...
... Prey can minimize the risk of predation by forming larger groups (Creel & Winnie, 2005;Moll et al., 2016), increasing their levels of vigilance, avoiding risky habitats, and limiting their activity when predators are active (Creel et al., 2014;Makin et al., 2017;Périquet et al., 2012;Tambling et al., 2015). Ultimately prey probably exhibit a context-dependent continuum of behavioral and spatial responses to minimize predation risk, and these responses are likely to be driven by a variety of direct and indirect cues (Grostal & Dicke, 1999), including visual, olfactory, and auditory indicators of predator occurrence and hence risk. ...
Predators can induce behavioral changes in prey that influence vigilance, grouping patterns, and space use, and these can ultimately affect prey demography and trophic interactions. Consequently, prey must respond to the risk of predation, but little is known about the features that drive the spatial responses of prey species to predators. We tested what factors affected the proximity of prey to the lions reintroduced to Addo Elephant National Park, South Africa. We also tested whether prey species that are preferentially killed by lions revealed greater responsiveness than those that are not, and whether prey respond to predator behavioral states and hunger. From 1588 observations of potential prey locations in relation to lions under varying wind directions , lion behaviors, and hunger states throughout the day and night, we found no evidence of wind-driven odor responses affecting prey proximity to lions. Prey species that were not preferentially preyed upon by lions occurred closer to lions than those species that lions prefer to hunt. Prey were closer to lions performing noisy behaviors compared to those performing quiet behaviors. Prey were more likely to be closer to covertly behaving lions and further from stationary lions. Our results, compared to the published literature and accepted dogma of the primacy of odor in predator detection, suggest large vertebrate prey responses to predators in intact, multi-species assemblages are context dependent. K E Y W O R D S avoidance behavior, olfaction, predation risk, prey preferences, vigilance
... For species with a segmented best fit, the slope of the final segment was not significantly different than zero, indicating that the breakpoint corresponds with a threshold of support. Species 2013, Makin et al. 2017) and use land cover or terrain features to stalk prey until close enough for a sudden attack (Wilmers et al. 2007, Bailey et al. 2013, Makin et al. 2017. The increased distances covered by cursorial predators may lead to higher energetic expenditures than more sessile stalking and ambush predators, especially when deep, low-density snow is present (Crête andLarivière 2003, Scharf et al. 2006). ...
... For species with a segmented best fit, the slope of the final segment was not significantly different than zero, indicating that the breakpoint corresponds with a threshold of support. Species 2013, Makin et al. 2017) and use land cover or terrain features to stalk prey until close enough for a sudden attack (Wilmers et al. 2007, Bailey et al. 2013, Makin et al. 2017. The increased distances covered by cursorial predators may lead to higher energetic expenditures than more sessile stalking and ambush predators, especially when deep, low-density snow is present (Crête andLarivière 2003, Scharf et al. 2006). ...
Full-text available
Snowpack dynamics have a major influence on wildlife movement ecology and predator–prey interactions. Specific snow properties such as density, hardness, and depth determine how much an animal sinks into the snowpack, which in turn drives both the energetic cost of locomotion and predation risk. Here, we quantified the relationships between five field‐measured snow variables and snow track sink depths for widely distributed predators (bobcats Lynx rufus , cougars Puma concolor , coyotes Canis latrans , wolves C. lupus ) and sympatric ungulate prey (caribou Rangifer tarandus , white‐tailed deer Odocoileus virginianus , mule deer O. hemionus , and moose Alces alces ) in interior Alaska and northern Washington, USA. We first used generalized additive models to identify which snow metrics best predicted sink depths for each species and across all species. Next, we used breakpoint regression to identify thresholds of support for the best‐performing predictor of sink depth for each species (i.e. values wherein tracks do not sink appreciably deeper into the snow). Finally, we identified ‘danger zones,' wherein snow impedes the mobility of ungulates more than carnivores, by comparing sink depths relative to hind leg lengths among predator–prey pairs. Near‐surface (0–20 cm) snow density was the strongest predictor of sink depth across species. Thresholds of support occurred at near‐surface snow densities between 220–310 kg m – ³ for predators and 300–410 kg m – ³ for prey, and danger zones peaked at intermediate snow densities (200–300 kg m – ³ ) for eight of the ten predator–prey pairs. These results can be used to link predator–prey relationships with spatially explicit snow modeling outputs and projected future changes in snow density. As climate change rapidly reshapes snowpack dynamics, these danger zones provide a useful framework to anticipate likely winners and losers of future winter conditions.
... For example, herbivores form groups to lower their risk of predation, however the maximum group size which affects their predation risk is determined by the availability of food and its dispersion . Herbivores may alter their behaviour and space use so that they are more difficult to encounter, detect and capture Makin et al., 2017;Owen-Smith, 2019) with responses differing depending on predation risk . Herbivore behavioural changes vary in space and time, resulting in them avoiding areas that pose a greater risk than others (Valeix et al., 2009;. ...
... It is recommended that a study is undertaken to unravel the dynamics of fire in MWR and its effect on mammal distribution, as other studies suggest fire has impact on mammal space use Anderson et al., 2016). Makin et al., 2017) Other potential predictors of herbivore space use are facilitation and intraguild competition between herbivores (Sinclair & Norton-Griffiths, 1982;Arsenault & Owen-Smith, 2002) as was shown through a camera trap study by Anderson et al. (2016). However, in order to properly understand the potential influence of these mechanisms, species-specific analysis would need to be undertaken (Anderson et al., 2016) which was not possible in this study due to the number of drivers already being assessed and potential model overfitting. ...
... Similar to a watering hole in an arid environment, the presence of a rich carrion resource that occurs for a short time attracts a variety of species acting as a potential trap for rodent scavengers (Sutherland et al., 2018). Research conducted at watering holes has demonstrated that prey partition waterhole use to avoid predators (Hayward and Hayward, 2012;Makin et al., 2017). Similarly, rodents often alter their activity patterns when carrion is present, avoiding avian predators, such as ravens or hawks, that are active during the day (Frank et al., 2020). ...
... Therefore, our findings echo prior research that the presence of blue sheep is a critical biological factor determining snow leopard spatial utilization , Filla, Lama, Ghale, et al., 2022Suryawanshi et al., 2021). Prey species employ various strategies to mitigate predation risk in numerous ways, such as reducing foraging time, selecting less risky areas or times for foraging, or enhancing vigilance in high-risk zones (Chitwood et al., 2022;Makin et al., 2017) in alpine screes, were more attracted to productive alpine scrub and meadows (Figure 4; Aryal et al., 2013Aryal et al., , 2014, which somewhat reduced their probability of encountering snow leopards. ...
Full-text available
Long recognized as a threat to wildlife, particularly for large carnivores, livestock grazing in protected areas can potentially undermine conservation objectives. The interspecific interactions among livestock, snow leopards (Panthera uncia), and their wild prey in fragile Asian highland ecosystems have been a subject of debate. We strategically deployed 164 camera traps in the Wolong National Nature Reserve to systematically investigate the activities of snow leopards, their primary wild ungulate prey species, and free-ranging livestock. We found that snow leopard habitat use was influenced by both wild prey and livestock. Blue sheep served as the main wild prey that spatially attracted snow leopards and coexisted with yaks while free-ranging yaks significantly restricted snow leopard habitat use both temporally and spatially. This study challenges the conventional understanding that livestock indirectly impacts large carnivores by competing with and displacing wild prey. Our findings highlight that free-ranging yaks within the alpine canyon terrain could directly limit snow leopard habitat use, suggesting a potential risk of grazing in reducing apex predator distribution and jeopardizing their populations. Consequently, managing their coexistence in shared habitats requires a more nuanced approach. Furthermore, our research underscores the importance of further research efforts aimed at enhancing our comprehension of the complex interplay within animal communities and ecosystems. This knowledge will contribute to the development of informed, evidence-based conservation strategies and policies.
... In such a system with contrasting spatial risk, prey might find it difficult to spatially avoid all predators (Atwood et al., 2009;Cresswell & Quinn, 2013;Theuerkauf & Rouys, 2008). Prey species often respond to risk from predators that provide more reliable cues (Makin et al., 2017), and hunters are generally more conspicuous in the landscape than wolves. Additionally, avoiding certain habitats to decrease predation from one predator may lead to increased exposure to other predators, a phenomenon known as risk enhancement F I G U R E 5 Relative wolf predation risk of moose in relation to (a) wolf space use; (b) distance to clearcuts and young forests (abbreviated to "distance to young forest"); and (c) distance to main roads after the hunting season. ...
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Landscape characteristics, seasonal changes in the environment, and daylight conditions influence space use and detection of prey and predators, resulting in spatiotemporal patterns of predation risk for the prey. When predators have different hunting modes, the combined effects of multiple predators are mediated by the physical landscape and can result in overlapping or contrasting patterns of predation risk. Humans have become super‐predators in many anthropogenic landscapes by harvesting game species and competing with large carnivores for prey. Here, we used the locations of wolf (Canis lupus)‐killed and hunter‐killed moose (Alces alces) in south‐central Scandinavia to investigate whether environmental and anthropogenic features influenced where wolves and hunters killed moose. We predicted that the combined effects of wolves and hunters would result in contrasting spatial risk patterns due to differences in hunting modes. We expected these contrasting spatial risk patterns also to differ temporally. During the hunting season, the probability of a wolf kill increased with distance to bogs, whereas it decreased with increasing building density and distance to clearcuts and young forests. After the hunting season, the probability of a wolf kill increased with increasing terrain ruggedness and decreased with increasing building density, distance to main roads, and distance to clearcuts and young forests. The probability of a hunter kill was highest closer to bogs, main and secondary roads, in less rugged terrain and in areas with lower building density. Hunters killed all moose during the day, whereas wolves killed most moose at night during and after the hunting season. Our findings suggest that environmental and anthropogenic features mediate hunting and wolf predation risk. Additionally, we found that hunter‐ and wolf‐killed moose exhibited contrasting spatial associations to landscape features, most likely due to the different hunting modes displayed by hunters and wolves. However, wolf predation and hunting risks also contrasted over time since wolves killed mostly at night and hunters were restricted to hunting during daytime and during the hunting season. This temporal segregation in risk might therefore suggest that moose could minimize risk exposure by taking advantage of spatiotemporally vacant hunting domains.
... The vigilance levels for both prey species were low prior to the cheetah reintroduction compared to typical vigilance values found in the literature for many other herbivore species exposed to higher predation risk (i.e. large carnivores present; Underwood, 1982;Makin et al., 2017Makin et al., , 2018Stears et al., 2020). For example, impala (Aepyceros melampus), when herding with conspecifics in high predation risk areas (i.e. ...
Rewilding is a conservation strategy used to restore ecosystems to previous states and can involve the reintroduction of large carnivores into areas from where they had been previously extirpated. Whilst rewilding has been important for ecosystem functioning, it can have negative implications for naïve prey that have had no exposure to the presence of large carnivores. Therefore, understanding prey responses to the reintroduction of predators is crucial for management and conservation. We assessed the effects of reintroduced cheetahs (Acinonyx jubatus) on the vigilance of two species of naïve prey: the steenbok (Raphicerus campestris) and the springbok (Antidorcas marsupialis).We hypothesized that both species would increase their vigilance behaviour post-cheetah reintroduction, but that the steenbok would demonstrate a greater response due to their smaller body size and more solitary nature. To test this, we compared the vigilance of both species before and after the reintroduction of cheetahs. Both species increased vigilance within one year post-cheetah reintroduction, but the steenbok demonstrated a much stronger response with a ~70% increase in the percentage of time spent vigilant post-cheetah reintroduction. Springbok levels of vigilance were lower (~50% increase), which we suggest is a function of body-size and/or grouping behaviour. Importantly,we showthat naïve prey species are able to exhibit a rapid response to the reintroduction of large carnivores.However, the variation in responses highlights the importance of species-level monitoring after large carnivore reintroductions.
It is often assumed that because predators typically consume large numbers of prey, they automatically control prey population sizes and help shape the evolution of their prey’s distinctive traits. Examining the evolutionary history, ecology, and behavior of equids challenges these assumptions. A suite of morphological traits appears to be a response to changing climates, habitat opening and selection for lowering locomotory costs, not to the emergence of pursuit predators. And while predation can drive down equid numbers locally, large regional populations and the fact that predators do not specialize on equids, suggests that most extant equid populations will stabilize, or even grow, unless other factors control population numbers. Behaviors enhancing equid survival come in a variety of forms: living in groups automatically dilutes the risk of being the one eaten if predators successfully kill one group member; sharing vigilance to maintain a level of personal protection without forgoing other activities such as grazing; adjusting daily activity schedules to balance risk without paying for lost foraging opportunities; changing habitats when predators are detected prior to an attack; maintaining cohesion or confusing predators while fleeing; or even staying put and fighting back when early detection fails. Which of these many adaptations will be deployed will depend not only on each species’ suite of physical traits and how its society is structured, but also on an individual’s reproductive or nutritional state as well as on features of the environment.
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The restoration of ecosystems through trophic rewilding has become increasingly common worldwide, but the effects on predator–prey and ecosystem dynamics remain poorly understood. For example, predation pressure may impose spatiotemporal behavioural adjustments in prey individuals, affecting herbivory and predation success, and therefore potentially impinging on the long-term success of trophic rewilding through apex predator reintroduction. Predation risk might have detrimental effects on prey through displacement from water or other vital resources. We investigated how five species of African ungulates responded behaviourally to changes in predation risk, following cheetah releases in the system. We grouped ungulates by body size to represent preferred prey weight ranges of the cheetah and examined changes in visitation rates, duration of stay, and activity patterns at waterholes with and without cheetah presence. During cheetah presence, visitation rates of ungulates were low for medium-sized species but high for large-sized species, suggesting that the species within the cheetah’s preferred prey weight range adjusted behaviourally to minimize waterhole visits. Visits to waterholes were longer for small- and large-sized ungulates with cheetah presence, possibly indicating increased vigilance, or a strategy to maximize water intake per visit while minimizing visits. We did not detect significant differences in circadian or seasonal activity in waterhole visits, which may be attributable to the need of ungulates to access water year-round in our semi-arid study system and where migration was impeded due to physical barriers (fencing). We recommend further research into the long-term behavioural consequences of trophic rewilding on prey populations and trophic cascades to assist the success of recovery programs and to minimize potential detrimental effects at target sites.
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In dry biomes, spatio-temporal variation in surface water resource stocks is pervasive, with unknown effects on the ranging behaviour of large predators. This study assessed the effect of spatial variation in surface water resources on the ranging behaviour of the African wild dog (Lycaon pictus). We analyzed data for 1992 (dry year with 20 water points) and 2000 (wet year with 30 water points) against presence-only data for five packs of L. pictus in a part of Hwange National Park and adjacent smallholder communal farming areas in western Zimbabwe. Modelling the potential habitat for L. pictus using Maxent with distance from water points (Dw) and Normalized Difference Vegetation Index (NDVI) as predictor variables was successful for 2000 (AUC = 0.793) but not successful for 1992 (AUC = 0.423), with L. pictus probability of occurrence near water points being more for year 2000 than for year 1992. The predicted L. pictus range was wider in 1992 (~13888.1 km2) than in 2000 (~958.4 km2) (Test of Proportions, χ2 = 124.52, df = 1, P = 0.00). Using the 2nd order Multitype Nearest Neighbour Distance Function (Gcross), we also observed significant attraction between L. pictus and water points within only ~1km radius for 1992 but up to ~8km radius for 2000. Our study reinforced the notion that surface water resources attract wild dogs in the savannahs but paradoxically less so when water resources are scarce. In particular, our study furthers current understanding of the effects of changing water availability regimes on the endangered L. pictus, providing evidence that the endangered predator's home range encroaches into potential ecological traps (i.e., smallholder communal farming areas) when water resources are scarce.
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The predator-prey space game and the costs associated with risk effects are affected by prey 1) proactive adjustments (when prey modify their behaviour in response to an a priori assessment of the risk level) and 2) reactive adjustments (when prey have detected an immediate threat). Proactive adjustments are generally well-studied, whereas the frequency, strength and duration of reactive adjustments remain largely unknown. We studied the space use and habitat selection of GPS-collared zebras Equus quagga from 2 to 48 h after an encounter with lions Panthera leo. Lion-zebra encounters generally occurred close to artificial waterholes (< 1 km). Two hours after an encounter, zebras were more likely to have fled than stay when the encounter occurred in more risky bushy areas. During their flight, zebras selected grasslands more than usual, getting great visibility. Regardless of their initial response, zebras finally fled at the end of the night and reached areas located far from waterholes where encounters with lions are less frequent. The large-scale flights (∼4-5 km) of zebras led to a local zebra depression for lions. Zebras that had fled immediately after the encounter resumed their behaviour of coming close to waterholes on the following day. However, zebras that had initially stayed remained far from waterholes for an extra 24 h, remaining an elusive prey for longer. The delay in the flight decision had different short-term consequences on the lion-zebra game. We reveal that the spatial context of the encounter shapes the immediate response of prey, and that encountering predators induces strong behavioural responses: prey flee towards distant, safer, areas and have a constrained use of key resource areas which are at the heart of the predator-prey game at larger spatio-temporal scales. Nighttime encounters were infrequent (once every 35 days on average), zebra responses were short-lived (< 36 h) but occurred over a large spatial scale (several km).
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Extinction risk in African wild dogs (Lycaon pictus) has been linked to their wide-ranging movement behavior. However, drivers of variability in African wild dog ranging are not well understood. This study examines the effects of intrinsic and extrinsic factors on ranging patterns and describes scale-dependent and intra-annual variation in the ranging of 5 packs of African wild dogs in the Okavango Delta from 2007 to 2010. 95% fixed kernel home ranges (X = 739 ± 81 km2) and daily step lengths (X = 8.5 ± 0.5 km) in this study are larger than have generally been reported for African wild dogs elsewhere. Little seasonal variation in daily ranging distances was observed despite home-range contractions during denning to 27% of packs’ ranges outside the denning period. During nondenning periods, litter size was the most influential driver of ranging patterns, with large litters associated with reduced pack movements and smaller home ranges at all temporal scales. Pack size was also a significant driver of home-range size (but not daily distance travelled) at weekly timescales, where larger packs utilized smaller ranges. Daily temperatures were inversely related to home-range size and step length at short timescales, while higher flood levels were related to reduced ranging distances at intermediate timescales. Our results indicate that extrinsic drivers of African wild dog ranging behavior tend to be scale dependent, while intrinsic factors may be more influential for ranging patterns than previously reported.
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The response of prey to predation risk varies through time and space. These responses relate to trade-offs between foraging and predator avoidance. Following the extirpation of predators from many landscapes, the responses related to predator avoidance may have been lost or diluted. Investigating the activity pattern of prey species on comparable landscapes with and without large predators provides an opportunity to understand how predators may shape prey activity and behaviour. Using camera trap data from neighbouring fenced sections of the Addo Elephant National Park (Eastern Cape, South Africa), we investigated the activity patterns of species exposed to large predators, where the predators were only present in one of the sections. Our results suggest that prey species at risk of predation (e.g., buffalo, kudu and warthog) are more likely to be active diurnally when co-existing with nocturnally active predators, thereby reducing the activity overlap with these predators. In the absence of predators, kudu and buffalo were more active at night resulting in a low overlap in activity between sections. Warthog activity was predominantly diurnal in both sections, resulting in a high overlap in activity between sections. The presence of predators reduced the nocturnal activity of warthogs from 6 to 0.6 % of all warthog captures in each section. Elephants, which are above the preferred prey weight range of the predators and therefore have a low risk of predation, showed higher overlap in activity periodicity between predator-present and predator-absent areas. Our findings suggest that maintaining prey with their predators has the added benefit of conserving the full spectrum of prey adaptive behaviours.
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Increasingly, the restoration of large carnivores is proposed as a means through which to restore community structure and ecosystem function via trophic cascades. After a decades-long absence, African wild dogs (Lycaon pictus) recolonized the Laikipia Plateau in central Kenya, which we hypothesized would trigger a trophic cascade via suppression of their primary prey (dik-dik, Madoqua guentheri) and the subsequent relaxation of browsing pressure on trees. We tested the trophic-cascade hypothesis using (1) a 14-year time series of wild dog abundance; (2) surveys of dik-dik population densities conducted before and after wild dog recovery; and (3) two separate, replicated, herbivore-exclusion experiments initiated before and after wild dog recovery. The dik-dik population declined by 33% following wild dog recovery, which is best explained by wild dog predation. Dik-dik browsing suppressed tree abundance, but the strength of suppression did not differ between before and after wild dog recovery. Despite strong, top-down limitation between adjacent trophic levels (carnivore- herbivore and herbivore-plant), a trophic cascade did not occur, possibly because of a time lag in indirect effects, variation in rainfall, and foraging by herbivores other than dik-dik. Our ability to reject the trophic-cascade hypothesis required two important approaches: (1) temporally replicated herbivore exclusions, separately established before and after wild dog recovery; and (2) evaluating multiple drivers of variation in the abundance of dik-dik and trees. While the restoration of large carnivores is often a conservation priority, our results suggest that indirect effects are mediated by ecological context, and that trophic cascades are not a foregone conclusion of such recoveries.
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Non-consumptive effects of predators result from the cost of responses to perceived risk. Prey modulate risk exposure through flexible habitat selection at multiple scales which, in interaction with landscape constraints, determines their use of risky habitats. Identifying the relative contributions of landscape constraints and habitat selection to risk exposure is a critical first step towards a mechanistic understanding of non-consumptive effects.Here, we provide an integrative multi-scale study of roe deer spatial responses to variable hunting pressure along a landscape gradient of open habitats and dispersed refuges. Between low-risk and high-risk periods, we investigated shifts in 1) home-range location, 2) probability of using risky habitats (between-habitat scale) and 3) distance to the nearest refuge (within-habitat scale). For 2) and 3), we disentangled the contributions of landscape constraints and habitat selection to risky habitat use.We found that when risk was high, roe deer did not shift their home-range, but generally decreased their use of risky habitats, and sometimes reduced their distance to cover (particularly older animals). There was a functional response in between-habitat selection, with animals living in more open landscapes responding more than those living in landscapes with more refuges. However, individuals living in more open landscapes avoided open risky habitat less. Finally, we found that among-individual variation in risk exposure was generally, but not always, minimized by habitat selection across gradients of landscape constraints.To our knowledge, this is the first study simultaneously documenting prey responses to risk at the within-habitat, between-habitat and home-range scales. Our results support the view that between-habitat selection acts at a higher hierarchical level than within-habitat selection, and provide a framework for disentangling the contributions of habitat selection and landscape constraints to risk exposure. Selection cannot always compensate for landscape constraints, indicating a need for further investigation of the processes underlying habitat selection.
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Predators alter prey dynamics by direct killing and through the costs of antipredator responses or risk effects. Antipredator behavior includes proactive responses to long-term variation in risk (e.g., grouping patterns) and reactive responses to short-term variation in risk (e.g., intense vigilance). In a 3-year field study, we measured variation in antipredator responses and the foraging costs of these responses for 5 ungulates (zebra, wildebeest, Grant’s gazelle, impala, and giraffe) that comprised more than 90% of the prey community available to the 2 locally dominant predators, lions and spotted hyenas. Using a model-selection approach, we examined how vigilance and group size responded to attributes of the predator, prey, and environment. We found that 1) the strength of antipredator responses was affected by attributes of the predator, prey, and environment in which they met; 2) grouping and vigilance were complementary responses; 3) grouping was a proactive response to the use of dangerous habitats, whereas vigilance was a reactive response to finer cues about predation risk; 4) increased vigilance caused a large reduction in foraging for some species (but not all); and 5) there was no clear relationship between direct predation rates and the foraging costs of antipredator responses. Broadly, our results show that antipredator responses and their costs vary in a complex manner among prey species, the predators they face, and the environment in which they meet.
S-Plus is a powerful environment for statistical and graphical analysis of data. It provides the tools to implement many statistical ideas which have been made possible by the widespread availability of workstations having good graphics and computational capabilities. This book is a guide to using S-Plus to perform statistical analyses and provides both an introduction to the use of S-Plus and a course in modern statistical methods. All data sets and S-Plus functions used are supplied with the book on a diskette.
We collect together several ways to handle linear and non-linear models with random effects, possibly as well as fixed effects.