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Abstract

Prey species develop anti-predatory strategies as a response to minimising the risk of being predated. However, how the European rabbit (Oryctolagus cuniculus) adapts to different predator pressure is not fully known. Here, we studied the adap-tive anti-predatory responses of European rabbits exposed to different terrestrial predation pressure. To do this, we took advantage of a rabbit translocation programme in the Sierra Norte Natural Park of Sevilla (SW Spain), where rabbits from the same donor population were translocated in plots with and without terrestrial predator exclusion fences (aerial predation was not excluded in any of the plots). This presented an ideal opportunity to observe whether the behaviour of individuals from the same population adapts to situations with different predator pressure; thus, their behaviour was evaluated through direct observations. Although most rabbits were observed close to cover, differences in distance to cover, group size and behaviour were observed between fenced and unfenced plots. Overall, both adult and juvenile rabbits moved further from cover in the unfenced plot than in the fenced plot. Most of the observations in the unfenced plot corresponded to rabbits in pairs or alone; whereas in the fenced plot, rabbits were primarily in pairs or in larger groups. Our findings suggest that in the unfenced plot, rabbits that moved further from cover were often part of larger groups (≥ 4 rabbits); whereas in the fenced plot, it was rabbits in smaller groups (< 4 rabbits). Rabbits in the unfenced plot were alert and running more frequently than rabbits in the fenced one; in the latter, these rabbits were mostly feeding. Other relaxed behaviours such us grooming or resting were more frequent close to cover. In summary, our results highlight rabbits' capacity to promptly adjust behaviour in response to predation risk, exhibiting adaptive anti-predatory responses tailored to different predation pressures. These insights contribute to understanding the nuanced dynamics of prey species' responses to diverse predation scenarios.
Vol.:(0123456789)
Mammalian Biology
https://doi.org/10.1007/s42991-024-00398-3
ORIGINAL ARTICLE
Adaptive anti‑predatory responses ofEuropean rabbits exposed
todifferent predation pressure
JorgeTobajas1 · C.C.Ferreira2· M.Delibes‑Mateos3 · R.Villafuerte3 · CarlosRoucoZuaurre4
Received: 9 May 2023 / Accepted: 10 January 2024
© The Author(s) 2024
Abstract
Prey species develop anti-predatory strategies as a response to minimising the risk of being predated. However, how the
European rabbit (Oryctolagus cuniculus) adapts to different predator pressure is not fully known. Here, we studied the adap-
tive anti-predatory responses of European rabbits exposed to different terrestrial predation pressure. To do this, we took
advantage of a rabbit translocation programme in the Sierra Norte Natural Park of Sevilla(SW Spain), where rabbits from
the same donor population were translocated in plots with and without terrestrial predator exclusion fences (aerial predation
was not excluded in any of the plots). This presented an ideal opportunity to observe whether the behaviour of individuals
from the same population adapts to situations with different predator pressure; thus, their behaviour was evaluated through
direct observations. Although most rabbits were observed close to cover, differences in distance to cover, group size and
behaviour were observed between fenced and unfenced plots. Overall, both adult and juvenile rabbits moved further from
cover in the unfenced plot than in the fenced plot. Most of the observations in the unfenced plot corresponded to rabbits in
pairs or alone; whereas in the fenced plot, rabbits were primarily in pairs or in larger groups. Our findings suggest that in the
unfenced plot, rabbits that moved further from cover were often part of larger groups (≥ 4 rabbits); whereas in the fenced
plot, it was rabbits in smaller groups (< 4 rabbits). Rabbits in the unfenced plot were alert and running more frequently than
rabbits in the fenced one; in the latter, these rabbits were mostly feeding. Other relaxed behaviours such us grooming or
resting were more frequent close to cover. In summary, our results highlight rabbits' capacity to promptly adjust behaviour
in response to predation risk, exhibiting adaptive anti-predatory responses tailored to different predation pressures. These
insights contribute to understanding the nuanced dynamics of prey species' responses to diverse predation scenarios.
Keywords Behavioural ecology· Threat-sensitive predator avoidance hypothesis· Small mammals· Carnivores· Predator–
prey relationship· Predation risk
Introduction
Prey species have developed a variety of strategies to
reduce the strong selective pressures caused by predators
(Barnard 1983; Futuyma and Moreno 1988). Physiological,
morphological and also behavioural adaptations serve as
mechanisms to enhance survival in response to predation
risk (Nilsson etal. 1995; Teplitsky etal. 2005; Rouco etal.
2011a; Tobajas etal. 2023). These adaptations can manifest
as distinct anti-predatory strategies depending on the type of
predation pressure experienced by the prey (e.g. terrestrial
vs. aerial predators) (Curio 1975; Hanson and Coss 1997;
Taraborelli etal. 2008). However, anti-predatory strategies
are costly, including energetic investments in defensive
structures and mechanisms (e.g. flight, autotomy), or by
potential reductions in mating success (Preisser etal. 2005;
Handling editor: Raquel Monclús.
* Jorge Tobajas
sc2togoj@uco.es; jtobajas47@gmail.com
* Carlos Rouco Zufiaurre
crouco@us.es
1 Departamento de Botánica, Ecología y Fisiología
Vegetal, Campus de Rabanales, Universidad de Córdoba,
14071Córdoba, Spain
2 Environment andClimate Change Canada, Toronto, ON,
Canada
3 Instituto de Estudios Sociales Avanzados (IESA-CSIC),
Campo Santo de los Mártires 7, 14004Córdoba, Spain
4 Departamento de Biología Vegetal y Ecología, Facultad de
Biología, Universidad de Sevilla, 41012Seville, Spain
J.Tobajas et al.
Ferretti etal. 2019; Savvides etal. 2019). Therefore, several
factors may influence predation risk, such as predator diver-
sity and abundance, availability of alternative prey, habitat
characteristics or the perceived risk of predation by the prey.
This perception can depend on various factors, including
age, group size, predator recognition or habitat characteris-
tics (Bolles 1970; Lima 1995; Villafuerte and Moreno 1997;
Blanchard etal. 2016; Savvides etal. 2019).
One of the mammalian prey species that has received
significant attention in terms of its anti-predatory responses
is the wild European rabbit (Oryctolagus cuniculus). It is
native from the Iberian Peninsula, where it is a key prey
species for more than 30 predators and where it is one of
the main small game species (Delibes-Mateos etal. 2008).
Consequently, the European rabbit has been used as a model
to test several ecological hypotheses regarding predation risk
in mammal prey. This is not only for purely scientific inter-
est (e.g. Villafuerte and Moreno 1997; Monterroso etal.
2013; Descalzo etal. 2021), but also holds significance for
conservation efforts, such as bolstering rabbit populations
for endangered predators (Ferreira and Delibes-Mateos
2010) and/or game management, including predator con-
trol interventions to increase rabbit populations (Calvete
and Estrada 2004; Tobajas etal. 2021a, b). Previous studies
have unveiled diverse anti-predatory responses in rabbits,
including behavioural and physiological mechanisms (Mon-
clús etal. 2005, 2006a, b; Villafuerte and Moreno 1997;
Monterroso etal. 2013; Rocha etal. 2022), in addition to
naïve short-term adaptive responses to predators (Rouco
etal. 2011a; Descalzo etal. 2021). These anti-predatory
strategies may be modulated by the hunting strategy of the
predator (Jaksic and Soriguer 1981; Moreno etal. 1996).
Nevertheless, there is a knowledge gap regarding the rapidity
of this adaptation to the presence of predators and whether
rabbits will adjust differently to distinct predation pressures.
In 2009, Monclús etal. (2009) tested the threat-sensitive
predator avoidance hypothesis in mammals for the first time.
This investigation focused on a European rabbit population
in Doñana National Park (southwest Spain). This hypothesis
states that animals modulate their anti-predatory responses
based on the perceived risk of predation (Helfman 1989;
Horat and Semlitsch 1994). That study suggested that rabbits
exposed to higher predation pressure showed higher levels
of faecal corticosterone metabolites, indicating heightened
physiological stress (Monclús etal. 2009). The rabbit popu-
lations studied by Monclús etal. (2009) in Doñana National
Park (i.e. one with high and another with low predation pres-
sure) had inhabited the study areas for decades before the
experiment. This extended exposure allowed for long-term
adaptation to the different predation pressure conditions.
However, the study did not assess potential changes in rab-
bit behaviour, leaving the short-term behavioural adapta-
tions of rabbits unexplored. In a subsequent investigation,
Descalzo etal. (2021) demonstrated that rabbits can adjust
their daily activity patterns to reduce predation risk depend-
ing on the pressure exerted by different mammalian predator
species. However, it is unclear whether this adaptation to the
presence of predators could go beyond the activity pattern
(Monterroso etal. 2013; Tobajas etal. 2023).
Previous investigations have established that both dis-
tance from cover and group size can serve as proxies for
perceived predation risk and can affect European rabbit
behaviour (Moreno etal. 1996; Caro 2005; Blanchard etal.
2016; but see Monclús and Rödel 2008). Specifically, an
increase in distance from cover correlates with heightened
perceived predation risk. Consequently, rabbits are expected
to venture shorter distances from cover when predation pres-
sure is higher (Jaksic and Soriguer 1981; Villafuerte and
Moreno 1997). Regarding rabbit group size, their response
may vary depending on the type of predator. Large groups
may attract terrestrial predators due to an increase in prey
odour (Roberts 1996). Nevertheless, these large groups may
also act as a deterrent to raptors, as the absence of a clear
individual target makes it challenging for the raptors to sin-
gle out prey (Villafuerte and Moreno 1997).
In this study, we leveraged a large-scale recovery pro-
gramme for European rabbits that was implemented in the
Sierra Norte Natural Parkof Sevilla (SW Spain) to assess
the anti-predatory responses of European rabbits to aerial
and terrestrial predation. For this purpose, we translocated
rabbits to two distinct plots: an unfenced plot with higher
predation pressure (exposed to both aerial and terrestrial
predation) and another fenced plot with lower predation
pressure (terrestrial predation excluded but exposed to aerial
predation). In line with the threat-sensitive predator avoid-
ance hypothesis, our hypothesis posited that rabbits in the
area with lower predation pressure (without terrestrial preda-
tors) would exhibit larger group sizes, move to larger dis-
tances from cover and exhibit behaviours that are typically
associated with a low level of risk perception (e.g. feeding,
apparent inactivity), while decreasing those associated with
a higher level of risk (e.g. running, alertness).
Materials andmethods
Study area
The experiment was conducted in the area of Los Melon-
ares (Sierra Norte Natural Park of Sevilla, SW Spain). This
region has two main biotopes: Mediterranean grassland
(70%) and scrubland (30%). The rabbit population in the
study area prior to conducting the experiment was virtu-
ally non-existent (see below), but both mammalian (9 spe-
cies) and raptor (19 species) predators that prey upon rabbits
were recorded (complete list in Rouco 2008). In particular,
Adaptive anti-predatory responses ofEuropean rabbits exposed todifferent predation pressure
the most common species of terrestrial carnivores recorded
at our study area were red fox (Vulpes vulpes), Egyptian
mongoose (Herpestes ichneumon), and to a lesser extent
stone marten (Martes foina) and least weasel (Mustela niva-
lis) (Rouco etal. 2008). The bird of prey community was
mainly composed by the short-toed snake eagle (Circaetus
gallicus), Bonelli's eagle (Aquila fasciata), golden eagle
(Aquila chrysaetos) and to a lesser extent black kite (Mil-
vus migrans), booted eagle (Hieraaetus pennatus), Spanish
imperial eagle (Aquila adalberti) and the Eurasianeagle owl
(Bubo bubo) (Rouco 2008; Tobajas etal. 2021a, b).
Experimental design
The study population originates from a rabbit transloca-
tion programme carried out by a governmental entity (i.e.
Confederacion Hidrográfica del Guadalquivir) as a com-
pensatory measure for the construction of a reservoir in
the Sierra Norte Natural Park of Sevilla. During autumn
2002 (i.e. October–November), rabbits from a high-den-
sity source population located at a hunting estate ~ 300km
from our study site (Cádiz province, southern Spain) were
translocated into two experimental plots 1km apart (for
details regarding housing conditions of the rabbit popula-
tion, see Ferreira etal. 2009; Rouco etal. 2008, 2011b).
Rabbits corresponded to the subspecies O. c. algirus,
which is predominant in southern Spain (Ferreira etal.
2015). Prior to the translocation, rabbit abundance in the
plots was negligible. Each of the two plots consisted of a
grassland field approximately 4ha in size. To reduce the
effect of confinement in rabbit movements and behaviour,
this size is much larger than a rabbit average home range in
high-density natural populations (e.g. ~ 0.7–1.2ha, Lom-
bardi etal. 2007; Devillard etal. 2008). To completely
exclude predation risk due to terrestrial carnivores, one
of the plots had a fence (1.0m below ground, 2.5m above
ground) with an electrified wire on top (hereinafter fenced
plot; Rouco etal. 2008). The mesh size was small enough
to prevent the passage of any predator, such as the weasel.
The other plot had the same characteristics excepting the
presence of the fence (hereinafter unfenced plot). Birds of
prey were not excluded from either plot. Each plot con-
tained 18 artificial rabbit warrens built above ground, con-
sisting of piles of stumps and rocks covered with loam and
branches (Rouco etal. 2011b). Since no vegetation existed
in the plots, warrens were the only refuge available against
predators within the plots. Water and food suppliers were
situated close to each warren (~ 4m), and water and food
were available adlibitum. Fresh alfalfa was additionally
provided once a week and placed close to warren entrances
(~ 1m). Throughout the experiment, the plots were regu-
larly inspected for depredated rabbits or predator scats. In
the fenced plots, no rabbits depredated by carnivores or
their scats were detected; however, pellets from raptors
like the Eurasian eagle owl were found in both fenced and
unfenced plots.
Distance tocover, rabbit group size andrabbit
behaviour
Rabbit’s response to predation pressure was assessed by
direct observations of rabbits in the two plots. Observa-
tions were carried out between February and March 2003
during fine evenings at dusk, starting three hours before
sunset for a total of 12 non-consecutive days (6days on
each plot) and finishing observations just after sunset (i.e.
an average of 3-h observation per day; total of 18-h obser-
vation per plot). The same experimental observer (CR)
conducted rabbit focal observations from a fixed position
approximately 100m away from the plots, using a field
telescope with a 25–60 power lens from a hideout. Cam-
ouflage clothing was consistently worn to blend with the
surroundings, and the observation point was strategically
placed behind shrubs or bushes for maximum inconspicu-
ousness. No effect on the behaviour of the rabbits was
observed due to the presence of the observer. Poles were
strategically positioned at various known distances on the
ground within each plot, serving as reference points to
ensure precise distance estimations during observational
assessments.
The methodology consisted of scanning the whole plot
starting from one fixed point and continuing until the
whole plot has been scanned. The same procedure was
repeated successively until the end of all plots each day.
Every time a rabbit was sighted, the observer focused on
the animal to estimate its age based on body size (i.e.
adult or juvenile, but only really obvious juveniles based
on previous studies; Rouco etal. 2008), and to estimate
distance to nearest cover. To calculate the rabbit distances,
previously placed poles at known distances were used. The
observer also estimated the distance to the nearest rabbit.
Rabbits were considered paired or in a group when the
distance between them did not exceed 5m (Villafuerte and
Moreno 1997). If any animal was further than 5m away
from another rabbit when first sighted it was considered as
solitary. Thus, rabbits were assigned to four group sizes:
solitary, pairs, groups of three rabbits or groups of four
rabbits and larger (Villafuerte and Moreno 1997). The rab-
bits were assigned to each group regardless of their age, as
long as they were within 5m. Distance of a group to cover
was estimated as the mean distance of all the individuals
in the group to cover. Finally, the observer classified all
rabbit’s behaviour in one of the following categories: alert,
feeding, running or other (the latter included grooming,
sniffing and/or resting).
J.Tobajas et al.
Statistical analysis
To assess the statistical differences in the proportions
of observations of rabbits across different group sizes in
fenced versus unfenced plots, standard contingency table
tests (chi-square) were employed. General linear models
(GLM) with a Poisson distribution and a log link function
using R package ‘lmtest’ (Zeileis and Hothorn 2002)were
fit to the data to test whether distance of rabbits to cover was
affected by rabbit group size, age and type of predation pres-
sure (unfenced and fenced) and their interactions. To assess
the effect of factors on each rabbit behaviour, GLMs with a
binomial distribution and a logit link function were applied.
The response variable was the presence of the behaviour in
each rabbit observation, and the factors included predation
pressure (fenced, unfenced), age, group size and distance
from cover. If significant differences were found in GLMs,
a pairwise post hoc comparison between factor levels was
performed using Tukey’s test with the package ‘emmeans’.
Collinearity between predictors was checked (all predictors
r < 0.5), as well as violations to all modelling assumptions
through analyses of residuals (Zuur etal. 2009). All analyses
were carried out using the R statistical computing environ-
ment (version 4.0.2, R Core Team 2020).
Results
A total of 504 rabbit observations were recorded, 207 in
the unfenced plot (116 adults and 91 juveniles) and 297 in
the fenced plot (136 adults and 161 juveniles). Most of the
observations in the unfenced plot corresponded to rabbits
in pairs or solitary, whereas in the fenced plot rabbits were
mostly in pairs or in larger groups, and these differences
were statistically significant (χ2 = 95.59, df = 3, P < 0.001,
Fig.1). In the later, only 10% of the observations were soli-
tary animals. The GLM results revealed that rabbits moved
further from cover in the unfenced plot than in the fenced
plot (χ2 = 15.34, df = 1, P < 0.001) (Fig.2). No significant
differences were found in group size (χ2 = 5.43, df = 3,
P = 0.14) and age (χ2 = 0.56, df = 1, P = 0.46), but there was
a significant effect in the interaction between group size and
plot (χ2 = 27.9, df = 3, P < 0.001). However, post hoc analy-
ses showed that these differences (P < 0.05) were observed
in larger groups (≥ 4 rabbits) that were in the unfenced
plot, whereas rabbits in the fenced plot that moved further
from cover were solitary rabbits or smaller groups rather
than larger groups (Fig.2). Finally, a significant interac-
tion between group and age was found (χ2 = 8.21, df = 3,
P = 0.042), showing differences in the distance from cover
depending on age, especially in the solitary rabbits ventured
further than adults.
Overall, direct observations revealed that both adult and
juvenile rabbits in the fenced plot behaved different to those
in the unfenced plot (Fig.3). In particular, rabbits in the
0
5
10
15
20
25
30
35
40
45
Solitary Pairs3 ≥4
% of adults observed
Unfenced plot
Fenced plot
0
5
10
15
20
25
30
35
40
45
Solitary Pairs3 ≥4
% of juveniles observed
Group size
Unfenced plot
Fenced plot
B
A
Fig. 1 Percentage of direct observations of adult (A) and juvenile (B)
rabbits according to group size in unfenced and fenced plots. Rab-
bits were considered paired or in a group when the distance between
them did not exceed 5m. Rabbits further than 5m away from another
rabbit were considered as solitary. The rabbits were assigned to each
group regardless of their age
0.0
2.0
4.0
6.0
8.0
10.0
Solitary Pairs
3≥
4
Mean distance from cover (m)
Group size
Unfenced plot
Fenced plot
*
Fig. 2 Mean distance (+ 95% confidence intervals) from cover of
rabbit groups in unfenced and fenced plots. Rabbits were considered
paired or in a group when the distance between them did not exceed
5m. Rabbits further than 5 m away from another rabbit were consid-
ered as solitary. *Indicates significant (P < 0.05) differences between
plots
Adaptive anti-predatory responses ofEuropean rabbits exposed todifferent predation pressure
unfenced plot were alert and running more frequently than
in the fenced plot; the latter were mostly feeding and other
relaxed behaviours (Fig.3). The GLM showed a significant
effect of plot for running (χ2 = 12.17, df = 1, P < 0.001),
feeding (χ2 = 7.38, df = 1, P = 0.006) and slightly effect for
alert (χ2 = 2.71, df = 1, P = 0.09). No other significant effect
of factors was found for these behaviours. Interestingly,
only a significant negative relationship was found in other
behaviours (related with relaxing activity such us groom-
ing or resting) with distance from cover (χ2 = 4.86, df = 1,
P = 0.027), spending the rabbits less time in this behaviour
far from cover.
Discussion
The results show that, regardless of the presence of car-
nivores, both adult and juvenile rabbits exhibited limited
movement away from cover owing to the risk of predation.
In Iberian Mediterranean habitats there are various diurnal
and visible predator species (mainly birds of prey), contrib-
uting to a persistent predation risk for rabbits but diminish-
ing during last hours of daylight (Moreno etal. 1996; Pente-
riani etal. 2006), coinciding with the observation period in
our study. In our study area we observed a high diversity of
raptor species (detailed in study area section, Rouco 2008),
which may explain that rabbits preferred to feed closer to
cover during the day (i.e. it is safer). In addition, rabbits
tend to not move far from cover in open grasslands if few
shelters are available (Palomares and Delibes 1997), as
occurred in our study site. In contrast to our expectations,
rabbits in the unfenced plot, where they were less abundant
(see Rouco etal. 2011b) and terrestrial carnivores access
was unrestricted (see Rouco etal. 2008), moved further than
those in the fenced plot. This is in disagreement with other
findings. For example, Banks etal. (1999) found that rabbits
moved further from cover in an area where red foxes had
been removed than in other areas where this predator was
present, which was attributed by these authors to a perceived
reduction in predation risk. The fact that rabbits moved fur-
ther from cover in the area with a higher predation risk in
our study could be due to several reasons. First, rabbits tend
to have larger home ranges (i.e. move further) in areas of
lower density (Devillard etal. 2008), a pattern observed in
social species (Efford etal. 2016). Second, the increased
distance from cover in the unfenced plot could be driven by
nutritional needs, as rabbits were observed feeding at greater
distances where fresh pasture, potentially of higher qual-
ity than supplementary food, was available. While we did
not quantify food availability, the unfenced plot had more
pasture due to lower rabbit abundance and, consequently,
reduced grazing pressure. Therefore, rabbits could have
reached better quality food (e.g. fresh pasture) found at fur-
ther distances from the warren (Crowell etal. 2016), than
the weekly supplementary food. Thirdly, it is possible that
due to the higher rabbit abundance found in the fenced plot,
rabbits were closer to their warren for territorial defence. In
larger groups, higher density is usually related to increased
aggression rates and social instability (Monclús etal. 2009).
Nonetheless, most adults and juveniles in the fenced plot
were feeding at close distance (< 5m) to cover.
In this study, we assessed experimentally how a reduction
in terrestrial predation pressure affected the behaviour of
European rabbit populations. Prey behaviour in any given
situation depends on the proportion of time that prey spe-
cies spend in high-risk versus low-risk situations (Lima and
Bednekoff 1999). When high-risk situations are scarce rab-
bits devote most time to feeding and maintaining a moderate
level of vigilance (Sih and Ziemba 2000), as observed in
the fenced plot (Fig.3). Conversely, it is expected that in
a high predation risk situation rabbits would spend more
time alert or engaging in evasive running behaviours. How-
ever, because safe periods are infrequent, prey must forage
intensely and exhibit minimal or no vigilance during these
periods (Sih and Ziemba 2000), which agrees with our
results in the unfenced plot (Fig.3).
Interestingly, we predominantly observed solitary or
pairs of rabbit in the area with higher terrestrial predation
pressure (i.e. unfenced plot), and the few larger groups
were only observed at larger distances from cover (Fig.2),
where rabbits spent most of the time feeding. In contrast,
pairs and larger groups were more common insituations
where terrestrial predation was excluded (Fig.2), and the
rabbits that ventured further from cover usually did so in
smaller groups. These contrasting responses can be attrib-
uted to a common principle, namely a cooperative vigi-
lance among rabbits (Roberts 1988, 1996). In scenarios
0
20
40
60
80
100
Alert FeedingRunning Other
% of rabbits observed
Unfenced plot
Fenced plot
*
*
Fig. 3 Percentage of direct observations (+ 95% confidence intervals)
of the behaviour recorded (i.e. alert, feeding, running or other) in rab-
bits in unfenced and fenced plots. Other behaviours included groom-
ing, sniffing and resting. *Indicates significant (P < 0.05) differences
between plots
J.Tobajas et al.
where terrestrial predators posed the primary predation
pressure (i.e. unfenced plot where foxes accounted for more
than twice the mortality caused by raptors, Rouco 2008),
rabbits tended to be in smaller groups, perhaps to reduce
predator attraction by reducing group prey odour. Larger
groups were only observed when rabbits needed to feed at a
greater distance from cover, likely because the vigilance of
group-mates increases the probability of detecting a preda-
tor (Roberts 1996). In the fenced plot, the presence of larger
groups could be an anti-predatory strategy against birds of
prey (Villafuerte and Moreno 1997), the only predators that
could access those rabbits. Individuals in larger groups can
enjoy the same or improved predator detection rate while
scanning less frequently and having more time to feed (e.g.
Roberts 1996).
In general, our results suggest that European rabbits seem
to adjust their behavioural responses according to the type of
perceived predation risk, in accordance with previous stud-
ies (Monterroso etal. 2013; Descalzo etal. 2021). These
results resemble those obtained by Monclús etal. (2009),
and therefore tend to agree with the threat-sensitive preda-
tor avoidance hypothesis. Notably, our study additionally
suggests that behavioural adaptations to reduce the preda-
tion risk can be adopted by rabbits in a short period of time
(i.e. ~ 3months). Complementarily, this study also reveals
that these adaptations extend beyond changes in activity
patterns previously observed (Monterroso etal. 2013; Mar-
tín-Díaz etal. 2018; Descalzo etal. 2021), encompassing
alterations in spatial utilisation and cooperative vigilance
behaviours. Finally, our results suggest that these adapta-
tions depend on the type of predator, the rabbits adjusting
their response as a function of whether they are being pre-
dated from the air or from the ground. It is remarkable that
in this experiment, rabbits were translocated, whose adapta-
tion is presumed more difficult than for rabbits born in the
study area. However, our results show the high plasticity
of this species to adapt to environmental conditions sig-
nificantly different from those of its place of origin (natural
population). These types of studies help wildlife managers to
implement conservation measures based on translocations,
since they show that prey species can have the ability to
quickly adapt to new environments, including different pre-
dation pressures (Descalzo etal. 2021). These results offer
new insights into the behavioural ecology of the European
rabbit, aiding the development of conservation strategies
for this threatened species (Villafuerte and Delibes-Mateos
2019).
Acknowledgements We thank E. Grosso and M. A. Puerta from Con-
federación Hidrográfica del Guadalquivir (M.M.A.) and P. González.
Special thanks go to C. Calvete, G. Calabuig, C. Iriarte, J. Castillo, R.
Estrada, A. Finque, I. Rouco, A. Linares, S. Luna, L. E. Mínguez, O.
Rodriguez, M. Reglero and J. Retamar for their help during the field
work.
Author contributions RV and CRZ did the conceptualization. JT, CCF,
MDM, RV and CRZ did the field work and investigation, JT and CRZ
did the data analyses, JT and CRZ wrote the main manuscript text and
prepared figures. All authors reviewed the manuscript.
Funding Funding for open access publishing: Universidad de Córdoba/
CBUA. Jorge Tobajas benefitted from a postdoctoral contract funded
by the University of Cordoba and the Consejería de Transformación
Económica, Industria, Conocimiento y Universidades of Junta de Anda-
lucía through the grants programme “Plan Andaluz de Investigación,
Desarrollo e Innovación (PAIDI 2020)”. C. Rouco Zufiaurre was sup-
ported by the Plan Propio grant funded by University of Córdoba.The
study was partially funded by the project PID2020114724RB-I00
(Spanish Ministerio de Ciencia Innovación y Universidades).
Data availability The data used in the article will be available on the
first author’s personal and/or Researchgate website, and additional
information may be requested from the corresponding authors upon
reasonable request.
Declarations
Conflict of interest Authors declare no conflicts of interests. One of
the authors of this article, C. Rouco Zufiaurre, is a member of the edi-
torial board of Mammalian Biology.
Ethical statement Since the present study was a strictly observational
research, no manipulations were carried out on any animals. The rabbit
translocation programme, upon which the present study is based, was
approved by the Ethical Committee for Animal Experimentation of the
University of Castilla-La Mancha and is in accordance with Spanish
and European regulations (Law 32/2007, R.D. 1201/2005, and Council
Directive 2010/63/EU).
Open Access This article is licensed under a Creative Commons Attri-
bution 4.0 International License, which permits use, sharing, adapta-
tion, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article are
included in the article’s Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
the article’s Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
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... Species modify their activity times to minimize exposure to perceived riskstermed risk allocation hypothesis (Lima and Bednekoff, 1999)while maintaining necessary resources (Baker et al., 2007;Dowding et al., 2010;Thomas et al., 2018). Species can deal with risk allocation in two ways ( Figure 1): Reducing total time while increasing activity intensity (Potash et al., 2023;Tobajas et al., 2024) or shifting the temporal niche to times of lower risk (Louvrier et al., 2022). Changes in the temporal niche can have different fitness consequences, they can reduce stress factors such as warming, but they can also have negative effects, for example if predators shift their activity to times when their prey is less active, or if the shift conflicts with the species' genetic predispositions (Spoelstra et al., 2016;Levy et al., 2019;Gilbert et al., 2023). ...
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