Download Prey naivete´ in an introduced prey species: the wild rabbit in Australia

Behavioral Ecology
doi:10.1093/beheco/arq103
Advance Access publication 30 June 2010
Prey naiveté in an introduced prey species: the
wild rabbit in Australia
Isabel C. Barrio,a C. Guillermo Bueno,b Peter B. Banks,c and Francisco S. Tortosaa
Department of Zoology, University of Córdoba, Campus de Rabanales Ed. Darwin, E-14071 Córdoba,
Spain, bDepartment of Conservation of Biodiversity and Ecosystem Restoration, Pyrenean Institute of
Ecology, Spanish National Research Council, E-22700 Jaca, Spain, and cEvolution and Ecology Research
Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney
NSW 2052, Australia
a
Early detection of predators by their prey is an essential element of antipredator tactics, and for many mammalian predator prey
interactions, detection comes mainly via a predators olfactory cues. The avoidance of predator odors can reduce the likelihood of
encountering predators and increases the chances of prey survival. However, the role of coevolutionary history in the exploitation
of odors in mammalian predator–prey interactions is not so well understood. The prey naiveté hypothesis predicts the lack of
effective antipredator behaviors given the lack of a coevolution between predator and prey but has so far been only tested
on native prey. In this study, we describe the short-time responsiveness of an introduced prey species, the European rabbit
(Oryctolagus cuniculus), to scents from coevolved and novel predators in Australia. We quantified rabbit activity rates by means of
pellet counting and activity indices based on footprints, in a series of experimental plots treated with predator odors, and both
methods yielded consistent results. Rabbits responded to coevolved predators by reducing their activity rates to scented experimental plots, whereas no avoidance was found for novel allopatric predators. These results suggest a shared evolutionary history
between the antipredatory responses of rabbits and their natural predators. Key words: antipredator response, avoidance behavior, coevolutionary history, Oryctolagus cuniculus, predation, space use. [Behav Ecol 21:986–991 (2010)]
he early detection of predators is a key strategy used by prey
to avoid a predation event. Although tactics of fleeing and
defense can be useful in fending off predators once an attack
has been made, avoidance strategies are predicted to have the
greatest influence on the outcome of a potential predation interaction (Endler 1993). In order to enact avoidance behavior,
potential prey must first detect a predation risk. This is typically in the form of either the predator itself or the potential
for predator presence. Although indirect cues such as environmental conditions (e.g., habitat structure, moonlight,
wind) can indicate possible predator presence (Orrock et al.
2004), more direct indicators of predator use of an area can
often allow prey to more efficiently balance the risks of predation with the costs of avoidance behavior (Kats and Dill
1998).
Many predatory carnivores use scent for territory marking,
individual, or intersexual recognition, regularly returning to
the focal points of scent marking. These scent points are
not only attractive to other predator individuals but are also
regularly inspected by the initial scent donor, creating a potential hot spot of predator activity (Wallach et al. 2009). However,
these signals are part of an open signaling system, and prey
individuals can eavesdrop on these signals to detect possible
predator presence (Endler 1993). Olfactory cues can be an
accurate indicator about risk of carnivore predation to the
potential prey even in the absence of the predator, and their
detection usually elicits the display of a behavioral response,
such as the direct avoidance of the odor, or temporal and
spatial activity modifications (Kats and Dill 1998). By avoiding
areas with these odors, potential prey may reduce the likeli-
T
Address correspondence to I.C. Barrio. E-mail: [email protected].
Received 27 May 2010; revised 3 June 2010; accepted 3
June 2010.
The Author 2010. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
hood of encountering predators and increase their chances of
survival, and thus, predator odor recognition may be an important adaptive trait.
The correct identification of which species pose predation
risk is also an important component of early detection. Avoidance behavior carries significant costs in terms of missed
opportunities of resource use, with flow-on consequences to individual fitness. Thus selection should favor refined detection
of predator identity. Despite this prediction, the response of
many prey species tends to be a generalized avoidance of
predator odors (Apfelbach et al. 2005) rather than a speciesspecific response to a particular predator, and requisite exposure in either evolutionary time or short-term experience
seems unnecessary (Hayes et al. 2006). The responsiveness
to scents from sympatric and allopatric predators seen in many
prey species suggests an innate reaction to a signal, which may
be common to carnivores (Dickman and Doncaster 1984).
The ‘‘common constituents hypothesis’’ (Nolte et al. 1994)
suggests that odors from predators share common compounds
that can be used by prey, even when predators are unfamiliar.
However, such generalization is not universal, and some prey
species do not necessarily recognize a potential predator odor
innately (e.g., see Blumstein et al. 2002). The ‘‘prey naiveté
hypothesis’’ predicts the existence of ineffective antipredator
defenses owing to the lack of an evolutionary history with
a given predator archetype (Cox and Lima 2006). The ability
of a prey species to detect and avoid predators may thus depend in part on the life history, ecology, and evolutionary
history of both predator and prey (Hayes et al. 2006). Thus,
although avoidance behaviors are species specific for some
predator–prey systems (Jedrzejewski et al. 1993) for a diversity
of other taxa, olfactory predator recognition may have to be
learned (Griffin et al. 2000; Blumstein 2002). In a similar way,
some antipredator behaviors to a given coevolved predator
may persist in evolutionary time even when the predator is
Barrio et al.
•
Rabbit responses to predator odors
missing, given the presence of other predators, as suggested
by the ‘‘multipredator hypothesis’’ (Blumstein 2006).
Most studies illustrating the role of coevolutionary history on
olfactory exploitation in predator–prey systems have focused
on the responses of native prey to the odors of introduced versus native predators (e.g., (Banks 1998; Blumstein et al. 2002;
Russell and Banks 2007), and little attention has been given to
prey species introduced to a novel environment in which they
face novel predation threats (but see Dickman 1992). In this
paper, we examine the predator detection and avoidance by
European rabbit (Oryctolagus cuniculus hereafter rabbit) in
Australia where it is an invasive introduced prey species
that poses serious threats to the conservation of Australian
ecosystems. The rabbit is a good model for studying prey detection of predation risk as predation is a major modifier of
rabbit dynamics in many systems (e.g., Newsome 1990; Banks
2000) and hence likely to be a strong selective force on strategies of predator avoidance. Rabbits use scent marking for
intraspecific communication and rely strongly on their olfactory sense (Mykytowycz 1968) to assess the territorial, sexual,
and social status of conspecifics. Rabbits do recognize and
react to coevolved predator odors (Monclús, Rödel, and Von
Holst 2006; Monclús, Rödel, Palme, et al. 2006), even if they
have not been exposed to them before (Boag and Mlotkiewicz
1994; Bakker et al. 2005; Monclús et al. 2005). However, no
study has tested specifically the response of rabbits as an alien
prey species to coevolved and novel predators in a novel place.
The European rabbit was introduced to Australia by the
European settlers, and the lack of natural predators is one
of the hypotheses supporting its successful colonizing ability
in mainland Australia (Myers et al. 1994). Foxes (Vulpes
vulpes), the archetypal enemy of rabbits, were not introduced
until 10 years after the initial rabbit introduction and rapidly
spread after the rabbit invasion. Foxes are major predators
of rabbits that can modify their population dynamics (Trout
and Tittensor 1989; Banks 2000). Cats (Felis catus) arrived with
Europeans in 1824 (Abbott 2002), after which they rapidly
spread across all of Australia but at relatively low densities
until rabbits arrived. Ferrets (Mustela furo) were introduced
to address the problem of rabbits in rural areas and were used
in localized rabbit control by hunters—there are only limited
naturalized populations of ferrets in mainland Australia yet
(Myers et al. 1994). All these predators, that is, foxes, cats,
and ferrets, share a long coevolutionary history with rabbits
in the Iberian Peninsula and represent 3 families of mammalian predators responsible for most predation on rabbits
(Jaksic and Soriguer 1981). In Australia, foxes and cats are
considered as opportunistic predators for which rabbits are
main prey item when available, representing up to 45% and
54% of their respective diets (Jones and Coman 1981; Catling
1988). On the other hand, upon their arrival, rabbits have
been subjected to predation from generalist mammal species
native to Australia, which are in evolutionary terms novel
predators for the rabbit, such as the spotted-tailed quoll
(Dasyurus maculatus), an opportunistic marsupial carnivore
that preys heavily upon rabbits when available (Glen and
Dickman 2006). All these make the European rabbit an ideal
experimental system for asking questions about the responsiveness of prey species to predators with which they share
a different evolutionary history.
In the present study, we investigate the short-term response
of European rabbits to the odors of coevolved and novel
predators using a field experiment. We used seedlings as an
attractant for rabbits because browsing damage to foliage by
rabbits is a common vegetation management problem (Marks
and Moore 1998). Nonlethal solutions to rabbit browsing
are increasingly becoming preferred management tools in
Australia, and the use of predator odors has the potential to
987
deter rabbit browsing (Apfelbach et al. 2005). We used odors
from fox (coevolved predator and sympatric in the study
area), cat (coevolved and sympatric), ferret (coevolved but
allopatric), and quoll (novel predator and allopatric) and
compared rabbit responses with a procedural control (water)
to answer the following questions: 1) Do rabbits avoid using
patches scented with predator odors and 2) are rabbits able to
discriminate between potential predators with which they
share a different evolutionary history? According to the predictions of the prey naiveté and the multipredator hypotheses,
rabbits should show avoidance responses to the odors of predators with which they have coevolved, whether they are locally
present or not, although no response is to be expected to the
odor of novel predators. On the contrary, a generalized response to predator odors is to be expected according to the
common constituent hypothesis.
MATERIALS AND METHODS
Study area and experimental design
The study was conducted at the Mallee Research Station, Walpeup (lat 3507#S, long 14201#E), north-western Victoria,
Australia. The area is primarily a wheat-growing region interspersed with large patches of remnant mallee woodland, which
is habitat to a range of endangered plants and wildlife; smaller
patches of this woodland also separate large wheat fields. Currently, rabbit populations are regularly controlled in the area
mainly by large-scale poisoning, but ferrets have not been used
in rabbit control in the area for more than 40 years if ever.
Foxes and cats are relatively common despite annual fox control efforts to reduce impacts on nearby lamb farms, whereas
quolls are absent and would have never occurred in the area.
Three sites were randomly selected within the study area separated by at least 1 km to ensure independence between sites.
Each site consisted of 5 plots (1 per treatment: 4 predator
odors and a procedural control) spaced at least 50 m apart,
so that odors applied in different experimental plots were unlikely to reach the other plots but ensuring that rabbits could
visit all plots within a site because rabbits normally use areas up
to 150 m apart from their warrens (Eldridge et al. 2006).
Within each plot, 25 seedlings were planted 2 m apart in a grid
(5 3 5 seedlings), and a treatment was randomly assigned to
each plot. Thus, 125 seedlings were planted on each site, 375
in total. Latex gloves were used to handle seedlings during
planting in order to prevent contaminating the plants with
human odor. A different treatment was applied to each of
the 5 plots within a site; on each plot, every second plant
was sprayed with the corresponding liquid, that is, predator
odor or water (procedural control), resulting in 13 sprayed
and 12 unsprayed seedlings per plot, to evaluate potential
differences between the large- and small-scale effects of predator odors on rabbits’ use of space. We used different spray
bottles to apply each treatment, and the whole plant foliage
was uniformly covered. All seedlings were hand watered, and
treatments (both, predator odors, and water) were reapplied
every second day to the corresponding seedlings. Around
each seedling, a circular sandplot (0.5 m2) was set to assess
rabbit daily activity rates by means of footprints. Therefore,
within each plot, we had 25 sandplots, 13 of them corresponding to sprayed seedlings and the remaining to unsprayed
seedlings.
Sandplots were checked each morning for the presence of
footprints for 7 days after plantation; plots were then raked after each assessment ensuring that only fresh footprints were
detected on each visit. Rabbit daily activity rates for each plot
and spraying level (sprayed or unsprayed) were then calculated
as the proportion of sandplots having fresh rabbit footprints on
Behavioral Ecology
988
each day. This allowed an assessment of how rabbits perceived
predation risks associated with discrete predator odor points at
the patch (i.e., seedling) level by comparing seedlings either
sprayed or not sprayed within a plot and thus reflect use of
space at a finer scale, that is, patch level.
To assess larger scale responses (i.e., plot level) to different
predator odors, which would occur if rabbits avoided areas with
high perceived predation risk, rabbit use of plots was assessed
using dung pellet counts. Immediately after setting each experimental site, the number of rabbit pellets was counted in 16
circular sampling units (0.5 m2) systematically located within
each plot to have a raw estimate of rabbit abundance in each
site (Taylor and Williams 1956). Abundance estimates for
each plot were pooled to allow a more robust initial estimate
of local rabbit abundance at each site. All pellets were removed after the initial count, and newly deposited pellets
were counted again in the same sampling units at the end
of the monitoring period when treatments were expected to
create smaller scale differences in rabbit use. An index of
rabbit use (RUij) was obtained for each plot i by correcting
the final abundance estimate by the initial estimate of rabbit
abundance in each site j to account for site differences in
initial abundances (n ¼ 15).
RUij ¼ final estimateij initial site estimatej :
Predator odors
A liquid extract of predator feces was used as the predator odor
source in order to standardize the delivery of odor cues to
plants. Predator feces were selected among the potential odor
sources, that is, urine, skin or fur, and anal gland secretions
(Apfelbach et al. 2005), to make our results more comparable
with other studies using rabbits as the prey species. We used 4
rabbit predator species: 3 coevolved predator species, red fox
(V. vulpes), ferret (M. furo), cat (F. catus), and a novel predator
species, the spotted-tailed quoll (D. maculatus). The liquid
extract was obtained following Fuelling and Halle (2004),
mixing 50 g of feces with 1 l water, left for about 2 h, and
filtered through coarse cloth to remove solid material. In the
experiment, the resulting liquid was distributed with spray
bottles by spraying a constant dose of liquid onto each treated
seedling. The application of predator odor as a topical spray
on a potential food source has been widely applied on trials to
prevent foraging damage by herbivores (e.g., Swihart 1991).
Feces of all predators were obtained from captive animals, all
of them being fed on a similar meat diet. Diet of predators
can modulate odor aversiveness to prey, but this seems to be
mediated by metabolites of meat digestion (Nolte et al. 1994;
Berton et al. 1998). Therefore, we ensured that all predators
were being fed meat. All feces were collected fresh and then
frozen at 220 C until shortly before use.
Data analysis: footprints and pellet counts
The effect of predator odors on rabbit daily activity rates was
evaluated using linear mixed models. Activity rates were first
log transformed to achieve normality, and the effect of plot
within sampling site was included in the model as a random
factor to account for the nestedness of the data. Odor treatment, spraying, and their interaction were included in the
fixed part of the model as predictor variables. Categorical variables were included in the models as dummy variables, and all
comparisons were made taking ‘‘control’’ and ‘‘unsprayed’’ as
the baseline level. Because the structure of the data corresponded to short-time series, that is, only 7 time points in each
series, data could be safely analyzed using mixed models that
assume a compound symmetry correlation structure, instead
of including more complex time correlation structures (Zuur
et al. 2009). Model selection was based on Akaike’s Information Criterion (AIC) and log-likelihood ratio tests using
maximum-likelihood estimation. Final models are presented,
which retained all significant terms and had lowest AIC (Zuur
et al. 2009), but nonsignificant terms removed during model
selection are also commented when relevant. All modeling
assumptions of normality, homogeneity of variances, and independence in the residuals were met.
Rabbit use indices as assessed by pellet counts were analyzed
using a Gaussian linear model after log transformation. Odor
treatment was included as the predictor variable, and being categorical was transformed into the corresponding dummy variable taking ‘‘control’’ as the baseline level for all comparisons.
Sampling site effect was not included as a random factor because it did not significantly improve the model (P ¼ 0.500;
P value is corrected here for ‘‘testing on the boundary,’’ as
suggested by Verbeke and Molenberghs 2000).
All statistical analyses were performed with R 2.10.1 (R
Development Core Team 2009).
RESULTS
Rabbit footprints
Rabbit daily activity rates, that is, the proportion of sandplots
that recorded fresh rabbit footprints, varied widely (median ¼
0.08, interquartile range ¼ 0.25; range ¼ 0–1). The final model
for rabbit activity rates retained only the treatment applied that
had a significant effect (log-likelihood ratio ¼ 11.926, P ¼
0.018), with all predator odors having lower rabbit activity
rates than the procedural control (Figure 1a). However, activity rates in quoll-scented plots did not differ significantly from
those in the control (t value ¼ 20.647, P ¼ 0.536). Spraying
level, that is, if the seedling was directly sprayed or not, did
not have a significant effect on rabbit activity rates (loglikelihood ratio ¼ 0.769, P ¼ 0.381), indicating no small-scale
effects of predator odors on rabbits’ use of space, although
rabbits responded to odors at a wider scale, that is, the plot
level. In the same way, the interaction between spraying level
and treatment was not statistically significant (log-likelihood
ratio ¼ 1.902, P ¼ 0.754), showing that the lack of response
to predator odors at a fine scale was consistent across odor
treatments.
Pellet counts
Rabbit use indices obtained with pellet counts also indicated
a wide variation in rabbit use of the different experimental
plots (median ¼ 0.02 pellets/m2day; interquartile range ¼
0.04; range ¼ 0.00–0.12; n ¼ 15). Odor treatment had a significant effect on rabbit use (F ¼ 8.074, degrees of freedom ¼
4,10, P ¼ 0.004). According to these rabbit use indices, control plots had higher rabbit use than predator-scented plots
(Figure 1b) but did not significantly differ from quoll-scented
plots (t value ¼ 21.731, P ¼ 0.114).
DISCUSSION
Our results indicate that rabbits respond to the odors of their
natural coevolved predators by reducing the use of scented
plots, whereas no significant avoidance is detected when exposed to novel allopatric predators. It is known that rabbits
are able to recognize predators by means of their odors and
display both behavioral and physiological responses (Monclús,
Rödel, and Von Holst 2006; Monclús, Rödel, Palme, et al.
2006), but no such responses are found when rabbits are
confronted to nonpredator odors (Monclús et al. 2005).
•
Rabbit responses to predator odors
Footprints
Pellet counts
b)
a
a
ab
b
b
b
b
b
−2.5
b
rabbit use
−1.6
−1.2
−1.5
a
−2.0
rabbit daily activity rate
−0.8
a)
989
−2.0
Barrio et al.
control
ferret
fox
quoll
control
treatment
However, what rabbits perceive as a potential predator needs
to be discussed. Previous studies have used odor sources from
predators with which rabbits share a long coevolutionary history, such as the red fox (V. vulpes) (Monclús et al. 2005;
Monclús, Rödel, and Von Holst 2006) or mink (M. vison)
(Bakker et al. 2005), a species known to occasionally prey
upon rabbits and closely related to a major natural predator
of rabbits, that is, the polecat (M. putorius). In our study,
rabbits effectively avoided areas treated with the odors of 3
predators of rabbits that are common within their native
range: foxes, cats, and ferrets. However, only foxes and cats
were present in the study area. Since their introduction
in Australia, rabbits have been exposed to heavy predation
by cats and foxes that can even regulate their numbers
(Newsome et al. 1989; Pech et al. 1992) and to a lesser extent
to ferreting. Thus, a response to fox and cats’ olfactory cues,
both coevolved sympatric predators, is to be expected. According to the predictions of the multipredator hypothesis
(Blumstein 2006), the presence of any predator may be sufficient to maintain antipredator behaviors for missing predators. Therefore, the ability to recognize a former predator as
such may persist as long as there is some exposure to any
predators. This would explain rabbits’ response to ferret odor
even though this species is allopatric in the study area.
In contrast, rabbits did not avoid areas contaminated by the
odor of quoll, a generalist marsupial carnivore that preys upon
rabbits where both coexist (Glen and Dickman 2006) but
which do not share an evolutionary history with rabbits. Quoll
feces have been used under other experimental settings and
have shown to elicit avoidance responses by native Australian
rodents to which quolls are familiar predators (Hayes et al.
2006; Russell and Banks 2007). Although rabbits are generally
uncommon in areas where quolls occur, they can represent up
to 35% of quolls’ diet when they coexist (Belcher 1995) and
therefore may pose a potential threat to rabbits. Weaker responses of prey species to quoll feces compared with those of
other predators have been related to the use of latrines by
quolls, which may serve other functions than scent marking
alone and may convey lesser information on predation risk to
the potential prey (Dickman 1992).
The lack of significant avoidance we found can be due to the
absence of quolls in the study area reflecting a lack of exposure
in ecological as well as evolutionary time. The lack of recognition of quolls as predators supports the idea proposed by the
prey naiveté hypothesis (Cox and Lima 2006); when facing
a novel source of predation risk, predation sensitive behaviors
ferret
treatment
fox
quoll
Figure 1
Rabbit use of plots at the different treatments applied, as
assessed by (a) footprints (rabbit daily activity rate log transformed) and (b) pellet counts
(rabbit use index log transformed). Lower case letters indicate significant differences
between groups of responses:
a ¼ no avoidance, b ¼ avoidance, and ab ¼ mixed situation. Vertical dashed lines
separate the control from the
predator-scented treatments
for ease of visualization.
may not even be performed (Banks and Dickman 2007). It has
been suggested that olfactory predator recognition may need
to be learned for some species (Griffin et al. 2000; Blumstein
2002). This has been demonstrated for marsupial prey species
(Blumstein et al. 2002) but has failed for placental prey species, such as the yellow-bellied marmot (Marmota flaviventris;
(Blumstein et al. 2008). In the latter study, marmots did not
respond differently to familiar and novel predators, but they
were presented with novel predator odors from 2 species of
placental predators, belonging to 2 different families within
the same taxonomic order. It is known that odors derived
from anal gland secretions are informative phylogenetically
(Bininda-Emonds et al. 2001), and thus, odors from individuals of the same order might be more closely related than
those from different higher taxonomic levels.
The prey naiveté hypothesis (Cox and Lima 2006) suggests
that predator archetypes, that is, a set of predator species
that use similar behavioral and morphological adaptations
in obtaining prey, might be determined at the family level.
Predators representing a different predator archetype to a coevolved predator would not elicit any antipredator responses.
Marsupial predators may differ from placental predators in
some unknown but key behavioral traits, thus representing
different predator archetypes (Cox and Lima 2006). For
instance, Australian native predatory taxa might have been
evolutionarily isolated long enough to produce unique archetypes because the continent did not participate fully in the
faunal exchanges of the past several million years (Cox and
Lima 2006). In the same sense, the only study on the response
of rabbits to the odor of a novel allopatric predator species
was that of Boag and Mlotkiewicz (1994), where they used
a lion feces–based chemical repellent. Rabbit avoidance of
areas treated with such repellent can be explained by a more
generalized response to felid odors, as also shown by our
results where rabbits responded to cat’s feces because they
would represent the same predator archetype.
Our results contradict to some extent the ‘‘common constituent hypothesis’’ (Dickman and Doncaster 1984; Nolte et al.
1994), according to which, there is a general nonspecific carnivorous odor that prey are able to assess as a perilous signal.
This olfactory cue has been suggested to be sulfurous compounds associated with meat digestion. However, we found
that rabbits did not avoid quoll-scented patches, a hypercarnivore with an extremely high proportion of meat in its diet
(Glen and Dickman 2006). A recent study revealed that the
odor profiles of urine and feces of marsupial predators differ
Behavioral Ecology
990
significantly from those of placental ones (Russell 2005), suggesting that the common constituent hypothesis may only
apply for closely related taxonomic levels, that is, at the family
level.
Avoidance behaviors reduce the probabilities of encounters
with predators (Lima and Dill 1990) and are a widespread
response of mammalian prey species to predator odor cues
(Kats and Dill 1998). However, some studies have failed in
recording avoidance behaviors in response to perceived predation risk (Jonsson et al. 2000), but this might be a scale
effect. Recently, Lima (2002) suggested that olfactory communicating species use scale-sensitive antipredatory behavioral
changes. Foraging theory predicts that predation risk can operate at multiple spatial scales, and thus, to best measure
behavioral shifts by prey, several scales should be accounted
for (Hughes and Banks 2010). In this sense, we detected no
avoidance responses at a small scale, that is, rabbits did not
avoid directly sprayed seedlings, whereas such responses were
evident at a wider scale (plot level effect), as assessed by both
pellet counts and footprint records. This can be related to
rabbits’ perception of predation risk and the distances they
venture into risky patches. In a study conducted in Southern
Spain, Villafuerte and Moreno (1997) found that rabbits foraged further from cover when perceived predation risk was
counteracted by bigger group sizes, whereas individual
rabbits foraged less than 5 m away from cover. Our results
here indicate that the small distances between seedlings with
and without predator odors (2 m) do not carry different predation risks, and rabbits treated scented plots as risky patches
as a whole, consistent with the scale at which risk from these
predators would occur.
Most studies testing the prey naiveté hypothesis have focused
on the responses of prey to alien predators (Banks 1998;
Blumstein et al. 2002; Russell and Banks 2007). Only one
study has evaluated the responses of an introduced prey
(Dickman 1992), but our study is the first to specifically test
the predictions of the prey naiveté on rabbits, an invasive introduced prey species, to which native predators that may
represent a novel threat. Our results suggest a shared evolutionary history between the antipredatory responses of rabbits
and their natural predators, whereas no such responses are
shown when presented with an unfamiliar potential predator
as predicted by the prey naiveté hypothesis. However, further
research is warranted, and new experimental settings will
likely provide useful insights. For instance, using other olfactory stimuli such as predator urine or fur will help in
disentangling the mechanisms underlying predator odor recognition by wild rabbits. As well, studying rabbits’ response to
other novel predators under similar or different scenarios
(i.e., in sympatry) will improve the understanding of the role
of shared evolutionary history in the olfactory recognition of
predators by rabbits.
FUNDING
Predoctoral fellowship to I.C.B. from the Spanish Ministry of
Science and Innovation that covered a short stay abroad, during which this project was conducted; Australian Research
Council Discovery Grants (University of New South Wales)
DP0881455 and DP0877585 to P.B.B.
We are grateful to C. Price for her help in the field, to the NSW Ferret
Society and Featherdale Wildlife Park for kindly providing scat samples, and to the Mallee Research Station for their hospitality. R. Monclús and the people in Banks’ lab provided useful comments that
greatly improved previous versions of the manuscript, and S. Petrovan
kindly helped with the final version. Special thanks to D. Blumstein, H.
Hofmann, and an anonymous reviewer for their encouraging and help-
ful comments. Part of this work was presented at the Mammal Society
Conference 2010 and was awarded the Acorn Prize for the best student
presentation.
REFERENCES
Abbott I. 2002. Origin and spread of the cat, Felis catus, on mainland
Australia, with a discussion of the magnitude of its early impact on
native fauna. Wildl Res. 29:51–74.
Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS.
2005. The effects of predator odors in mammalian prey species:
a review of field and laboratory studies. Neurosci Biobehav Rev.
29:1123–1144.
Bakker ES, Reiffers RC, Olff H, Gleichman JM. 2005. Experimental
manipulation of predation risk and food quality: effect on grazing
behaviour in a central-place foraging herbivore. Oecologia. 146:
157–167.
Banks PB. 1998. Responses of Australian bush rats Rattus fuscipes, to
the odor of introduced Vulpes vulpes. J Mammal. 79:1260–1264.
Banks PB. 2000. Can foxes regulate rabbit populations? J Wildl Manage. 64:401–406.
Banks PB, Dickman CR. 2007. Alien predator and the effects of multiple levels of prey naiveté. Trends Ecol Evol. 22:229–230.
Belcher CA. 1995. Diet of the tiger quoll (Dasyurus maculatus) in East
Gippsland, Victoria. Wildl Res. 22:341–357.
Berton F, Vogel E, Belzung C. 1998. Modulation of mice anxiety in
response to cat odor as a consequence of predators diet. Physiol
Behav. 65:247–254.
Bininda-Emonds ORP, Decker-Flum DM, Gittleman JL. 2001. The utility of chemical signals as phylogenetic characters: an example from
the Felidae. Biol J Linn Soc. 72:1–15.
Blumstein DT. 2002. Moving to suburbia: ontogenetic and evolutionary consequences of life on predator-free islands. J Biogeogr.
29:685–692.
Blumstein DT. 2006. The multipredator hypothesis and the evolutionary persistence of antipredator behaviour. Ethology. 112:209–217.
Blumstein DT, Barrow L, Luterra M. 2008. Olfactory predator discrimination in yellow-bellied marmots. Ethology. 114:1135–1143.
Blumstein DT, Mari M, Daniel JC, Ardron JG, Griffin AS, Evans CS.
2002. Olfactory recognition: wallabies may have to learn to be wary.
Anim Conserv. 5:87–93.
Boag B, Mlotkiewicz JA. 1994. Effect of odor derived from lion faeces
on behavior of wild rabbits. J Chem Ecol. 20:631–637.
Catling PC. 1988. Similarities and contrasts in the diets of foxes,
Vulpes vulpes, and cats, Felis catus, relative to fluctuating prey populations and drought. Aust Wildl Res. 15:307–317.
Cox JG, Lima SL. 2006. Naiveté and aquatic-terrestrial dichotomy in
the effects of introduced predators. Trends Ecol Evol. 21:674–680.
Dickman CR. 1992. Predation and habitat shift in the house mouse,
Mus domesticus. Ecology. 73:313–322.
Dickman CR, Doncaster CP. 1984. Responses of small mammals to
Red fox (Vulpes vulpes) odour. J Zool. 204:521–531.
Eldridge DJ, Constantinides C, Vine A. 2006. Short-term vegetation
and soil responses to mechanical destruction of rabbit (Oryctolagus
cuniculus L.) warrens in an Australian box woodland. Restor Ecol.
14:50–59.
Endler JA. 1993. Some general comments on the evolution and design
of animal communication systems. Philos Trans R Soc Lond B Biol
Sci. 340:215–225.
Fuelling O, Halle S. 2004. Breeding suppression in free-ranging greysided voles under the influence of predator odour. Oecologia.
138:151–159.
Glen AS, Dickman CR. 2006. Diet of the spotted-tailed quoll (Dasyurus
maculatus) in eastern Australia: effects of season, sex and size.
J Zool. 269:241–248.
Griffin AS, Blumstein DT, Evans CS. 2000. Training captive-bred
or translocated animals to avoid predators. Conserv Biol. 14:
1317–1326.
Hayes RA, Nahrung HF, Wilson JC. 2006. The response of native
Australian rodents to predator odours varies seasonally: a by-product of life history variation? Anim Behav. 71:1307–1314.
Hughes NK, Banks PB. 2010. Interacting effects of predation risk and
signal patchiness on activity and communication in house mice.
J Anim Ecol. 79:88–97.
Barrio et al.
•
Rabbit responses to predator odors
Jaksic FM, Soriguer RC. 1981. Predation upon the European rabbit
(Oryctolagus cuniculus) in Mediterranean habitats of Chile and
Spain: a comparative analysis. J Anim Ecol. 50:269–281.
Jedrzejewski W, Rychlik L, Jedrzejewska B. 1993. Responses of bank
voles to odours of seven species of predators: experimental data and
their relevance to natural predator-vole relationships. Oikos. 68:
251–257.
Jones E, Coman BJ. 1981. Ecology of the feral cat, Felis catus (L.), in
south-eastern Australia I. Diet. Aust Wildl Res. 8:537–547.
Jonsson P, Koskela E, Mappes T. 2000. Does risk predation by mammalian predators affect the spacing behaviour of rodents? Two
large-scale experiments. Oecologia. 122:487–492.
Kats LB, Dill LM. 1998. The scent of death: chemosensory assessment
of predation risk by prey animals. Écoscience. 5:361–394.
Lima SL. 2002. Putting predators back into behavioral predator-prey
interactions. Trends Ecol Evol. 17:70–75.
Lima SL, Dill LM. 1990. Behavioral decisions made under the risk of
predation: a review and prospectus. Can J Zool. 68:619–640.
Marks CA, Moore SJ. 1998. Nursery practices influence comparative
damage to juvenile blue gum by wallabies (Wallabia bicolor) and
European rabbits (Oryctolagus cuniculus). For Ecol Manage. 112:1–8.
Monclús R, Rödel HG, Palme R, Von Holst D, De Miguel J. 2006. Noninvasive measurement of the physiological stress response of wild
rabbits to the odour of a predator. Chemoecology. 16:25–29.
Monclús R, Rödel HG, Von Holst D. 2006. Fox odour increases vigilance in European rabbits: a study under semi-natural conditions.
Ethology. 112:1186–1193.
Monclús R, Rödel HG, Von Holst D, De Miguel J. 2005. Behavioural
and physiological responses of naı̈ve European rabbits to predator
odour. Anim Behav. 70:753–761.
Myers K, Parer I, Wood D, Cooke BD. 1994. The rabbit in Australia. In:
Thompson HV, King CM, editors. The European rabbit: the history
and biology of a successful colonizer. Oxford: Oxford Science
Publications. p. 108–157.
Mykytowycz R. 1968. Territorial marking by rabbits. Sci Am. 218:
116–126.
Newsome AE. 1990. The control of vertebrate pests by vertebrate
predators. Trends Ecol Evol. 5:187–191.
991
Newsome AE, Parer I, Catling PC. 1989. Prolonged prey suppression by
carnivores—predator-removal experiments. Oecologia. 78:458–467.
Nolte DL, Mason JR, Epple GM, Aronov E, Campbell DL. 1994.
Why are predator urines aversive to prey? J Chem Ecol. 20:
1505–1516.
Orrock JL, Danielson BJ, Brinkerhoff RJ. 2004. Rodent foraging is
affected by indirect, but not by direct, cues of predation risk. Behav
Ecol. 15:433–437.
Pech RP, Sinclair ARE, Newsome AE, Catling PC. 1992. Limits to
predator regulation of rabbits in Australia: evidence from predator-removal experiments. Oecologia. 89:102–112.
R Development Core Team. 2009. R: a language and environment for
statistical computing. Vienna (Austria): Austria R Foundation for
Statistical Computing.
Russell BG. 2005. The role of odour in Australian mammalian predator/prey interactions. Sydney: University of New South Wales.
Russell BG, Banks PB. 2007. Do Australian mammals respond to native
and introduced predator odours? Austral Ecol. 32:277–286.
Swihart RK. 1991. Modifying scent-marking behavior to reduce woodchuck damage to fruit trees. Ecol Appl. 1:98–103.
Taylor RH, Williams RM. 1956. The use of pellet counts for estimating
the density of populations of the wild rabbit, Oryctolagus cuniculus
(L.). N Z J Sci Technol. 38:236–256.
Trout RC, Tittensor AM. 1989. Can predators regulate wild rabbit
Oryctolagus cuniculus population density in England and Wales?
Mammal Rev. 19:153–173.
Verbeke G, Molenberghs G. 2000. Linear mixed models for longitudinal data. New York: Springer.
Villafuerte R, Moreno S. 1997. Predation risk, cover type and group
size in European rabbits in Doñana (SW Spain). Acta Theriol.
42:225–230.
Wallach AD, Ritchie EG, Read J, O’Neill AJ. 2009. More than mere
numbers: the impact of lethal control on the social stability of a toporder predator. PLoS One. 4:e6861.
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM. 2009. Mixed
effects models and extensions in ecology with R. New York:
Springer.