Survey
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
* Your assessment is very important for improving the workof artificial intelligence, which forms the content of this project
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.