Implications of shared predation for space use in two sympatric leporids

Abstract Spatial variation in habitat riskiness has a major influence on the predator–prey space race. However, the outcome of this race can be modulated if prey shares enemies with fellow prey (i.e., another prey species). Sharing of natural enemies may result in apparent competition, and its implications for prey space use remain poorly studied. Our objective was to test how prey species spend time among habitats that differ in riskiness, and how shared predation modulates the space use by prey species. We studied a one‐predator, two‐prey system in a coastal dune landscape in the Netherlands with the European hare (Lepus europaeus) and European rabbit (Oryctolagus cuniculus) as sympatric prey species and red fox (Vulpes vulpes) as their main predator. The fine‐scale space use by each species was quantified using camera traps. We quantified residence time as an index of space use. Hares and rabbits spent time differently among habitats that differ in riskiness. Space use by predators and habitat riskiness affected space use by hares more strongly than space use by rabbits. Residence time of hare was shorter in habitats in which the predator was efficient in searching or capturing prey species. However, hares spent more time in edge habitat when foxes were present, even though foxes are considered ambush predators. Shared predation affected the predator–prey space race for hares positively, and more strongly than the predator–prey space race for rabbits, which were not affected. Shared predation reversed the predator–prey space race between foxes and hares, whereas shared predation possibly also released a negative association and promoted a positive association between our two sympatric prey species. Habitat riskiness, species presence, and prey species’ escape mode and foraging mode (i.e., central‐place vs. noncentral‐place forager) affected the prey space race under shared predation.


| INTRODUC TI ON
In the behavioral response race between predators and their prey (Sih, 2005), predators select locations and times in response to the use of space by prey (Laundré, 2010), resulting in "risky places" and "risky times" (Creel, Winnie, Christianson, & Liley, 2008, i.e., land-scape of fear, Laundré, Hernández, & Altendorf, 2001), whereas prey in turn often select locations and times to avoid these risky places and times (Lima & Dill, 1990) (Figure 1a). The predator-prey space race, based on game theory, is affected by fear imposed by the habitat or the "inherent riskiness of the habitat" (sensu Hugie & Dill, 1994), which is determined by the habitat characteristics that affect the probabilities of attack and escape (Bednekoff & Lima, 1998).
The habitat characteristics that determine the probability of an attack (i.e., pre-encounter risk) are not necessarily the same habitat characteristics that determine the probability of escape from a predator (i.e., postencounter risk) (Gorini et al., 2012). For example, open habitats with low vegetation density, little cover, or short vegetation provide high visibility for the prey and facilitate movement or escape (Gorini et al., 2012;Lima, 1992), however, they have low possibilities for hiding and concealment. In contrast, more closed habitats have low visibility for the prey and hinder movement or escape, however, they have more possibilities for hiding and concealment (Wirsing, Cameron, & Heithaus, 2010). As a result, spatial variation in habitat riskiness has a major influence on the relation between the use of space by prey and predators (Chesson, 2000); however, its outcome can be modulated if prey shares enemies with fellow prey (i.e., another prey species). Sharing of natural enemies by different prey species is common in natural communities (Chaneton & Bonsall, 2000). It may result in apparent competition, an indirect effect in which a given prey species experiences more predation risk resulting from the presence of fellow prey (Holt, 1977(Holt, , 2009. Competition for enemy-free space causes prey species to avoid risky places and times as a result of the presence of fellow prey, that is, short-term apparent competition or aggregative response (Holt & Kotler, 1987;Holt & Lawton, 1994).
The effect of a shared predator on each prey species, among others, depends on the amount of resource overlap and spatial overlap between prey species, and the riskiness of the habitat (DeCesare, Hebblewhite, Robinson, & Musiani, 2010). Additionally, differences in prey escape strategy (e.g., the use of refuges), predator type, and the density of additional prey and predators that influence the probability of an encounter and/or the subsequent probability of an attack can affect the response of prey to shared predation (Carbone & Gittleman, 2002;Holley, 1993).
However, the implications of shared predation on prey space use remain poorly studied (Chaneton & Bonsall, 2000). In particular, more insight is needed on the fine-scale space use by prey and predator species as a result of the interaction between habitat riskiness and the presence or absence of shared predation (see e.g., Camacho, Sáez-Gómez, Potti, & Fedriani, 2017). Spatial variation in habitat riskiness, for example, can prevent depensatory predation and extinction of prey (Sinclair et al., 1998). However, the effect of spatial variation in habitat riskiness on the relation between the use of space by prey that share a predator is not well understood (DeCesare et al., 2010;Oliver, Luque-Larena, & Lambin, 2009;Wirsing et al., 2010). Therefore, our objective was to test how prey species spend time among habitats that differ in riskiness, and how shared predation modulates the space use by prey species.

| S TUDY SYS TEM
We used a one-predator, two-prey system composed of the European hare (Lepus europaeus, Pallas, 1778) and European rabbit (Oryctolagus cuniculus, Linnaeus, 1758) as sympatric prey species and the red fox (Vulpes vulpes, Linnaeus, 1758) as their main predator.
We used European hare as the focal species and rabbit as the fellow prey species and vice versa to investigate prey space use. Rabbits are social central-place herbivores and prefer edge habitat near grasslands (Bakker, Reiffers, Olff, & Gleichman, 2005;Barnes & Tapper, 1986), such as coastal dune habitat. The hare is a solitary noncentral-place herbivore that is common in open grassland areas (Barnes & Tapper, 1986), such as agricultural (Smith, Jennings, & Harris, 2005), and coastal habitat (Kuijper & Bakker, 2008). Although there is considerable spatial overlap in habitat use between rabbits and hares (Flux, 2008), their habitat-specific escape modes differ markedly. Rabbits use their burrows to escape predation risk. According to Bakker et al. (2005), rabbit space use is not affected by habitat riskiness or predation risk. In contrast, the effect of hare predation has been suggested to depend on the available vegetation structure, cover, and openness of the landscape (Focardi & Rizzotto, 1999;Smith et al., 2005). Hares are known to use tall vegetation as cover or resting places (Neumann, Schai-Braun, Weber, & Amrhein, 2011).
Additionally, hare space use is sometimes positively or negatively related to edge habitats (Bresinski, 1983;Caravaggi, Montgomery, & Reid, 2015), presumably depending on the associated riskiness of F I G U R E 1 Conceptual representation of the relationship between space use by prey and that of their predators: (a) single prey predator system with prey (P) and predator (E), (b) predator two-prey system with asymmetrical apparent competition between two prey species (P R = rabbit; P H = hare) that share a common predator (i.e., red fox) (adjusted from Chaneton & Bonsall, 2000). Solid lines are direct effects; dashed lines are indirect effects. Arrows point toward dependent entity. Negative magnitudes indicate spatial avoidance by prey; positive magnitudes indicate spatial aggregation by predator. Arrow widths indicate the relative strength of the effects E P + - the habitat. Hares stand up to predators and can make use of crypsis and flight (Focardi & Rizzotto, 1999). Foxes can substantially impact hare and rabbit populations (Banks, 2000;Schmidt, Asferg, & Forchhammer, 2004); however, foxes often prefer rabbits over other species (Díaz-Ruiz et al., 2011;Norbury, 2001;Smith & Quin, 1996).
Red fox is known to make use of linear landscape features (Frey & Conover, 2006), and select for ecotones and habitats with protective cover (Kiener & Zaitsev, 2010) to ambush prey (Holley, 1993); however, foxes can also make use of open areas. We hypothesize that the habitat riskiness perceived by prey species is low in habitats in which predators are inefficient in searching or capturing prey species, such as structurally complex habitats (Hugie & Dill, 1994).
Therefore, we expect prey species to perceive low risk in habitats with protective cover (e.g., areas with tall shrubs and half-open vegetation structures). Besides, we expect prey species to perceive low risk in nonedge habitats, because foxes are efficient in capturing (i.e., ambush) mobile prey using cover that can be associated with edges (Holley, 1993). Even though there is a lack of knowledge on species edge responses, edge habitats affect perceived predation risk by prey species differently than nonedge habitats, because many terrestrial predators probably hunt more effectively along habitat edges, increasing predation (Lesmeister, Nielsen, Schauber, & Hellgren, 2015;Lidicker, 1999;Tscharntke et al., 2012).
For example, a change in the plant species composition could lead to an increase or decrease in preferred food plants available for hares F I G U R E 2 Location of the three study areas with fox, hare, and rabbit populations: Vennewater (VW), Koningsbos (KB), and Infiltration area Castricum (ICAS) (Kuijper & Bakker, 2008;Whinam, Fitzgerald, Visoiu, & Copson, 2014). Moreover, the interspecific interaction between hares and rabbits may also be affected by differences in body size, feeding style, digestive system, and morphology (Bell, 1971;Prins & Olff, 1998). Hares are twice as large as rabbits and have a relatively larger bite size. In comparison to rabbits, hares forage less efficiently on short vegetation and require taller vegetation to obtain their absolute daily energy requirements (Shipley, 2007). Habitat modification by rabbits could reduce hare foraging efficiency, leading to exploitative competition. The smaller rabbits may thus have a competitive advantage over hares in terms of resource exploitation (Persson, 1985), because they are central-place foragers that are more ecologically specialized (Flux, 2008;Shipley, 2007).
Because of the stronger competitive ability of the rabbit and the ability of the rabbit to use its burrow as a predator-free space, we hypothesize that the effect of shared predation on the space use by the two prey species is asymmetric in favor of the rabbit (i.e., apparent competition). Such asymmetric indirect effects are often observed in one-predator, two-prey systems when prey species differ in prey characteristics (Chaneton & Bonsall, 2000). Therefore, we expect that the indirect effects of rabbits on hares are stronger than the indirect effects of hares on rabbits ( Figure 1b). Hence, we investigated the following hypothesis: space use by hares is more strongly negatively affected by shared predation than space use by rabbits.

| ME THODS
We conducted field work in the coastal dune landscape   (Trewhella, Harris, & McAllister, 1988), the fox density in this coastal dune landscape was estimated to be very high, between five and eight individuals per square kilometer (Mulder, 2005).

| Space use and habitat riskiness
To study space use, we distinguished four vegetation strata that were related to habitat riskiness. First, we made a distinction be-  (Lidicker, 1999). We chose these dimensions, because  We considered prey species to perceive low risk in patches with tall shrubs. Cameras were set to record a burst of 10 photos (1 s −1 ) when triggered, without any time lapse between bursts.
We quantified residence time by hares, rabbits, and foxes as an index of fine-scale space use (T). We visually assessed residence time of a visit from sequences of camera trap photos. Sequences of trap photos without a quiet period longer than 120 s were defined as visits. Because the average visit of hares, rabbits, and foxes was much shorter than 120 s (Supporting Information Table S3), this seemed justified. We calculated average residence time per visit as a prey response to predation risk (e.g., Fortin et al., 2009;Visscher, Merrill, & Martin, 2017), because in contrast to the total residence time, the average residence time is independent of the frequency a species visits a camera location. The average prey residence time thus differentiates between many quick visits (i.e., high risk) and several longer visits (i.e., low risk) that could add up to the same total residence time. In a similar fashion, the average predator residence time differentiates between many quick visits (i.e., low risk) and several longer visits (i.e., high risk). We corrected residence time for the effective detection area, total deployment time of each camera and speed (Equation (1)).

| Data analysis
We investigated prey space use by selecting camera locations that captured the species under investigation on at least one occasion. Potential effects of undetected foxes were considered negligible, because camera detection correlates positively with body mass and average residence time in front of a camera (Rowcliffe et al., 2011).
Effects of species avoiding camera patches, however closely present to a camera, were also considered negligible, because we investigated fine-scale effects of predation risk in front of the camera (±10-25 m 2 ), whereas rabbits and hares experience a change in risk over distances smaller than 12 m (Crowell et al., 2016;Neumann et al., 2011;Rizzotto & Focardi, 1997 To compare datasets and assess whether and how shared predation affected prey space use, we additionally tested the effects of (a) the average residence time of fellow prey, (b) the interaction between the average residence time of fellow prey and predators, and (c) the interaction between the average residence time of fellow prey and habitat riskiness on the prey average residence time.
We hypothesized that hares and rabbits perceived a high risk with an increase in the fellow prey average residence time that can increase predation risk for prey with a shared predator (Holt, 2009).
Moreover, we hypothesized that risk associated with fellow prey average residence time depended on predator space use and the habitat riskiness (Kuijper et al., 2015).
We assessed the prey average residence time by running linear mixed models (lmer, R Package lme4 version 1.  (Gelman, 2008).
The data points of the standardized predictor variables were within two standard deviations from the mean. We verified the assumptions by visual inspection and plotted the residuals against the predicted values. Finally, we corrected for the false discovery rate in each dataset by a simple sequential Bonferroni-type procedure (Benjamini & Hochberg, 1995). Habitat riskiness perceived by prey species is low in habitats in which predators are inefficient in searching or capturing prey species such as structurally complex habitats Closed habitats have more possibilities for hiding and concealment. We expect prey species to perceive low risk in habitats with protective cover (e.g., areas with tall shrubs and half-open vegetation structures). Hugie and Dill (1994) and Wirsing et al. (2010) We expect prey species to perceive low risk in nonedge habitats, because foxes are efficient in capturing (i.e., ambush) mobile prey using cover that can be associated with edges. Edge habitats affect perceived predation risk by prey species differently than nonedge habitats, because many terrestrial predators probably hunt more effectively along habitat edges, increasing predation. Holley (1993), Lidicker (1999), Tscharntke et al. (2012), and Lesmeister et al.

| Effects of predator and habitat on prey residence time
2 The effect of shared predation on the space use by hare and rabbit is asymmetric in favor of the rabbit, that is, space use by hares is more strongly negatively affected by shared predation than space use by rabbits.
Intense grazing by rabbits can change the plant species composition, vegetation height, and perceived predation risk, thereby affecting the interaction between hares and rabbits Bakker et al. (2007) and Shipley (2007) Hares are twice as large as rabbits and have a relatively larger bite size. In comparison to rabbits, hares forage less efficiently on short vegetation and require taller vegetation to obtain their absolute daily energy requirements Shipley (2007) In contrast to hares, rabbits can use a refuge (i.e., burrow) as a predator-free space Asymmetric indirect effects are often observed in one-predator, two-prey systems when prey species differ in prey characteristics Chaneton and Bonsall (2000) 3 Hares and rabbits perceived a high risk when fox average residence time increased Prey perceives more risk when a predator spends on average more time in a patch Lima and Dill (1990) 4 Risk associated with fox total residence time was depended on the habitat riskiness (i.e., context dependent) Predation risk and habitat riskiness interact to affect prey response Kuijper et al. (2015) 5 Hares and rabbits perceived a high risk with an increase in the fellow prey average residence time Prey perceives more risk when fellow prey that increase predation risk spends on average more time in a patch Holt (2009) 6 Risk associated with fellow prey average residence time, depended on predator space use and the habitat riskiness (i.e., context dependent) Predation risk and habitat riskiness interact to affect prey response Kuijper et al. (2015) Residence time of foxes was only correlated with edge habitat when hares were present. When hares were present, foxes spent more time in edge habitats compared to nonedge habitats (t = 4.9, n = 36, p < 0.0001).

| Effects of fellow prey on predator-prey residence time
The presence of rabbits (i.e., introducing shared predation) affected the relation between the residence times of foxes and hares. In the presence of rabbits, hare average residence time was positively re-  (Figure 4). This interaction was reversed in the absence of rabbits (see Figure 3;  1,065). b Beta's standardized by 2*SD (Gelman, 2008). The beta of an interaction is different in the slope between the two values when the covariate increases by 1 standard deviation. c *p < 0.05, **p < 0.01, ***p < 0.001, significance level α is corrected for the false discovery rate in each dataset (Benjamini & Hochberg, 1995). d Highly correlated fixed effects, r > 0.7. e Open vegetation structure is the reference category. f High rate of type II error because of unequal and small group sizes; ratio n small /n large ≤ 0.5 (Supporting Information Table S3). g Nonedge location is the reference category. h Too few samples in nonedge locations to estimate the effect.  (Table 2, compare dataset A, C, and D). The presence of hares did not affect the predator-prey space race between foxes and rabbits.

| Effects of predator on fellow prey-prey residence time
The presence of foxes (i.e., introducing shared predation) affected the relation between the residence times of rabbits and hares. In the absence of foxes, hare average residence time was negatively re-   (Gelman, 2008). The beta of an interaction is different in the slope between the two values when the covariate increases by 1 standard deviation. c *p < 0.05, **p < 0.01, ***p < 0.001, significance level α is corrected for the false discovery rate in each dataset (Benjamini & Hochberg, 1995). d Open vegetation structure is the reference category. e High rate of type II error because of unequal group sizes; ratio n small /n large ≤ 0.5 (Supporting Information

| Prey and predator distribution among habitats differing in habitat riskiness
Overall, predator space use and habitat riskiness more strongly affected space use by hares than space use by rabbits. Noncentralplace foragers like hares are more capable of shifting their use of space as a response to a change in predation risk, as they have larger home ranges, have access to a wider range of food resources, and possess multiple escape modes (Stott, 2007;Wirsing et al., 2010).
Moreover, hares have a relatively small digestive system, which acts as a weight-minimizing adaptation to enhance flight and maximizes the passage rate to cope with low-quality forage (Kuijper et al., 2004;Stott, 2007). Therefore, hares can compensate for a poorer diet that comes at the cost of a shift in space (Laundré, Hernández, & Ripple, 2010). As a central-place forager, rabbits are less capable of shifting their use of space as a result of predation risk. Even though predation risk is predicted to increase with distance from the central location of central-place foragers (Lima & Dill, 1990), space use by a central-place forager like rabbit was not affected by predation risk; instead space use was strongly affected by food quality (Bakker et al., 2005). However, rabbit space use could be affected by the spatial arrangement of their refuges (Wilson, Rayburn, & Edwards, 2012). Central-place foragers should maximize net energy gain and have more difficulty to compensate for a poorer diet that comes at the cost of a shift in space (Demment & Van Soest, 1985;Schoener, 1979;Shipley, 2007;Stott, 2007). Hence, as a response to predation risk, central-place foragers could shift their activities in time (Bakker et al., 2005).
As expected, hares spent more time in locations with tall shrubs and half-open vegetation structures when foxes were present.

Structure-rich tall shrub and half-open vegetation may reduce risk
for prey that hide from predators by a reducing their encounter rate with predators (Lima & Dill, 1990;Riginos & Grace, 2008;Verdolin, 2006). However, hares also spent more time in locations near edges when foxes were present, even though foxes prefer protective cover, and ecotones, and are considered ambush predators (Holley, 1993;Kiener & Zaitsev, 2010). Prey escape mode is context dependent (Kuijper et al., 2015;Wirsing et al., 2010). Even though hares use closed vegetation as a hiding place (Neumann et al., 2011), and can conceal themselves from predators by their cryptic coloration (Focardi & Rizzotto, 1999)

| The effects of shared predation on space use by prey
Few field studies on terrestrial systems have quantitatively investigated the effects of shared predation on fine-scale space use by prey species (Camacho et al., 2017;Johnson et al., 2013;Oliver et al., 2009). As expected, the presence of rabbits (i.e., introducing shared predation) affected the predator-prey space race for hares more strongly than vice versa. However, we did not find shared predation to negatively affect space use by hare as expected. In contrast, we found that shared predation reduced predation risk for hares and did not affect rabbit. Fellow prey that are preferred prey, such as rabbit, can attract predators (Díaz-Ruiz et al., 2011;Doherty et al., 2015;Norbury, 2001;Smith & Quin, 1996) that can reduce the probability of being targeted or increase the probability of escape for other prey when collectively detected (Bednekoff & Lima, 1998). Predation risk for the weaker competitor is expected to be lower, if the stronger competitor is more vulnerable to predation (Grand & Dill, 1999). Both prey are then expected to aggregate in the risky but productive open habitat. This corroborates our results, particularly, if we assume that the smaller rabbits have an exploitative competitive advantage over the larger hares (Flux, 2008;Persson, 1985;Shipley, 2007), and that rabbits are more vulnerable to predation because they are preferred prey of predators like feral cat and red fox. Preferred prey species experience regulatory predation, in contrast to prey species that are less preferred, which are more prone to depensatory predation (DeCesare et al., 2010;Sinclair et al., 1998).
Hares and rabbits seemed to be negatively associated in open vegetation structure and in tall shrubs in the absence of foxes. This behavior could erroneously be interpreted as apparent competition, but in our case, this is most likely the result of exploitative competition (Halliday & Morris, 2013 Noonburg & Byers, 2005). The presence of foxes (i.e., introducing shared predation) affected the space use between hares and rabbits.
The presence of a shared predator can release competition between prey species and promote their coexistence in productive open vegetation structures with high risk, and in landscapes that contain spatial variation in habitat riskiness (Bonsall, Bull, Pickup, & Hassell, 2005;Bonsall & Hassell, 2000;DeCesare et al., 2010;Grand & Dill, 1999;Gurevitch, Morrison, & Hedges, 2000). Nevertheless, it seemed that even though foxes were present, the negative association between hares and rabbits in tall shrubs with low risk persisted (see Table 2 dataset D), possibly because rabbit as a stronger competitor prefers burrows in edge habitat with protective shrub cover (Bakker et al., 2005).
Several other factors could explain the response of prey to shared predation. First, the presence and density of other prey species, such as mice, and ground breeding birds will affect the relationship between our prey and their shared predator, because additional prey can affect the density of predators (Carbone & Gittleman, 2002;Duffy et al., 2007). Nevertheless, in our coastal dune landscape, a small part of the fox diet (<25% of feces content) did not constitute of rabbit and hares (Mulder, 2005). Second, the timing of prey responses to predation risk is important (Lima & Dill, 1990).
Prey species can vary in their space use over time and can shift their space use in time as a response to increased predation risk (Eccard, Pusenius, Sundell, Halle, & Ylönen, 2008;Tambling et al., 2015), affecting the temporal overlap between prey and predator (Linkie & Ridout, 2011). Third, the prey space use is affected by the trade-off between food and the risk of predation that is related to prey body size and food availability (Hopcraft, Anderson, Pérez-Vila, Mayemba, & Olff, 2012;Hopcraft, Olff, & Sinclair, 2010;Owen-Smith, Fryxell, & Merrill, 2010). Compared to hare, rabbit is much smaller in body size.
Space use by rabbits is thus more strongly affected by food than predation (Bakker et al., 2005;Hopcraft et al., 2012Hopcraft et al., , 2010, because the metabolic rate of smaller prey is relatively higher, mass-specific nutritional requirements increase with declining body mass, and smaller herbivorous mammals are more limited in their digestive efficiency (Demment & Van Soest, 1985;Owen-Smith, 1988;Schmidt-Nielsen, 1990). Possibly, rabbits are thus unable to avoid predation risk via spatial shifts, because of their foraging mode as a result of their food requirements and the central place of their burrow.

| CON CLUS IONS
Hares and rabbits spent time differently among habitats that differ in riskiness. Space use by predators and habitat riskiness affected space use by hares as a noncentral-place forager more strongly than space use by rabbits as a central-place forager. Residence time of hare was shorter in habitats in which the predator was efficient in searching or capturing prey species. However, hares spent more time in edge habitat when foxes were present, even though foxes are considered ambush predators. Habitat riskiness and species presence interacted with the space use by predators and the space use by fellow prey on the space use by prey. Shared predation affected the predator-prey space race for hares positively, and more strongly than the predator-prey space race for rabbits, which were not affected. Shared predation reversed the predator-prey space race between foxes and hares, whereas shared predation possibly also released a negative association and promoted a positive association between hares and rabbits. Prey species' properties, such as escape mode and characteristics that affect foraging mode (i.e., body size, competitive ability, and dependence or independence of a prey to a central place), affect the space use by prey among habitats that differ in riskiness by shared predation.