Behaviour and resource use of two competing vole species under shared predation risk

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1 Oecologia (2008) 157: DOI /s BEHAVIORAL ECOLOGY - ORIGINAL PAPER Behaviour and resource use of two competing vole species under shared predation risk Lenka Trebatická Janne Sundell Emil Tkadlec Hannu Ylönen Received: 15 June 2007 / Accepted: 10 June 2008 / Published online: 9 July 2008 Springer-Verlag 2008 Abstract Indirect interaction between two competing species via a shared predator may be an important determinant of population and community dynamics. We studied the evect of predation risk imposed by the least weasel Mustela nivalis nivalis on space use, foraging and activity of two competing vole species, the grey-sided vole Myodes rufocanus, and the bank vole Myodes glareolus. The experiment was conducted in a large indoor arena, consisting of microhabitat structures providing food, shelter, trees for refuge and separated areas with high and low predation risk. Voles were followed for 5 days: 2 days before, 1 day during and 2 days after the presence of weasel. Our results suggest an evect of weasel presence on the vole community. Voles of both species shifted their activity from risky to less risky areas, climbed trees more often and were less active. Seed consumption was not avected by weasel Communicated by Roland Brandl. Electronic supplementary material The online version of this article (doi: /s ) contains supplementary material, which is available to authorized users. L. Trebatická (&) H. Ylönen Department of Biological and Environmental Science, Konnevesi Research Station, University of Jyväskylä, P.O. Box 35, Jyväskylä, Finland letrebat@cc.jyu.w; trebatickalenka@yahoo.com J. Sundell Department of Biological and Environmental Sciences, Metapopulation Research Group, University of Helsinki, P.O. Box 65, Helsinki, Finland E. Tkadlec Department of Ecology and Environmental Sciences, Palacky University, tr. Svobody 26, Olomouc, Czech Republic presence. The time spent in the risky and less risky area did not diver between species, but bank voles spent more time in trees than grey-sided voles. Males of both species were more exposed to predation risk than females, i.e. generally spent more time in the risky area. Proportion of time spent in the risky area, the use of area, trees and food stations were sex dependent. Activity and use of trees were species dependent. We found no evidence for despotic distribution between our two species, although bank voles seemed to be more avected by coexistence, since they lost weight during the experiment. Based on our results we conclude that predator response was largely similar between species, while the sex-speciwc responses dominated. Besides a stronger escape response in the bank vole, the strongest individual diverences were sex speciwc, i.e. males were more prone to take risks in space use and activity. Keywords Myodes glareolus (syn. Clethrionomys glareolus) Myodes rufocanus (syn. Clethrionomys rufocanus) Indirect predation evect Least weasel Shared predator Introduction Predation is known to be a strong selective force (see Vamosi 2005; Ylönen and Brown 2007 for reviews) and alters a variety of prey behaviours. The prey individual allocates its time between other activities (food, mating) and anti-predatory behaviours. Any animal that maximizes its anti-predatory behaviours will have a higher probability of survival, but its Wtness may decrease because of worse condition and/or mating success due to costs of antipredatory behaviour (Brown 1988). On the other hand, whenever an individual starts to allocate more time and resources to

2 708 Oecologia (2008) 157: some other activity than an anti-predatory response, then its vulnerability to predation increases (Lind and Cresswell 2005). Therefore, in regard to time allocation, prey individuals choose when, where and how long to be active. For instance, many animals respond to predator presence by using refuges (Sih et al. 1992) and they should optimize the decision of when to come out from the refuge, because hiding may be costly (Martín and Lopéz 1999; Sih 1997). Further, predation risk may avect the time and duration of foraging or it may shift the activity of vulnerable prey species to safe microhabitats (e.g. Brown et al. 1988). Such behavioural evects on prey animals can explain species coexistence as an interaction between predation and competition (Kotler and Holt 1989). In a prey community predators can alter interspeciwc competition substantially (see Chase et al for review) and lead to apparent competition processes (Holt 1977). However, interaction between predation and interspeciwc competition appears to bring confusing results. Predators have been shown to increase, decrease or to have very little evect on the strength of interspeciwc competition or on the prey community (Chase et al. 2002). Moreover, the various anti-predatory behaviours may not be independent. Also, it is unlikely that diverent prey species always respond in the same way to a particular predator (Jedrzejewska and Jedrzejewski 1990; Relyea 2001). Therefore, behavioural diverences among prey species may inxuence their vulnerability to predators (Wohlfahrt et al. 2006), and this might further lead to selective predation and changes in community structure. So far, most studies have focused either on evects of predators on the number of prey, or only on a single aspect of the anti-predatory behaviour (Caro 2005), such as choice of microhabitat versus foraging (Longland and Price 1991; Kotler et al. 1994; Jacob and Brown 2000), or time spent in the refuge (Martín et al. 2005; Rhoades and Blumstein 2007). Usually one predator and one prey species systems have been used. Only a few studies have focused on more complex issues, multi-behavioural anti-predatory responses (e.g. in birds Boyer et al. 2006; Lind and Cresswell 2006), or time allocation of prey species to antipredatory behaviours in a multi-predator environment (e.g. Korpimäki et al. 1996; Kotler et al. 1992). Commonly, antipredatory responses of diverent sexes are studied in separate experiments (e.g. Sundell and Ylönen 2004). Studies on genderspeciwc responses in a mixed group of mammals are lacking. To our knowledge, putting two prey species and both genders with a known dominance hierarchy in a single study is novel and allows comparison of species versus gender evects. Incorporating social interactions between/within species leads to a hierarchical use of space, time and resources, rexected in an ideal despotic distribution (Fretwell 1972). The presence of both competitor and opposite sex should expose prey individual to conxicting demands under predation risk. We tested experimentally the sexdependent and species-dependent behavioural responses of two prey vole species (Myodes rufocanus and Myodes glareolus) to mere presence of the common predator (Mustela nivalis nivalis) in terms of general activity, space use, foraging, and use of refuge sites. Our model species, bank voles, M. glareolus and grey-sided voles, M. rufocanus are sympatric vole species living in the northern boreal zone. To our knowledge, there are no published studies on behavioural responses of these two species sharing a common predator, but only on inter-speciwc competition in general (e.g. Johannesen and Mauritzen 1999; Johannesen et al. 2002). The heavier grey-sided vole (Bondrup-Nielsen and Ims 1990; Siivonen and Sulkava 1994) is dominant over the bank vole (e.g. Henttonen et al. 1977; Henttonen and Hansson 1984; Johannesen et al. 2002). Small mammals are good models for ecological studies, including those on resource use and partitioning, competition and predator avoidance behaviours (Ylönen and Brown 2007). For example, multi-species desert rodent communities that depend on daily renewable resource pulses and food competition, provide a good example of studies on social hierarchies and resource partitioning (Kotler et al. 1994; Kotler 1997). We predicted that in the presence of the weasel: (1) the overall activity of voles would decrease; (2) there should be a shift in space use and activity from the risky area to less risky one; (3) both vole species should increase the use of trees as a refuge; (4) foraging activity should decrease during the weasel presence and increase after that (Lima and BednekoV 1999); and, Wnally, as we have species with a known dominance hierarchy (5) grey-sided voles, as competitively dominant species, should dominate the less risky area and the two species distribution would be a despotic one (Fretwell and Lucas 1970). Materials and methods Study species and individuals Two Myodes vole species were used in the experiment, the grey-sided vole and the bank vole. Since they have similar requirements for food and shelter (Henttonen and Hansson 1984), they are potential competitors. The heavier greysided vole (Bondrup-Nielsen and Ims 1990; Siivonen and Sulkava 1994) is dominant over the bank vole (e.g. Henttonen et al. 1977; Henttonen and Hansson 1984; Johannesen et al. 2002). Females of both species are territorial (Viitala and HoVmeyer 1985), with home ranges both intra- and inter-speciwcally exclusive (Löfgren 1989). The grey-sided vole is assumed to be more vulnerable to predation by the

3 Oecologia (2008) 157: weasel than the bank vole because of its general clumsiness (Hanski and Henttonen 1996). This dissimilar vulnerability might be caused by the evectiveness of diverent antipredatory strategies in these two vole species. Although the habit of bank voles to climb trees when seeking food and for arboreal escape is commonly known (Jedrzejewski and Jedrzejewska 1990), observations on grey-sided voles in trees are rare (e.g. Siivonen and Sulkava 1994). The least weasel is common throughout the whole of Fennoscandia (Hellstedt et al. 2006). Due to its small size and elongated, snake-like body (King and Powell 2006), the least weasel is highly adapted for hunting small rodents in their natural boreal environment (burrows, tunnels, subnivean space), leaving practically no refuge for the prey (Simms 1979, but see Sundell and Norrdahl 2002). The least weasel is also known to be a major agent of vole mortality (Norrdahl and Korpimäki 1995). Due to these reasons, antipredatory response of the prey should be strong against this species. We used wild-born bank and grey-sided voles and their Wrst generation descendants born in the laboratory. We expected that the antipredatory response of voles is mainly innate, and therefore the response of wild-born and the F1 generation laboratory-born animals should be more or less similar. The study of McPhee (2003) with the oldweld mouse showed that antipredatory behaviours were not altered in the Wrst generations born in the laboratory. Bank voles were trapped in the Konnevesi region (62 37 N, E). Grey-sided voles were trapped in northern Finland and Norway in July Voles were housed in standard mouse cages of cm 3 and maintained in a 16/8 h light/dark period with a constant temperature of +20 C. Water and food (mice pellets) were provided ad libitum. All animals were in non-reproductive condition and of similar body mass distribution within each replicate (mean body mass, bank vole females, g; bank vole males, g; grey-sided vole females, g; grey-sided vole males, g). We used Wve diverent weasels (one per replicate); three females and two males. All weasels were born in captivity. Weasels were fed daily with chicks and dead voles (Microtus agrestis) prior to and during the experiment. Weasels were housed singly in plexiglass cages (each of cm 3 ) with wire netting on the top. All experimental animals were marked with passive integrated transponder (PIT) tags. Study arena and procedure The experiment was carried out in a large indoor arena at the Konnevesi Research Station of the University of Jyväskylä in Central Finland from January to April The large indoor arena ( m 2 ) was divided by a wire mesh-fenced tube system into two main areas, a risky and less risky area. Each area was further divided into two sub-compartments. All sides of the compartments consisted of weasel tubes (tubes in which weasels were released and could not leave and which could not be entered by voles) of cm 3. In the risky area, weasels moved freely in the fenced tubes but were not able to enter the less risky area, and neither were they visible from this area. Furthermore, each compartment was partly divided by a diagonal weasel tube to allow closer visual, acoustic and olfactory contact between the weasel and voles (Fig. 1.). All four compartments were connected by the gates through which voles could pass. Two spruces ( m) to allow an escape reaction of voles, one tile tube (30 cm long, 7 cm diameter) for hiding, one feeding box ( cm 3 ) with 50 sunxower seeds hidden either in 1 l (replicate one) or 4 l sand (four other replicates), and water cups were placed into each compartment. The topless feeding box, made of transparent plexiglas, had an opening ( cm 2 ) on each side wall 3 cm above the bottom covered with wire mesh to make the seed box more exposed to all predator cues. Each gate, tree, seed box, hiding tube, as well as weasel tubes, had readers of PIT tags to record the movement of the voles and weasels. Altogether we used 36 readers to cover all possible passages (see Fig. 1). Further, a nest box with a water cup was provided for the weasel. Weasels were fed on the day before release and during their stay in the arena. In each replicate, we released eight diverent voles, four of each species, with a sex ratio of 1:1, into the arena. Voles and weasels were marked with PIT tags. Trovan (Trovan, UK) technology based on automatic data-logging of PIT tagged animals was used to study individual foraging and resource allocation responses of prey voles to indirect risk by weasels, and to study interand intra-speciwc distribution of animals. Giving-updensity (GUD) was used to determine the foraging activity (Brown 1988). The experiment lasted for 7 days, including the Wrst 2 days of the habituation period for the voles. We had Wve replicates. Data were collected for the whole experimental period, but for an analysis we excluded data from the habituation period. Weasels were always released on the Wfth day of the experiment into the tube system and were trapped out after 24 h. GUD was measured every day by sieving the sand mixed with 50 sunxower seeds and counting the number of seeds left. Following this, 50 new seeds were provided. Sand was changed after each sieving but the same sand was used every second day. Spruces were replaced after the second and the fourth replicate. After each replicate, the arena and the weasel tubes were cleaned with water and alcohol.

4 710 Oecologia (2008) 157: Fig. 1 Experimental set up. Division of arena into risky (indicated by thick line) and less risky areas. Each area consisted of two compartments which contained two trees, one tube, one seed box, one water cup, one diagonal weasel tube leading from the weasel nest box and two vole passing gates leading to another compartment. Dashed lines represent wire mesh parts of the weasel tubes 360 cm 40 cm cm 360 cm 30 cm water cup gate tree seed box weasel tube tube we asel nest box with openings Data analysis and statistics The time in minutes was counted and converted into proportion of time that each individual spent in risky and less risky areas, in the trees and in the seed boxes, on each experimental day (24 h). When analysing GUDs, the absolute number of seeds left in seed boxes was counted. Activity was analysed as number of recordings of the particular vole in 2-h intervals for 24 h. On average there were recordings per bank vole per day and recordings per grey-sided vole per day in 5 experimental days. We used 5 days of the experimental period [2 days before the release of the weasel (2b), 1 day before the release of the weasel (1b), weasel day (w), 1 day after weasel removal (1a), and 2 days after weasel removal (2a)] when analysing data on space use, foraging and activity of voles, in order to Wnd out possible trends in changes of behaviour of voles due to indirect predation risk. For the analyses of the time spent in trees and seed boxes, analyses of data on arena level were also included, i.e. the response variable was expressed as the proportion of the day spent in trees, or in seed boxes, to Wnd a possible response to the weasel presence in general, regardless of area. Otherwise, we used the proportion of time spent in the risky area, in trees in the risky area, in seed boxes in the risky area from the overall time spent in the arena, in the trees or seed boxes, respectively. In the case of activity, we used the proportion of recordings in the risky area from the overall number of recordings. In GUDs and also activity analyses, absolute values of seeds left or number of recordings between the risky and less risky area were compared. In each analysis the evect of weasel presence was examined, i.e. contrasts w versus b (weasel vs. before weasel = weasel day vs. the mean of the days before weasel release, in order to avoid random variation) and w versus a (weasel vs. after weasel = weasel day vs. the mean of days after weasel removal). Additionally days w, 1a and 2a were contrasted to test for possible delayed evects. All statistical analyses were performed using SAS 9.1 (SAS Institute 2004). Proc GLIMMIX was used to analyse the evect of weasel presence, species and sex on the space use (area, i.e. risky and less-risky; and the use of trees), foraging activity (the time spent in seed boxes and GUD) and activity. Logistic general linear mixed model (GLMM) with binomial error distribution and logit link function were used to analyse time allocation. GUD was analysed by GLMM with Poisson error distribution and log link function. The variable (GUD) is an integer and cannot be negative. In both cases, replicate was used as random evect, individual vole as the repeated evect with Wrst-order covariance structure to specify that the observations in a single cluster are uniquely identiwed. We used period (2b, 1b, w, 1a, 2a), species (bank vole and grey-sided vole) and sex (male and female) as Wxed evects and independent variables, and measured proportion of time as a dependent variable in a full model (including interactions between variables). Interval multiple comparison procedures, i.e.

5 Oecologia (2008) 157: Tukey Kramer method, was used in cases of multiple comparisons. The F-test was used to test the signiwcance of Wxed evects, with the denominator df calculated by the Kenward Roger method. Incomplete data (e.g. when a vole escaped from the compartments, or died during the experiment) of particular voles were excluded from analysis. However, only in the Wfth replicate were data on three voles (one female bank vole and two males grey-sided voles) totally excluded. Results Space use There was a signiwcant diverence between the days in the utilization of risky and less risky areas [period: F 4,124 =4.18, P =0.003; Fig.2a; Appendix 1, Electronic supplementary material (ESM)]. Voles spent less time in risky area during weasel presence compared to the days before weasel presence (contrast: w vs. b, F 1,145 =11.36, P = 0.001). There was a trend after the weasel removal in proportional time diverence compared to weasel day (contrast: w vs. a, F 1,145 =3.17, P = 0.077). When the 2 days after the weasel presence were checked separately (delayed evect), no diverence was found between weasel day and Wrst day after its removal (contrast: w vs. 1a, F 1,120 =0.36, P = 0.548), but a signiwcant diverence between the Wrst and the second day after weasel removal was found (contrast: 1a vs. 2a, F 1,120 =5.97, P = 0.016). No diverence was detected between species (species: F 1,36 =1.60, P = 0.214). Females of both species spent less time in the risky area compared to males (sex: F 1,36 =6.61, P = 0.014). Voles responded to weasel presence by spending more time in trees during weasel day than during other days (contrasts: w vs. b, F 1,131 = 45.64, P < 0.001; w vs. a, F 1,129 =38.39, P <0.001; Fig.2b; Appendices 1, 2, ESM). Bank voles spent more time in trees than grey-sided voles (species: F 1,31 =7.82, P = 0.009). There was a strong trend showing a diverent use of trees between sexes, with males spending more time in trees than females (sex: F 1,31 = 3.55, P =0.069). The proportion of time spent in trees by voles in the risky area divered among the days depending on species and sex (period sex species: F 4,104 =2.57, P = 0.042, other main evects were non-signiwcant; Appendix 1, ESM). Moreover, there was also a delayed evect: voles returned to trees in the risky area only on the second day after weasel removal (contrasts: w vs. 1a, F 1,92 =0.29, P = 0.589; 1a vs. 2a, F 1,96 =5.16, P = 0.025; Appendix 2, ESM). Foraging The time spent in seed boxes was diverent among the days (period: F 4,122 =2.94, P = 0.023). There was no diverence in time spent in seed boxes during weasel presence and the days before weasel release or the days after weasel removal (contrasts: w vs. b, F 1,142 =0.81, P = 0.371; w vs. a F 1,141 =1.38, P = 0.241). However, voles spent more time in seed boxes during the Wrst day after the weasel removal than during the weasel presence (contrast: w vs. 1a, F 1,116 =4.98, P = 0.028), and also more time than during the second day after the removal of the weasel (contrast: 1a Fig. 2 a The proportion of time per day voles spent in the risky area, b the proportion of time spent in trees. For each day the proportion was calculated from the overall time spent in the arena in 24 h. c Foraging evort expressed as the number of seeds left in the seed box (giving-updensity), d activity expressed as number of recordings for each species and sex. Error bars denote SEM. Data were obtained during the 5 days of the experimental period. 2b 2 Days before weasel release, 1b 1 day before weasel release, w weasel day, 1a 1 day after weasel removal, 2b 2 days after weasel removal, bf bank vole females, bm bank vole males, gf grey-sided vole females, gm grey-sided vole males No. of seeds left Time in risky area A C less risky area risky area 2b 1b w 1a 2a Period Time in trees No. of recordings B D 2b 1b w 1a 2a Period bf bm gf gm

6 712 Oecologia (2008) 157: vs. 2a, F 1,116 = 4.47, P = 0.037). The proportion of time spent in seed boxes (Appendix 1, ESM) depended also on sex and species (species sex: F 1,38 =7.45, P = 0.01). Grey-sided vole males, bank vole females, bank vole males and grey-sided vole females spent, respectively, on average 0.114, 0.111, 0.084, as a proportion of the time in seed boxes. Bank vole females spent more time in seed boxes than grey-sided vole females (contrast: F 1,38 =6.04, P = 0.019), in males there was no diverence between species (contrast: F 1,38 =2.16, P =0.15). The proportion of time spent in seed boxes in the risky area was avected by weasel presence (contrasts: w vs. b, F 1,143 =6.00, P =0.016; w vs. a, F 1,143 = 10.98, P =0.001; Appendices 1, 2, ESM). Voles spent proportionally less time in seed boxes in the risky area during weasel presence. Males spent more time in seed boxes in the risky area than females (sex: F 1,40 =8.74, P = 0.005), but time did not diver between species (species: F 1,40 =0.01, P =0.912). GUD unexpectedly gradually decreased with time, i.e. the voles were eating more (period: F 4,18 =4.10, P =0.015; Fig. 2c), but apparently the weasel presence itself did not have an evect on seed exploitation (contrast: w vs. b, F 1,15 =2.17, P = 0.162; Appendix 2, ESM). After weasel removal, voles were still increasing seed consumption (contrast: w vs. a, F 1,18 = 10.72, P =0.004). There was a signiwcant diverence in the change of body mass (body mass at the beginning of the experiment minus body mass at the end) between bank voles and grey-sided voles (GLM: F 1,34 =9.93, P = ). Whereas bank voles were losing mass (females, pairwise t-test, t =3.59, P = , mean diverence g SD; males, pairwise t-test, t = 3.29, P = , mean diverence g SD), there was no signiwcant change in body mass in grey-sided voles (females, pairwise t-test, t = 1.17, P = , mean diverence g SD; males, pairwise t-test t = 0.80, P = , mean diverence g SD). There was no diverence in the change of body mass between sexes either within bank voles (GLM: F 1,17 = 0.00, P = ) or grey-side voles (GLM: F 1,15 =1.88, P = ). Activity The day had a signiwcant evect on the activity of voles (period: F 4,124 =11.16, P <0.001; Fig.2d; Appendix 1, ESM). Voles were less active during the weasel day, compared to the days before weasel release (contrast: w vs. b, F 1,137 =9.65, P = 0.002, Appendix 2, ESM) or to the days after its removal (contrast: w vs. a, F 1,135 =33.56, P < 0.001). However, no delay was found, because voles returned to normal activity after weasel removal (contrast: 1a vs. 2a, F 1,120 =0.59, P = 0.445). The number of recordings was avected by the area; voles were more active in a less risky area (area: F 1,4228 = 13.43, P < 0.001) and this depended on sex (sex area: F 1,4228 =25.33, P <0.001), species (species area: F 1,4228 =7.44, P = 0.006), and day (area period: F 4,1 = , P = 0.047). Grey-sided voles were more active than bank voles (species: F 1,32 = 7.27, P =0.011). The proportion of recordings in the risky area was lower during the weasel day, compared to both the days before its release (contrast: w vs. b, F 1,136 =61.94, P < 0.001) and the days after weasel removal (contrast: w vs. a, F 1,134 = 66.26, P < 0.001). The day had an evect on vole activity depending on species (species period: F 4,116 =3.66, P =0.008); with the lowest proportion of recordings in the risky area for bank voles and grey-sided voles during the weasel day. Males were more active than females (sex: F 1,36 = 5.14, P =0.030). Discussion In our experiment on the evect of predation risk imposed by the least weasel on space use, foraging and activity of two competing vole species, the grey-sided vole and the bank vole, we found that voles in general: (1) were less active, (2) shifted their activity from the risky to less risky area, and (3) spent more time in trees under weasel presence compared to weasel absence. In addition: (4) that even if foraging, in terms of seed consumption (GUDs), was not generally avected by weasel presence, voles spent less time in seed boxes during weasel presence than after it. Additionally, bank voles lost weight during the experiment while grey-sided voles did not. In general: (5) grey-sided voles and bank voles were equally distributed in the ground area, but bank voles spent more time in trees. Moreover, males of both species were more exposed to predation risk than females, i.e. spent more time in the risky area, as well as in seed boxes in the risky area. When looking at the proportion of time spent in the risky area, the use of area, trees and food stations were sex dependent. Activity and also the use of trees were species dependent. Spacing behaviour and foraging Our results show a clear antipredatory response in both Myodes species. Reduced activity, shifts in microhabitats (in the present study from the risky to less-risky area) and diverent escape response (e.g. climbing trees) are reported for diverent species of diverent taxa (see Lima and Dill 1990 for review). Reduced foraging, commonly associated with reduced mobility, is one of the most common antipredatory response reactions (e.g. Brown et al. 1992; Koivisto and Pusenius 2003, but see Pusenius and Ostfeld 2000). In our study, foraging, expressed as GUD, increased after

7 Oecologia (2008) 157: weasel introduction. However, both species showed diverent responses to persisting conditions, i.e. presence of another species and short-term predation risk. Whereas bank voles lost body mass, possibly suggesting an increasing marginal value of energy with hunger, grey-sided voles maintained their mass, suggesting an increasing level of comfort with a persistent situation. Although bank vole females spent signiwcantly more time in seed boxes than grey-sided vole females, they still lost mass. This may suggest that grey-sided vole females were less vigilant and therefore foraged more eyciently than bank vole females. An alternative explanation, which applies to both sexes, is that bank voles were more stressed, and possibly were harassed by the dominant grey-sided voles. However, this cannot be veriwed since animals were not observed for vigilance or for direct interactions and we do not know which species contributed more to the observed GUDs. Voles spent much more time in food stations during the day after weasel removal. The weasel risk and being highly vigilant might have increased the need for energy after the short period of peak risk during weasel presence, as suggested in Lima and BednekoV s (1999) model. We did not Wnd any storage places where voles would hide the seeds, which suggest that voles consumed seeds immediately. Ideal despotic distribution and escape behaviours The time spent in the risky and less risky area did not diver between species. This was unexpected, as grey-sided voles are considered to be dominant over bank voles due to their larger size (Henttonen and Hansson 1984; Löfgren 1995; Hanski and Henttonen 1996). Dominance of grey-sided voles over bank voles has previously been observed in habitat selection and behaviour (Johannesen and Mauritzen 1999; Johannesen et al. 2002). Although both species spent an equal amount of time in both areas, grey-sided voles were more active in a less risky area, which could rexect a more intense use of space and consequently be a sign of dominance. The diverence in weight change also supports this. One possible reason for not excluding bank voles from a less risky area by grey-sided voles could have been the lack of resident evect. A species that settles a site Wrst gains an advantage because individuals defend their home ranges more aggressively than other sites (WolV et al. 1983). We released individuals of both species at the same time, which may have precluded an intense interspeciwc interaction. Our result is similar to Wndings by Lin and Batzli (2001) who found only a weak interspeciwc competition between prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus) possibly due to the fact that increased predation risk might have weakened the intensity of interspeciwc interactions. Abramsky et al. (1998) suggested that high predation risk can overwhelm competitive evects. All of the voles were also in non-breeding condition, which could have also avected the intensity of interspeciwc competition. During the breeding season both inter- and intraspeciwc interactions are more intensive, and individuals within species compete more, e.g. for mating partners or establishing territories. We found no evidence for despotic distribution between the two species. Bank voles were more active in the use of the arboreal space, i.e. they spent more time in trees. Bank voles are known for arboreal escape reactions when exposed to small mustelid predators and also climb trees to forage (Jedrzejewski and Jedrzejewska 1990). Although grey-sided voles are able to climb trees, which has been also proven in the present study, observations on grey-sided voles in trees are only anecdotal (e.g. Siivonen and Sulkava 1994). It might be that trees are not the preferred type of refuge for greysided voles, i.e. it is too costly for them to climb. Compared to bank voles, grey-sided voles are heavier and slower, which could have a large impact on an escape decision and the type of refuge used. Some refuges are not entirely evective for eluding predators (Martín and Lopéz 2000). Prey are known to adjust their escape response and refuge use to minimize costs such as the loss of opportunities, for example foraging (Sih 1997). The evectiveness of diverent antipredatory strategies in these two vole species may avect their relative vulnerability to predation. We found that males were more prone to take risks and were more exposed to predation than females, shown by the time spent in the risky area and food stations there. This might be explained by the sexual status of our voles. Our study was carried out during the non-breeding season. During the breeding season, females are regarded to be vulnerable to predation due to sexual cues or pregnancy, and males due to greater mobility related to sexual activity and search for mates (see Ylönen and Brown 2007 for review). Also during the non-breeding season, regardless of resource distribution, males are prone to move more (Ylönen and Viitala 1991) and probably take more risks to Wnd food. Greater mobility and spending more time at the food patch correlates strongly with vulnerability to predation (Norrdahl and Korpimäki 1998; Kotler et al. 1994). Besides evects on individual behaviour (Ylönen and Brown 2007), reproduction and demography (Creel et al. 2007), predation risk has been suggested to avect community structure and even ecosystems through trophic cascades (Ripple and Beschta 2004). In our two-species system, because of diverent body size, dominance and escape behaviours, there were clear predictions that the grey-sided vole would exploit its dominance as an antipredatory strategy and occupy the less risky area. The bank vole would be forced to remain under a high risk but to exploit its better climbing ability (Jedrzejewski and Jedrzejewska 1990). However, although the bank vole was

8 714 Oecologia (2008) 157: more prone to climbing, both species reacted to weasel presence as a community, not as diverent species. Most probably this was because of the non-breeding status of the voles leading to a stronger social tolerance also interspeciwcally. However, in a concurrent study under Weld conditions (Sundell et al. 2008), where a real predator was put back into the experimental design (cf. Lima 2002) the speciesspeciwc behavioural responses were overridden by sexspeciwc ones, like in the present study. To conclude, the results suggest that under predation risk, space use (Weld layer and arboreal) and foraging were sex dependent, whereas activity and arboreal space use were species dependent. Although we used two sympatric vole species with a predicted clear dominance relationship, we did not Wnd any signs of exclusion of the subordinate species, M. glareolus, either in terms of space use or foraging. However, in the long term the relative dominance between species was possibly rexected in their condition; bank voles lost weight, while grey-sided voles did not. On the other hand, it seems that the common dominance of grey-sided vole over the bank vole was diluted under the predation risk, and was possibly avected by an interspeciwc social tolerance of non-breeding individuals. Generally, vanishing interspeciwc competition between species due to predation could be the mechanism enhancing coexistence between individuals in a multi-species community, which releases energy for vigilance and antipredatory needs instead of intraspeciwc processes. Acknowledgements Jyrki Raatikainen is greatly acknowledged for building the tube system, Jani Korpilauri, Janne Koskinen, Helinä Nisu, Irja Hänninen and Risto Latvanen for technical help. The study was supported by CIMO (to L. T.) and the Academy of Finland (to J. S., project no ; and H. Y., no ). The experiment was run under license from the Experimental Animal Committee of the University of Jyväskylä (25/ ). References Abramsky Z, Rosenzweig ML, Subach A (1998) Do gerbils care more about competition or predation? Oikos 83:75 84 Bondrup-Nielsen S, Ims RA (1990) Reversed sexual size dimorphism in microtines: are females larger than males or are males smaller than females. Evol Ecol 4: Boyer JS, Hass LL, Lurie MH, Blumstein DT (2006) EVect of visibility on time allocation and escape decisions in crimson rosellas. Aust J Zool 54: Brown JS (1988) Patch use as an indicator of habitat preference, predation risk, and competition. Behav Ecol Sociobiol 22:37 47 Brown JS, Kotler BP, Smith RJ, Wirtz WOII (1988) The evects of owl predation on the foraging behavior of heteromyid rodents. Oecologia 76: Brown JS, Morgan RA, Dow BD (1992) Patch use under predation risk. II. A test with fox squirrels, Sciurus niger. Ann Zool Fenn 29: Caro T (2005) Antipredator defenses in birds and mammals. University of Chicago Press, Chicago Chase JM, Abrams PA, Grover JP, Diehl S, Chesson P, Holt RD, Richards SA, Nisbet RM, Case TJ (2002) The interaction between predation and competition: a review and synthesis. Ecol Lett 5: Creel S, Christianson D, Liley S, Winnie JA Jr (2007) Predation risk avect reproductive physiology and demography of elk. Science 315:960 Fretwell SD (1972) Populations in a seasonal environment. Princeton University Press, Princeton Fretwell SD, Lucas HJ Jr (1970) On territorial behaviour and other factors inxuencing habitat distribution in birds. Acta Biotheor 19:16 36 Hanski I, Henttonen H (1996) Predation on competing rodent species: a simple explanation of complex patterns. J Anim Ecol 65: Hellstedt P, Sundell J, Helle P, Henttonen H (2006) Large-scale spatial and temporal patterns in population dynamics of the stoat (Mustela erminea) and the least weasel (Mustela nivalis) in Finland. Oikos 115: Henttonen H, Hansson L (1984) InterspeciWc relations between small rodents in European boreal and subarctic environments. Acta Zool Fenn 172:61 65 Henttonen H, Kaikusalo J, Tast J, Viitala J (1977) IntrespeciWc cometition between small rodents in subarctic and boreal systems. Oikos 29: Holt RD (1977) Predation, apparent competition, and the structure of prey communities. Theor Popul Biol 12: Jacob J, Brown JS (2000) Microhabitat use, giving-up-densities and temporal activity as short- and long-term anti-predator behaviors in common voles. Oikos 91: Jedrzejewska B, Jedrzejewski W (1990) Antipredator behaviour of bank voles and prey choice of weasels-enclosure experiments. Ann Zool Fenn 27: Jedrzejewski W, Jedrzejewska B (1990) EVect of a predator s visit on the spatial distribution of bank voles: experiments with weasels. Can J Zool 68: Johannesen E, Mauritzen M (1999) Habitat selection of grey-sided voles and bank voles in two subalpine populations in southern Norway. Ann Zool Fenn 36: Johannesen E, Brudevoll J, Jenstadt M, Korslund L, KristoVersen S (2002) Behavioural dominance of grey-sided voles over bank voles in dyadic encounters. Ann Zool Fenn 39:43 47 King CM, Powell RA (2006) The natural history of weasels and stoats: ecology, behavior, and management. Oxford University Press, Oxford Koivisto E, Pusenius J (2003) EVects of temporal variation in the risk of predation by least weasel (Mustela nivalis) on feeding behaviour of Weld voles (Microtus agrestis). Evol Ecol 17: Korpimäki E, Koivunen V, Hakkarainen H (1996) Microhabitat use and behavior of voles under weasel and raptor predation risk: predator facilitation? Behav Ecol 7:30 34 Kotler BP (1997) Patch use by gerbils in a risky environment: manipulating food and safety to test four models. Oikos 78: Kotler BP, Holt RD (1989) Predation and competition: the interaction of two types of species interactions. Oikos 54: Kotler BP, Blaustein L, Brown JS (1992) Predator facilitation: the combined evect of snakes and owls on the foraging behaviour of gerbils. Ann Zool Fenn 29: Kotler BP, Ayal Y, Subach A (1994) EVects of predatory risk and resource renewal on the timing of foraging acivity in a gerbil community. Oecologia 100: Lima SL (2002) Putting predators back into behavioral predator-prey interactions. Trends Ecol Evol 17:70 75 Lima SL, Dill LM (1990) Behavioural decisions made under the risk of predation: a review and prospectus. Can J Zool 68:

9 Oecologia (2008) 157: Lima SL, BednekoV PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153: Lin YK, Batzli GO (2001) The evect of interspeciwc competition on habitat selection by voles: an experimental approach. Can J Zool 79: Lind J, Cresswell W (2005) Determining the Wtness consequences of antipredation behaviour. Behav Ecol 16(5): Lind J, Cresswell W (2006) Anti-predation behaviour during bird migration; the benewt of studying multiple behavioural dimensions. J Ornithol 147: Longland WS, Price MV (1991) Direct observations of owls and heteromyd rodents: can predation risk explain microhabitat use? Ecology 72(6): Löfgren O (1989) Do intrinsic or extrinsic factors limit reproduction in cyclic populations of Clethrionomys glareolus and C. rufocanus? Hol Ecol 12:29 35 Löfgren O (1995) Niche expansion and increased maturation rate of Clethrionomys glareolus in the absence of competitors. J Mammal 76: Martín J, Lopéz P (1999) When to come out from the refuge: risk-sensitive and state-dependent decisions in an alpine lizard. Behav Ecol 10: Martín J, Lopéz P (2000) Fleeing to unsafe refuges: evects of conspicuousness and refuge safety on the escape decisions of the lizard Psammodromus algirus. Can J Zool 78: Martín J, Marcos I, Lopéz P (2005) When to come out form your own shell: risk-sensitive hiding decisions in terrapins. Behav Ecol Sociobiol 57: McPhee ME (2003) Generations in captivity increases behavioural variance: considerations for captive breeding and reintroduction programs. Biol Conserv 115:71 77 Norrdahl K, Korpimäki E (1995) Mortality factors in a cyclic vole population. Proc R Soc Lond B 261:49 53 Norrdahl K, Korpimäki E (1998) Does mobility or sex of voles avect risk of predation by mammalian predator? Ecology 79: Pusenius J, Ostfeld RS (2000) EVects of stoat s presence and auditory cues indicating its presence on tree seedling predation by meadow voles. Oikos 91: 130 Relyea RA (2001) Morphological and behavioural plasticity of larval anurans in response to diverent predators. Ecology 82: Rhoades E, Blumstein DT (2007) Predicted Wtness consequences of threat-sensitive hiding behavior. Behav Ecol 18: Ripple WJ, Beschta RL (2004) Wolves and the ecology of fear: can predation risk structure ecosystems? BioScience 54: SAS Institute (2004) SAS Help and documentation. SAS Institute., Cary Sih A (1997) To hide or not to hide? Refuge use in a Xuctuating environment. Trends Ecol Evol 12: Sih A, Kats LB, Moore RD (1992) EVects of predatory sunwsh on the density, drift, and refuge use of stream salamander larvae. Ecology 73: Siivonen L, Sulkava S (1994) Mammals of northern Europe (in Finnish). Otava, Helsinki Simms DA (1979) North American weasels: resource utilization and distribution. Can J Zool 57: Sundell J, Norrdahl K (2002) Body size dependent refuges in voles: an alternative explanation of the Chitty evect. Ann Zool Fenn 39: Sundell J, Ylönen H (2004) Behaviour nad choice of refuge by voles under predation risk. Behav Ecol Sociobiol 56: Sundell J, Trebatická L, Oksanen T, Ovaskainen O, Haapakoski M, Ylönen H (2008) Predation on two voles species by a shared predator: antipredatory response and prey preference. Popul Ecol 50: Vamosi SM (2005) On the role of enemies in divergence and diversi- Wcation of prey: a review and synthesis. Can J Zool 83: Viitala J, HoVmeyer I (1985) Social organization in Clethrionomys compared with Microtus and Apodemus: social odours, chemistry and biological evects. Ann Zool Fenn 22: Wohlfahrt B, Mikolajewski DJ, Joop G, Suhling F (2006) Are behavioural traits in prey sensitive to the risk imposed by predatory Wsh? Freshwater Biol 51:76 84 WolV JO, Freeberg MH, Dueser RD (1983) InterspeciWc territoriality in two species of Peromyscus. Behav Ecol Sociobiol 12: Ylönen H, Viitala J (1991) Social organization and food distribution in the bank vole Clethrionomys glareolus. Holarctic Ecol 14: Ylönen H, Brown JS (2007) Fear and the foraging breeding and sociality in rodents. In: WolV JO, Sherman PW (eds) Rodent societies. University of Chicago Press, Chicago, pp