Predation risk and food: opposite effects on overwintering survival and onset of breeding in a boreal rodent

Authors

  • Marko Haapakoski,

    Corresponding author
    1. Department of Biological and Environmental Science, Konnevesi Research Station, University of Jyväskylä, PO Box 35, 40014 Jyväskylä, Finland
      Correspondence author. E-mail: marko.j.haapakoski@jyu.fi
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  • Janne Sundell,

    1. Lammi Biological Station, University of Helsinki, Pääjärventie 320, 16900 Lammi, Finland
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  • Hannu Ylönen

    1. Department of Biological and Environmental Science, Konnevesi Research Station, University of Jyväskylä, PO Box 35, 40014 Jyväskylä, Finland
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Correspondence author. E-mail: marko.j.haapakoski@jyu.fi

Summary

1. In seasonal environments, optimal onset of breeding and survival plays major roles in individual fitness. Many physiological and behavioural factors related to breeding increase the risk of predation; thus, breeding decisions should be based on current risks and benefits. According to life-history theory, if current predation risk is high and breeding itself increases the risk, it may be beneficial to postpone breeding.

2. During winter in northern hemispheres, food availability is limited and is at its lowest just prior to the onset of breeding in spring. Food constraint may lead to poor condition and reduced ability to start breeding.

3. We studied the effects of food and predation risk on winter survival and onset of breeding in a common boreal rodent, the bank vole (Myodes glareolus). In a 2 × 2 factorial experiment, we manipulated food availability (food supplemented or not) and predation risk (presence/absence of predator odour) in 20 large outdoor enclosures in central Finland.

4. Survival probabilities were highest in no predation risk treatments, whereas they were lowest in the predator risk treatment. The same trend was observed in vole densities and the weight change in individuals. Voles with food addition bred earlier than in the other treatments.

5. We conclude that during energy constrained harsh conditions in winter, predation risk causes behavioural changes throughout the winter and has significant negative survival and fitness effects for small mammals, reflected as delay in the start of breeding.

Introduction

The roles of external factors such as predation and food in population regulation have puzzled population biologists for decades (Elton 1949). Food supplementation has been shown to affect positively survival and breeding across vertebrate taxa (see Boutin 1990; for review), and predation is one of the most widely studied processes negatively affecting prey populations (Krebs et al. 2001; Schmitz 2008). The mere risk of predation is known to affect behaviour, morphology and physiology of the prey individuals (Lima & Dill 1990; Lima 1998, 2002). Risk effects arise when a prey alters its behaviour in response to predation risk, and these responses carry survival or reproductive costs (Boonstra et al. 1998; Preisser, Bolnick & Benard 2005; Creel & Christianson 2008).

Predation risk effects on prey fitness are cascade-like processes. A common response of a prey is to avoid contacts with the predator by reducing activity or movement areas. Reduced activity and searching for food restricted to smaller area will lead to a reduced foraging efficiency and consequently may influence individual condition. In addition, predator avoidance by decreased activity during reproductive period may lead to missed encounters with potential mates (Brown 1988) or otherwise disturbed sexual encounters (Ronkainen & Ylönen 1994) and hence to lowered fitness. A lowered body condition can affect the breeding success by causing smaller and/or lower quality litters. It is also possible that the onset of breeding after the non-breeding season may be delayed and even cause a reduction in the number of litters produced during the shortened breeding season (Eccard & Ylönen 2001).

Suppressed or delayed breeding as an adaptive strategy enhancing individual (female’s) reproductive success, as proposed by Ylönen & Ronkainen (1994), has been tested experimentally and its optimality has been modelled in several studies. The main message is that under best breeding season conditions with all individuals in ‘moderate to high reproductive performance’ (Kokko & Ranta 1996), the strategy of not breeding is not optimal regardless of strength of predation pressure. This has also been proven in experimental populations (Mappes, Koskela & Ylönen 1998) under simulated predation risk during boreal summer. However, the theoretical approaches by Kokko & Ranta (1996) and Kokko & Ruxton (2000) leave the possibility open that some additional restrictive conditions are necessary before delayed breeding could be optimal. The same phenomenon of possible additive nature of predation risk with other breeding constraining factors like food limitation or high conspecific density stress was suggested also by Hansson (1995) and Ylönen, Koskela & Mappes (1995). The few studies having verified breeding delay in the field also come from this kind of restrictive conditions, from sub-alpine environment (Fuelling & Halle 2004) and from the latter half of the breeding season with high conspecific densities (Jochym 2011).

In northern areas, winter survival and onset of breeding are constrained by the kind of restrictive conditions described by Kokko & Ranta (1996) and Kokko & Ruxton (2000). Winter season is characterized by diminishing food resources and higher energetic demands for overwintering ground-dwelling animals because of low temperatures combined with high moisture in the sub-nivean space. On the other hand, the long-lasting permanent snow cover protects ground-dwelling small rodents from most predators during winter. Under the snow, the greatest predation risk threat is caused by small mustelids, especially by the least weasel (Mustela nivalis nivalis), which is small enough to hunt voles in their tunnels and cavities of the sub-nivean space. On the snow surface, dangers are more diverse and are caused by generalist mammalian predators and owls. In the sub-nivean space, vole predation is predictable. If there is a hunting small mustelid like the weasel in the area, there probably are also signs of its activity in the form of weasel scent (Erlinge, Sandell & Brinck 1982). On the other hand, lack of weasel odour cues under the snow should reliably indicate a low predation risk. Many of the experiments conducted during the breeding season using predator odour have failed to find effects of experimentally increased risk on breeding or spacing behaviour (Wolff & DavisBorn 1997; Jonsson, Koskela & Mappes 2000; Hellstedt, Kalske & Hanski 2002). However, it is likely that under the snow, the odour remains present for a longer period of time than in open air, because air circulation that increases the evaporation of volatile compounds in the weasel scent (Brinck, Erlinge & Sandell 1983) is practically absent. In addition, the reduced activity of microbial decomposers during cold climate should increase the time when volatile compounds are present.

In a strongly seasonal environment, overwintering rodent populations decline from the autumn population highs to next spring. Local populations may go also extinct, which has been shown in both experimental field populations (Aars & Ims 2002) and in enclosure experiments (Eccard et al. 2011a). Survival over the non-breeding season, gaining energy for physiological changes needed for hormonal changes during maturation after winter (Galea & McEwen 1999) and optimal timing of first reproduction are major determinants of individual fitness (Roff 1992; Eccard & Ylönen 2001). When to start breeding is the key question for iteroparous income breeders such as the bank vole (Myodes glareolus). Individuals may gain significant fitness benefits by starting to breed earlier than competing conspecifics, if the successfully weaned offspring are among first ones to start the next cohort breeding (Millar & Gyug 1981; Ergon 2007).

Overwinter survival, individual condition measured as weight change from the early winter weight to spring weight, as well as onset of breeding, have been shown to be strongly improved by food supplementation (Boutin 1990; Ylönen & Eccard 2004; Von Blanckenhagen, Eccard & Ylönen 2007). Studies on predation risk effects in winter are rare (see Krebs et al. 1995), but even if information would exist, it would be confounded by more plausible explanation of food limitation during the harsh non-breeding season (Creel & Christianson 2008). However, both predation risk and food can limit populations as suggested by Krebs et al. (1995) in their experimental case of the snowshoe hare (Lepus americanus).

Studying direct predation impact experimentally during winter is not possible. Thus, we conducted for the first time an experiment in 20 large outdoor enclosures to test the effects of either long-lasting predation risk (weasel odour under the snow) or continuous high quality food supplementation and their interaction for overwintering success and onset of breeding in bank voles. More importantly, we measured direct fitness effects of fear of predation on the population scale during the snowy period of winter when vole populations decline strongly or even go locally extinct (Aars & Ims 2002). Predation risk is not expected to cause direct mortality effects (cf. Preisser, Bolnick & Benard 2005), but could affect condition and even survival by indirect interactions with decreased activity and foraging, increased stress and vigilance and predator facilitation if risk under snow drives individuals on the snow and exposed to direct predation. We hypothesized that:

  • 1 Vole condition and survival are negatively affected by risk of predation and positively by food supplementation.
  • 2 Food supplementation advances breeding and predation risk delays it.

As we predict opposite effects of food and predation risk, an open question of the strength of these factors for individual performance remains in populations where both treatments run simultaneously.

Materials and methods

The experiment was carried out in 20 enclosures of 0·25 ha (50 m × 50 m) in size, fenced with metal sheets that reach 0·5 m below ground and c. 0·7–1 m above the ground preventing voles from escaping. Enclosures were built into old fields where vegetation was mainly tall grassland with some Salix spp. bushes. Bank voles commonly live in this kind of habitat in the absence of competition from larger species. In each enclosure, there were 25 Ugglan special multiple capture traps (Ugglan special, Grahnab ab, Hillerstorp, Sweden) in 10-m intervals in a 5 × 5 grid. The traps were covered with bottomless metal chimneys that allowed food and predation risk manipulation under the snow and trapping in snowy conditions.

Study species

The bank vole is small, common boreal microtine rodent. The breeding season of bank voles usually begins at the end of April and lasts until September. During the non-breeding season, bank voles are assumed to overwinter in small aggregations in winter nests (West & Dublin 1984; Ylönen & Viitala 1985). During the breeding season, female bank voles are strictly territorial and need an exclusive territory to breed (Bujalska 1985). Breeding male territories overlap with several female territories (Ims 1987).

The least weasel is a small mustelid specialized on hunting small mammals. Weasels maintain a kind of foraging territory during the breeding season (Erlinge 1974, 1975), but there is little information of weasel movements or spacing behaviour during winter (Nyholm 1959), but weasels hunt both on and under the snow. Populations of bank voles, like other small vole species fluctuate cyclically in boreal landscapes (e.g. Hanski et al. 2001). Weasel populations follow the vole cycles with an approximately half-year time lag (Korpimäki, Nordahl & Rinta-Jaskari 1991).

Experimental design

Experimental voles were bred in captivity and housed individually after weaning age (20 days) in standard mouse cages with wood shavings and dry hay as bedding material in the Konnevesi Research Station’s animal house. Water and food in the form of rodent pellets (LabFor) were available ad libitum. Light regime in the laboratory was 18L: 6D during summer and 12L: 12D from September onwards. At the beginning of the experiment, voles were 2–5 months old and marked individually with ear tags (Hasco Tag Company, Dayton, KY, USA, type 1005-1). Five female and five male bank voles were released into each enclosure during the second week of October. Weight and age distribution of the voles was equalized for all enclosure populations. No siblings or half-siblings were released into the same enclosure. Three weeks before releasing, the vole cages were brought to outdoor shelter to let voles acclimatize to the natural day length and temperatures.

It is commonly known that late autumn mortality before onset of permanent snow cover is high, especially because of avian predation before the onset of snow cover. Furthermore, increased stress levels of captive bred animals to the nature (Eccard, Jokinen & Ylönen 2011b) can increase mortality considerably. To compensate for this early mortality, we trapped enclosures on the 15th of November to assess vole post-release survival. Male survival from the release was lower than female, which was expected based on an earlier experiment (Klemme, Ylönen & Eccard 2008). At the end of this trapping session, vole densities in the enclosures were standardized by relocating voles from higher densities to lower-density enclosures, to give equal starting densities of three to four females and three males in each enclosure.

Food supplementation treatment

Food supplementation in the form of protein muffins was added biweekly in half (10) of the enclosures. Protein muffins were made of 4·5 g of hera80® protein and 15 g sunflower seed. These were mixed into a paper muffin mould and attached to a solid form with gelatin liquid. Ingredients for the muffins were chosen based on earlier studies, so that they included both plant (Ylönen & Eccard 2004) and animal protein (Von Blanckenhagen, Eccard & Ylönen 2007). Muffins were spread in 12 (every second) trap chimneys of the food supplementation enclosures. Food supplementation started in mid-November and lasted until the second week of April. Supplemental food was added to the enclosures 11 times, and altogether 132 protein muffins were added per enclosure. Each time new muffins were added, and the possible remnants from the previous supplementation were removed. As the food remnants were scarce, because of moderate food supplementation rate c. 2·5 g day−1 including husk with initial vole density, we did not weigh the remnants. Therefore, no direct consumption by voles was estimated. To give some reference value, bank voles living in rodent cage consumed 2·7 g of high protein and 3·5 g of low protein rodent pellets (S. Sipari, M. Haapakoski, I. Klemme, J. Sundell & H. Ylönen, unpublished) in climate-adjustable laboratory at 8 °C.

Predator risk treatment

Predator odour was made from c. 1·2 kg of weasel latrine beddings containing in average 330 g faeces that were collected from cages of a weasel colony housed at the Konnevesi Research Station. Faeces of many individuals and both sexes were mixed with 5 L of water and with c. 28 L of dry wood shavings in a 30-L bucket. The bucket was sealed with an air-tight lid and stored overnight at temperature of 4 °C. This was performed to get the smell and moisture evenly distributed into the wood shavings. The mixture was spread the following day. For all biweekly spreading of weasel odour, the mixture was prepared fresh. As control treatment, we used clean wood shavings mixed with water in same proportion than predator smell to make its consistency similar to that in predator treatment enclosures. One cup (c. 0·1 L) of the predator odour and control odour was spread biweekly in each trapping chimney in half of the enclosures. The weasel odour liquid was prepared with the same amounts of faeces and water like in summer studies where the odour then was sprayed to the vole habitat (e.g. Mappes, Koskela & Ylönen 1998). However, because of winter temperatures and avoiding freezing of ground in trap chimneys, we choose to use the mix of wood shavings and weasel scent. The amount of manipulated wood shavings for each trap chimney, probably, was as treatment weaker than the summer sprayings, but remained longer in confined sub-nivean space.

For all treatment populations, the avian predation risk caused by resident pygmy owls (Glaucidium passerinum) and Ural owls (Strix uralensis) was similar. Both owl species were seen, or hunting signs of them on snow cover were frequently found throughout the winter. Presence of pygmy owls was also evident in fresh caches from November in the nest boxes in the vicinity of the enclosure area.

Overall, the experiment was conducted in 20 enclosures: five enclosures with predator odour and without food supplementation (P+F−), five with food supplementation (P−F+), five with predator odour and food supplementation (P+ F+) and five enclosures with control odour and without food supplementation (P−F−). We had to exclude one enclosure (P−F+) from the analysis because the fence was damaged and field voles (Microtus agrestis) invaded the enclosure.

Trappings

Voles were trapped over one to two nights including two to three trap checks starting in February 21st, March 13th, March 30th, April 18th, May 9th and May 30th to follow vole survival, body mass and breeding condition. During trapping, traps were baited with a fifty–fifty mixture of sunflower seeds and oats. When traps were set, supplemental food was removed from the trap chimneys. Traps were emptied of the seeds and food, and predation treatments were always applied after trapping session. During each trapping session, voles were weighted with a Pesola scale to the nearest 0·5 g and their breeding status was recorded using similar method than Ergon, Lambin & Stenseth (2001), that is, females were defined as mature and capable for breeding when their vagina was perforated and males were regarded mature when their testes were in a scrotal position.

Statistical analysis

For data analysis, we used mixed effects models and library nlme (Pinheiro et al. 2010) in r (R Development Core Team 2010). Model selection was conducted by choosing the best model from the set of predefined models based on AIC (see Tables S1–S5, Supporting Information). Maximum likelihood method was used for comparing models and restricted maximum likelihood (REML) in the final model to obtain the model estimates. Based on initial evaluation (Zuur et al. 2009) and to account for pseudoreplication, enclosure was used as a random factor in all analysis. Predation risk, food supplementation and sex with all two-way interactions were used as fixed factors in the full model in the analysis.

Only individuals larger than 15 g in February were included in the analysis of the onset of breeding. Three female voles, one from P+F+ and two from P−F+, were lighter than 15 g in February and were excluded from the onset of breeding analysis. The onset of breeding was measured as the number of days after observing the first mature individual (open vagina in females, scrotal testes in males) in any enclosure. Vole condition was measured as a weight change from November to February. Weight change, although it does not measure directly condition, can be used as proxy for condition because it can be manipulated with supplemental food and it clearly affects breeding success after winter (Ylönen & Eccard 2004). All gravid females in February (n = 4) were excluded from condition analysis.

We analysed onset of breeding also by the date when 50% or more of individuals in the each enclosure were mature to be sure that our result is not based on the outliers in the data (Ergon et al. 2011). A two-way anova was used in this analysis with food, predation and the interaction as fixed factors. The interaction model was the full model, and all combinations until null models were run. Best model was chosen by lowest AIC. Both sexes were analysed first together, and then females and males were analysed separately.

For survival analysis, we used r (R Development Core Team 2010) package rmark (Laake & Rexstad 2008) to construct models for program mark (White & Burnham 1999). Survival analysis of different treatments was compiled by Cormac-Jolly-Seber (CJS) models with all the enclosures pooled, and it was conducted only with the founder voles. The CJS models allow an independent estimation of apparent survival (Φ) and recapture probabilities (P). We fitted survival and recapture models as functions of predation risk, food supplementation and time with their two-way interaction and sex without interaction (see all the candidate models from electronic supplementary material). We were studying the model fit/overdispersion of the most complex model with program RELEASE (Burnham et al.1987) test 2 and test 3. Models with ΔAICc values <2 (Burnham & Anderson 2002) were selected for model averaging to get survival and recapture probability estimates and standard errors.

We also monitored overall vole density in enclosure. The expectation was a general decline of adult densities. However, because of snow cover in some places reaching the height of the fence, and due wind-formed temporal snow bridges at the fences, there was possibility for some immigration from outside to the enclosures. This was only the case in the one food treatment enclosure, which attracted eight immigrant bank voles between November and February. These individuals may be seen behind the mid-winter increase in adult densities in the food treatment, but they were excluded in all other analyses. Density was analysed from capture data with robust design model in R (R Development Core Team 2010) with package Rcapture (Baillargeon & Rivest 2007). Chao m0 model was used to get the density estimates for each trapping session for each enclosure. In the density analysis, we used log-transformed densities. Trapping session within each enclosure was used as random factor to take account for the temporal pseudoreplication (Crawley 2007), and time was added as fixed variable. We analysed both sexes pooled, that is, total number of voles estimated to be alive in the enclosure.

Results

Winter climatical conditions

The study winter was very stable, and a permanent snow cover lasted from the end of November until April. We monitored sub-nivean and above snow temperatures using data loggers (Kooltrak®). The air temperature stayed below zero from December until the beginning of April. Thus, the snow kept its insulating properties for the whole snowy period and subnivean temperature was stable, close to 0 °C for the whole study period (Fig. 1).

Figure 1.

 Overwinter temperatures in °C at the study area. Black line shows the air temperature at 1·5 m height and dash line the sub-nivean temperature.

Onset of breeding

Predator odour (P+) delayed breeding compared to the P−F− treatment on average by 9·9 days (±4·7 SE), which was marginally non-significant (LME, Predator: F1,16 = 3·72, P = 0·072). Food supplementation (F+) advanced onset of breeding significantly by 20·6 (±4·7) days compared to P−F− treatment (LME, Food: F1,16 = 18·43, P < 0·001, Fig. 2). This approximates to 1 month difference between F+ and P+ treatments. In all enclosures, some males matured early, but surprisingly, on average females, matured earlier than males (LME, Sex: F1,66 = 6·28, P = 0·015). This may be due to fact the first signs of male maturation, especially during cold winter climate, are not as exact to determine like perforate vagina in females.

Figure 2.

 Onset of breeding (days) mean ± SE after first breeder in different treatments. Day 0 represents February 21st. P+ = increased predation risk manipulated with weasel odour soaked in clean wood shavings, P− = predation risk control, clean wood shavings only, F+ = supplemental food including plant and animal protein, P− = no food supplementation. Sample size on the right from the bars.

When analysing the onset of breeding by using date when at least 50% of individuals in each enclosure were in breeding condition, the model including food was supported. Food advanced onset of breeding significantly for both sexes combined (anova, Food: F1,17 = 9·68, P = 0·006). The same was true for females on their own (anova, Food: F1,17 = 11·74, P = 0·003), whereas for the males, the best model included food + predation, but only the food effect was significant (anova, Food: F1,14 = 7·09, P = 0·019, predation: F1,14 = 2·32, P = 0·150).

Individual Condition

Predation risk (P+) decreased, and food (F+) or sex alone did not affect the condition measured as a weight change from November to February in the voles (LME, Predator: F1,13 = 9·22, P = 0·009; Food: F1,13 = 0·23, P = 0·636; Sex: F1,55 = 1·58, P = 0·214). Food and predation had close to a significant interaction (LME, Food × Predator: F1,13 = 3·82, P = 0·073). However, males gained most weight when food was supplemented, but only if there was no predation risk P+ present (Predator × Food × Sex T1,55 = 9·02, P = 0·004; Fig. 3) for all other studied factors or combinations P > 0·214.

Figure 3.

 Weight change from November to February as index of individual condition; mean ± SE for females and males in different treatments. Sample size above x-axis. See captions from Fig. 2 legend.

Survival and density

All the best models, AICc < 2 for survival probabilities included time, sex and predation risk and only one included food. For recapture probabilities, the most important factors were predation risk × time interaction and sex (Fig. 4, Table 1).The goodness-of-fit tests with program RELEASE indicated minor underdispersion (inline image = 8·00, P = 0·628, ĉ = 0·80) of the most complex model to our data, so we set ĉ to one (Burnham & Anderson 2002). Model averaged survival probabilities to the next trapping session were highest in the P−F+ treatment and lowest in the P+F− treatment. The mean difference between these two treatments was about 10% and between some trapping sessions up to 20% (Fig. 4a,b). Overall survival estimates from November until the end of April for females were (P−F + 31%, P−F− 30%, P+F + 21% and P+F− 20%) and for the males (P−F + 18%, P−F− 17%, P+F + 10% and P+F− 10%).

Figure 4.

 Survival probability estimates ±SE of females (a) and males (b) in different treatments between different trapping sessions. Recapture probabilities ±SE of females (c) and males (d) in different treatments between different trapping sessions. All estimates are based on model averaging of five best Cormack Jolly Seber model. See captions from Fig. 2 legend. Filled symbols represent treatments with food addition F+, squares those with wesel odour P+.

Table 1. Five best models for survival (Φ) and for capture probability (P) according to ΔQAIC (quasi-likelihood corrected AIC for small sample size)
ModelNparQAICcΔQAICcWeightQDeviance
  1. Npar = number of parameters, QAICc = difference between model QAICc and minimum QAICc, weight = relative strength of evidence for a model within the set of models computed and QDeviance = total deviation between the computed model and a saturated model of the data.

Φ(∼time × predator + sex)
P(∼time × predator)
17938·6800·36203·27
Φ(∼food + predator + sex + time)
P(∼time × predator)
15939·831·150·20208·59
Φ(∼time + predator + sex)
P(∼time × predator + sex)
15940·371·680·16209·13
Φ(∼time + predator + sex)
P(∼time × predator)
15940·591·910·14209·35
Φ(∼time × predator + sex)
P(∼time × predator + sex)
18940·621·930·14203·12

There was a tendency that recapture rate estimates were consequently lower in both predator treatments P+F− and P+F+ (mean, 91% for females and 90% for males) than in the two treatments without weasel odour P−F− and P−F+ (mean, 95% for males and females, Fig. 4c,d).

Predation risk (P+) decreased vole density significantly (LME, Predation: F1,16 = 5·17, P = 0·037; Fig. 5). Density was not significantly higher in F+ treatment (LME, Food: F1,16 = 1·84, P = 0·193). Vole densities decreased with time (LME, Time: F1,93 = 16·22, P = 0·001).

Figure 5.

 Mean ± SE overall density estimates in different treatments in different trapping sessions. See captions from Fig. 4 legend.

Discussion

The survival estimates of the founder individuals of overwintering populations were highest in no predation risk and lowest in the increased predation risk treatments regardless of food supplementation. Predation risk, even without direct predation, had a strong effect in our experimental populations. It caused lower densities than in other treatments, especially in males, and a generally lowered body condition measured as weight change. Surprisingly, food supplementation did not increase survival or condition significantly. However, voles with supplemental food started to breed first and predator odour treatment delayed the onset of breeding by almost 1 month compared to food supplementation treatment. Physical conditions with stable, albeit very low, temperatures below zero (Fig. 1) and thick snow cover were favourable for general overwinter survival of voles (cf. Aars & Ims 2002) and did not confound our experimental treatment effects.

Overwinter survival affected by predation risk

Founder vole survival probabilities to the next trapping were c. 10% lower in predation risk enclosures than in food supplementation or in enclosures where food or predation risk were not manipulated (Fig. 4). More remarkably, during the most adverse periods when the overall survival was lowest, the effect of predator odour was close to 20%. Mere predation risk has been recognized as an important factor to negatively affect behaviour and consequently also population processes (for review Creel & Christianson 2008). Survival probabilities were highest in the food supplementation treatment, which was an expected result found in many overwintering studies (Boutin 1990; Ylönen & Eccard 2004). When there was food and predator odour combined in the enclosure, predator odour seemed to have a stronger effect. Thus, in this rare long-term experiment over non-breeding season, predation risk seemed to be a more important factor for the survival than food supplementation. Our study was not designed to measure direct predation effect, but it seems to support ideas proposed by (Preisser, Bolnick & Benard 2005) about a strong negative population effect of sole intimidation.

Our biweekly predation risk treatment used 1·2 kg of weasel latrine beddings mixed with wood shavings and water contained on average 330 g of weasel faeces plus some urine soaked in 30 L of wood shavings. This amount of ‘fear’ was spread into 250 trap chimneys, where the amount per chimney is a small cup of 1·5 dL maximally. We suggest our treatment to be close to biologically normal range compared to Short’s (1961) experiment where captive least weasel produced c. 20 g of faeces during same time. However, in our experimental set-up, the whole amount of weasel scent was applied at the same time across the whole enclosure area, whilst in nature, it would accumulate in latrine patches slowly over time. This might be one reason why predation risk treatment was so effective in our experiment.

Survival probability pattern between trapping session was similar for male and female voles with highest survival in F+P− and lowest in F−P+. Female survival probability estimates were in general higher (with an average of all treatments above 25%) than those of males, with lower than 14%. This is in accordance with other studies in boreal microtine rodents (Aars & Ims 2002; Klemme, Ylönen & Eccard 2008). One suggested reason for lower survival of males may be the larger body size and higher metabolic rates (Ergon et al. 2004). In the predation treatment, the disappearance of males may also be due to escaping predation risk by movements out of sub-nivean space on to the snow, and in many cases, those males may well be regarded to be ‘scared to death’Preisser, Bolnick & Benard (2005). Sundell et al. (2000) observed occasions where voles that have left their nest and escaped weasels on the snow were later found dead because of other causes than direct predation. They suggest that voles were exposed to the harsh weather conditions whilst searching for another shelter. Stronger behavioural response in males compared to females has been found also in other studies, for example in golden hamsters, Mesocricetus auratus, (McPhee, Ribbeck & Johnston 2009) or in meadow voles (Microtus pensylvanicus) (Perrot-Sinal et al. 1996). Leaving the warm nest in winter is risky due to the increased energetic and thermoregulatory demands, but also to the increased risk of being killed by predators. In our study, more mobile males may have been more prone to get killed by owls, as we observed a few successful owl hunting tracks on the snow during trappings.

Survival probability patterns with lowest survival from November to February and March to April also prove that the most critical times for vole survival are the early winter before thick snow cover (before we started manipulations) and the time when the insulating and protecting snow is melting in March and April (Merritt 1978; Huitu et al. 2003). Huitu et al. (2003) suggested that a spring decline in density is caused by the lack of food under the snow, at least in Microtus voles like used in that study. This hypothesis is not fully supported by our experiment with Myodes voles because survival probabilities were lower in both predation treatments with P+F− and P+F+ than without predator cue (P−F+ and P−F−). Survival probabilities were rising again in the last trapping session at the beginning of May when temperatures increased and vegetation slowly started to recover.

Predation risk (Hik, McColl & Boonstra 2001; Sheriff, Krebs & Boonstra 2009) and food depletion (Kusumoto 2009) can increase stress of an individual. Predation risk induced increased stress levels may have negative physiological effects. Similarly, reduced food intake in risky situation may cause poor condition (Sheriff, Krebs & Boonstra 2010). These negative effects on condition may also increase individual vulnerability to parasites or pathogens (Pedersen & Greives 2008). The role of parasites and pathogens in combination with food constraint (Huitu et al. 2003) or with winter-time predation risk, studied for the first time here, cannot be excluded as a mechanism for lower survival in the predation risk treatments. It is also possible that weasel risk may have driven voles on the snow and into the talons of the owls, especially those of pygmy owls and Ural owls in our study, which were resident around study area throughout the winter.

Onset of breeding, individual condition and predation risk

Decreased weight during winter (Dehnel’s phenomenon, Brown 1973) can be an adaptive response to decrease energy need during the most food constrained period of year. In our study, it can also be consequence of decreased foraging under predation risk, irrespective if food was supplemented or not (Hodges, Boonstra & Krebs 2006). We found that food supplementation increased male body mass, but predation risk decreased it even with food supplementation. Our finding with a significant interaction with food supplementation and predation risk in males is similar to what Hodges, Boonstra & Krebs (2006) found for the snowshoe hare. Bank vole males seem to be more sensitive to increased foraging cost caused by high predation risk similar to golden hamster (McPhee, Ribbeck & Johnston 2009) and meadow vole males (Perrot-Sinal et al. 1996) than females.

Voles with enhancement of high quality food supply (P−F+ and P+F+) started to breed earlier, whereas P+F− treatment delayed onset of breeding by almost 1 month (see also Boutin 1990; Von Blanckenhagen, Eccard & Ylönen 2007). In the combined treatment with food and predation, the voles probably decreased their activities because of fear and could not exploit effectively the offered supplemental food (Kotler, Brown & Bouskila 2004). This may be supported by the tendency of lower recapture probability in both predator treatments during early and mid-winter as predator odour was spread into the same trap chimney than the supplemental food. Voles needed to be more vigilant, which might have lead to lowered condition in the P+F+ enclosures as well.

Our experiment provides a clear effect that weasel odour simulated predation risk delaying onset of breeding after long breeding inactivity during winter. The effect was also evident in combination with supplemental food, which alone has proven to have an overwhelming positive effect on individual performance and breeding (see Boutin 1990; for review). Our results are in clear contradiction with studies carried out during best of breeding season in summer (Wolff & Davis-Born 1997; Mappes, Koskela & Ylönen 1998) having observed no effect of weasel scent simulated increased predation risk on vole reproduction. In theoretical models on optimal reproduction, ‘doing something wrong in terms of reproductive opportunity’ during the best of breeding season, regardless of intensity of predation risk, seems not to be valid option for short-lived iteroparous breeders (Kokko & Ranta 1996; Kokko & Ruxton 2000). However, like in our study, breeding delay under some additionally constraining or restrictive environmental circumstances has support. Fuelling & Halle (2004) observed decreased recruitment in the sub-arctic grey-sided vole (Myodes rufocanus) under weasel odour simulated predation risk. In a recent study, Jochym (2011) observed density-mediated breeding delay in the common vole (Microtus arvalis) also under field conditions. Thus, we conclude that in our experiment focusing on onset of breeding in a seasonal breeder, we entangle predation risk effects additive to some restrictive environmental factors suggested by Kokko & Ruxton (2000) to be needed for breeding delay to be adaptive and valid hypothesis to enhance individual reproductive success. We know already from a previous open population field experiment that conspecific female density affects onset of breeding (Eccard & Ylönen 2001). Here, we can add verification of predation risk effects having a similar effect in spring populations of bank voles.

Conclusions

To conclude, predator odour had strong effects on survival probabilities, density and condition of the voles overwinter. At the onset of breeding, the food effect was stronger that could mean that as an individual has ‘decided’ to breed despite the possible increased risk of predation, it uses all means to gain more energy for successful reproduction. However, fear effect can sometimes suppress the positive effect of supplemental food as seen here in the case of male condition in P+ F+ treatment. Our experiment clearly verified an effect of increased predation risk delaying breeding after long non-breeding season. Thus, environmental constraints after winter may form the kind of restrictive conditions needed additionally to risk of predation to affect directly or through nutritional constraints individual breeding strategies. We also think that we were successful in manipulating increased risk of predation with an odour cue in the sub-nivean space without vole habituation to the risk.

Acknowledgements

We thank the technicians of the Konnevesi Research Station and additionally Jani Korpilauri and Lenka Trebaticka for help in the field work. Ines Klemme, Carl Soulsbury, Rolf A. Ims and two reviewers provided valuable comments on the manuscript. The study was supported by the Finnish Academy to the CoE in Evolutionary Ecology at University of Jyväskylä. The Authors declares that there is no conflict of interest. Experiment and animal handling were conducted with animal experimentation permission at Jyväskylä University no. 35/31.5.2004.

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