Dynamic impacts of feral mink predation on vole metapopulations in the outer archipelago of the Baltic Sea

Predation impacts by introduced predators are predicted to be most intense in island ecosystems, and also variable depending on environmental conditions, but large-scale experimental field testing is rare. In this study we examine the factors that determine the distribution and abundance of vole metapopulations preyed upon by feral American mink Mustela vison in the outer Finnish archipelago of the Baltic Sea. Specifically, we follow the dynamics of field voles Microtus agrestis and bank voles Clethrionomys glareolus on 40 small islands under variable rainfall as part of a large-scale mink removal experiment. For both vole species occupancy rates were negatively influenced by island isolation, as were extinction events for field voles. High summer rainfall in 1998 corresponded to large vole populations where mink were absent, populations that then crashed in 1999 and 2000 when below average rains fell during the summer breeding season. Where mink were present however, vole abundance remained more constant between years with no boom-bust apparent. We conclude that weather and predation may drive vole abundance whereas habitat patchiness and metapopulation processes more strongly drive vole distributions. There may also be potential for interaction between these factors: because feral mink prevent rapid vole population growth after good summer rains, and vole dispersal is influenced by population size, feral mink may be changing vole dispersal patterns to disrupt the natural metapopulation dynamic. Hence this indirect impact of mink could lead to gradual erosion of vole populations in the outer archipelago by reducing recolonisation processes.     

Local and Regional Determinants of Colonisation-Extinction Dynamics of a Riparian Mainland-Island Root Vole Metapopulation

The role of local habitat geometry (habitat area and isolation) in predicting species distribution has become an increasingly more important issue, because habitat loss and fragmentation cause species range contraction and extinction. However, it has also become clear that other factors, in particular regional factors (environmental stochasticity and regional population dynamics), should be taken into account when predicting colonisation and extinction. In a live trapping study of a mainland-island metapopulation of the root vole (Microtus oeconomus) we found extensive occupancy dynamics across 15 riparian islands, but yet an overall balance between colonisation and extinction over 4 years. The 54 live trapping surveys conducted over 13 seasons revealed imperfect detection and proxies of population density had to be included in robust design, multi-season occupancy models to achieve unbiased rate estimates. Island colonisation probability was parsimoniously predicted by the multi-annual density fluctuations of the regional mainland population and local island habitat quality, while extinction probability was predicted by island population density and the level of the recent flooding events (the latter being the main regionalized disturbance regime in the study system). Island size and isolation had no additional predictive power and thus such local geometric habitat characteristics may be overrated as predictors of vole habitat occupancy relative to measures of local habitat quality. Our results suggest also that dynamic features of the larger region and/or the metapopulation as a whole, owing to spatially correlated environmental stochasticity and/or biotic interactions, may rule the colonisation – extinction dynamics of boreal vole metapopulations. Due to high capacities for dispersal and habitat tracking voles originating from large source populations can rapidly colonise remote and small high quality habitat patches and re-establish populations that have gone extinct due to demographic (small population size) and environmental stochasticity (e.g. extreme climate events).     

The impact of American mink Mustela vison and European mink Mustela lutreola on water voles Arvicola terrestris in Belarus

In the U.K. the impact of introduced American mink Mustela vison , on water voles Arvicola terrestris , may be exacerbated by habitat loss and fragmentation. Pristine wetlands in Belarus, which American mink invaded in the early 1990s, provide a three-pronged opportunity to test this hypothesis. First, we examine the evidence that, even in the unmanaged wetlands of our Belarussian study site, American mink have reduced water vole populations. Second, we ask whether habitat size, type and isolation mitigate the impact of American mink predation. Thirdly, we explore whether water voles are at greater risk of predation from American than European mink because of their patterns of habitat use. Following the invasion of American mink, water voles were most abundant in small, still-water sites, far from river banks, while American mink were most active in large, running-water sites. Small mammal remains were found in a higher percentage of American than European mink scats, and of these, more were water vole in American mink scats. The occurrence of water voles in scats of both mink species declined after the American mink invaded and established. Our results provide at least circumstantial evidence that American mink limit water vole populations even in unmanaged wetland eco-systems, and that they have a greater impact than their European congener at least partly because they make greater use of isolated marshes. Although by no means providing complete protection, the configuration and dispersion of available habitat mitigated the impact of American mink on water voles. This raises the possibility that habitat restoration, especially through the establishment of isolated enclaves, could help reduce the effect of American mink in the U.K. These observations are of broader interest in the context of assessing the effect of multiple pressures on vulnerable species.     

European water voles in a reconnected lowland river floodplain: habitat preferences and distribution patterns following the restoration of flooding

Water voles have suffered large population declines in the United Kingdom due to habitat degradation and predation by invasive American mink. Habitat restoration of floodplain wetlands could help to reverse this decline, but the detailed habitat preferences of water voles in these environments have not been well studied, and the impacts of restoration practices on water vole populations are not known. This study investigated the habitat preferences of water voles in a reconnected lowland river floodplain. The results show that water voles preferred wider water bodies, and taller and more diverse vegetation. The impact of flooding on water voles was also investigated by comparing their occurrence between two survey periods which were separated by large flood events, and by comparing distribution patterns before and after restoration. Contrary to previous reports, there was no observed negative impact of flood events on water vole distribution, which has slightly expanded since the floodplain was reconnected to the river in 2009. Overall this study demonstrates that restored wetlands can provide suitable habitat for water voles, and provides guidance on some of the factors which should be considered when designing floodplains for water vole conservation.     

The influence of American mink odour on the spatial distribution and behaviour of water voles

The perception and assessment of predation risk often cause changes in the activities of animals and induce behavioural responses that may in turn affect their movements and distribution. To simulate high predation risk in a midfield pond riparian habitat, we used fresh faeces from ranch American mink Neovison vison and recorded behavioural responses of water voles Arvicola amphibius. In areas where mink odour was deployed, the numbers of captured vole individuals and their trappability were significantly lower than in control areas. Several voles migrated from the zones with deployed mink faeces to the areas without faeces, thus proving that increased predation risk affects the distribution of individuals in a population. The response to mink odour was much more pronounced in females than in males; in areas with deployed mink faeces, not a single female was trapped. We conclude that although American mink is a non‐native, invasive predator, water voles respond to mink odour by reducing their activity and/or by avoiding places with higher predation risk.     

The role of colonization in the dynamics of patchy populations of a cyclic vole species

The crash phase of vole populations with cyclic dynamics regularly leads to vast areas of uninhabited habitats. Yet although the capacity for cyclic voles to re-colonize such empty space is likely to be large and predicted to have become evolved as a distinct life history trait, the processes of colonization and its effect on the spatio-temporal dynamics have been little studied. Here we report from an experiment with root voles (Microtus oeconomus) specifically targeted at quantifying the process of colonization of empty patches from distant source patches and its resultant effect on local vole deme size variation in a patchy landscape. Three experimental factors: habitat quality, predation risk and inter-patch distance were employed among 24 habitat patches in a 100 × 300-m experimental area. The first-born cohort in the spring efficiently colonized almost all empty patches irrespective of the degree of patch isolation and predation risk, but this was dependent on habitat quality. Just after the initial colonization wave the deme sizes in patches of the same quality were underdispersed relative to Poisson variance, indicating regulated (density-dependent) settlement. Towards the end of the breeding season local demographic processes acted to smooth out the initial post-colonization differences among source and colonization patches, and among patches of initially different quality. However, at this time demographic stochasticity had also given rise to a large (overdispersed) variation in deme sizes that may have contributed to an overshadowing of the effect of other factors. The results of this experiment confirmed our expectation that the space-filling capacity of voles is large. The costs associated with transience appeared to be so low, at least at the spatial scale considered in this experiment, that such costs are not likely to substantially constrain habitat selection and colonization in the increase phase of cyclic patchy populations.     

Landscape genetics highlights the role of bank vole metapopulation dynamics in the epidemiology of Puumala hantavirus

Rodent host dynamics and dispersal are thought to be critical for hantavirus epidemiology as they determine pathogen persistence and transmission within and between host populations. We used landscape genetics to investigate how the population dynamics of the bank vole Myodes glareolus, the host of Puumala hantavirus (PUUV), vary with forest fragmentation and influence PUUV epidemiology. We sampled vole populations within the Ardennes, a French PUUV endemic area. We inferred demographic features such as population size, isolation and migration with regard to landscape configuration. We next analysed the influence of M. glareolus population dynamics on PUUV spatial distribution. Our results revealed that the global metapopulation dynamics of bank voles were strongly shaped by landscape features, including suitable patch size and connectivity. Large effective size in forest might therefore contribute to the higher observed levels of PUUV prevalence. By contrast, populations from hedge networks highly suffered from genetic drift and appeared strongly isolated from all other populations. This might result in high probabilities of local extinction for both M. glareolus and PUUV. Besides, we detected signatures of asymmetric bank vole migration from forests to hedges. These movements were likely to sustain PUUV in fragmented landscapes. In conclusion, our study provided arguments in favour of source‐sink dynamics shaping PUUV persistence and spread in heterogeneous, Western European temperate landscapes. It illustrated the potential contribution of landscape genetics to the understanding of the epidemiological processes occurring at this local scale.     

Heterogeneous landscapes and the role of refuge on the population dynamics of a specialist predator and its prey

How, and where, a prey species survives predation by a specialist predator during low phases of population fluctuations or a cycle, and how the increase phase of prey population is initiated, are much-debated questions in population and theoretical ecology. The persistence of the prey species could be due mainly to habitats that act as refuges from predation and/or due to anti-predatory behaviour of individuals. We present models for the former conjecture in two (and three) habitat systems with a specialist predator and its favoured prey. The model is based on dispersal of prey between habitats with high reproductive output but high risk of predation, and less productive habitats with relatively low risk of predation. We illustrate the predictions of our model using parameters from one of the most intriguing vertebrate predator–prey systems, the multi-annual population cycles of boreal voles and their predators. We suggest that cyclic population dynamics could result from a sequence of extinction and re–colonization events. Field voles (Microtus agrestis), a key vole species in the system, can be hunted to extinction in their preferred meadow habitat, but persist in sub-optimal wet habitats where their main predator, the least weasel (Mustela nivalis nivalis) has a low hunting efficiency. Re–colonization of favourable habitats would occur after the predator population crashes. At the local scale, the model suggests that the periodicity and amplitude of population cycles can be strongly influenced by the relative availability of risky and safe habitats for the prey. Furthermore, factors like intra-guild predation may lead to reduced predation pressure on field voles in sub-optimal habitats, which would act as a refuge for voles during the low phase of their population cycles. Elasticity analysis suggested that our model is quite robust to changes in most parameters but sensitive to changes in the population dynamics of field voles in the optimal grassland habitat, and to the maximum predation rate of weasels.     

The combined effect of environmental factors and neighbouring populations on the distribution and abundance of Arvicola terrestris. An approach using rule-based models

We investigated how the interplay between environmental factors and presence of neighbouring populations determines the distribution and abundance of a small, endangered rodent, the water vole ( Arvicola terrestris ). We studied thriving and non-fragmented populations of water voles in the absence of their main predator, the introduced American mink ( Mustela vison ). A low degree of population fragmentation, such as the one characterizing the studied populations, was probably typical of water voles before their decline started. We found that under these conditions water voles' distribution is mainly determined by three environmental factors: presence of freshwater, adequate food, and cover. Variance in other factors is well tolerated by water voles. We obtained this result by the use of rule-based models in two separate areas. The two models correctly classified 81% and 83% of the observed cases, respectively. When optimised on one area and cross-validated on the other area the performance of the models was still high (73% and 79%) indicating that the models were robust and generalizable. We also found that the density of animals was lower in sub-optimal than in optimal habitat. We then tested the hypothesis that the number of neighbouring colonies determines the probability of finding voles in a given section. We found that the presence of nearby colonies was an important factor in determining the presence of water voles in sub-optimal habitat, while isolated patches of suitable habitat were less likely to host water voles. These observations suggest the possible presence of a source-sink dynamic, where an optimal habitat acts as a source for populating sub-optimal habitats that may be considered a sink habitat. These findings are discussed in the context of water vole conservation.     

Competition, predation and interspecific synchrony in cyclic small mammal communities

Although competition and predation are considered to be among the most important biotic processes influencing the distribution and abundance of species in space and time, the relative and interactive roles of these processes in communities comprised of cyclically fluctuating populations of small mammals are not well known. We examined these processes in and among populations of field voles, sibling voles, bank voles and common shrews in western Finland, using spatially replicated trapping data collected four times a year during two vole cycles (1987–1990 and 1997–1999). Populations of the four species exhibited relatively strong interspecific temporal synchrony in their multiannual fluctuations. During peak phases, we observed slight deviations from close temporal synchrony: field vole densities peaked at least two months earlier than those of either sibling voles or bank voles, while densities of common shrews peaked even earlier. The growth rates of all four coexisting small mammal species were best explained by their own current densities. The growth rate of bank vole populations was negatively related to increasing densities of field voles in the increase phase of the vole cycle. Apart from this, no negative effects of interspecific density, direct or delayed, were observed among the vole species. The growth rates of common shrew populations were negatively related to increasing total rodent (including water voles and harvest mice) densities in the peak phase of the vole cycle. Sibling voles appeared not to be competitively superior to field voles on a population level, as neither of these Microtus voles increased disproportionately in abundance as total rodent density increased. We suggest that interspecific competition among the vole species may occur, but only briefly, during the autumn of peak years, when the total available amount of rodent habitat becomes markedly reduced following agricultural practices. Our results nonetheless indicate that interspecific competition is not a strong determinant of the structure of communities comprised of species exhibiting cyclic dynamics. We suggest that external factors, namely predation and shortage of food, limit densities of vole populations below levels where interspecific competition occurs. Common shrews, however, appear to suffer from asymmetric space competition with rodents at peak densities of voles; this may be viewed as a synchronizing effect.     

Effects of landscape and patch-level attributes on regional population persistence

Species responses are influenced by processes operating at multiple scales, yet many conservation studies and management actions are focused on a single scale. Although landscape-level habitat conditions (i.e., habitat amount, fragmentation and landscape quality) are likely to drive the regional persistence of spatially structured populations, patch-level factors (i.e., patch size, isolation, and quality) may also be important. To determine the spatial scales at which habitat factors influence the regional persistence of endangered Ord's kangaroo rats (Dipodomys ordii) in Alberta, Canada, we simulated population dynamics under a range of habitat conditions. Using a spatially-explicit population model, we removed groups of habitat patches based on their characteristics and measured the resulting time to extinction. We used proportional hazards models to rank the influence of landscape and interacting patch-level variables. Landscape quality was the most influential variable followed by patch quality, with both outweighing landscape- and patch-level measures of habitat quantity and fragmentation/proximity. Although habitat conservation and restoration priorities for this population should be in maximizing the overall quality of the landscape, population persistence depends on how this goal is achieved. Patch quality exerted a significant influence on regional persistence, with the removal of low quality road margin patches (sinks) reducing the risk of regional extinction. Strategies for maximizing overall landscape quality that omit patch-level considerations may produce suboptimal or detrimental results for regional population persistence, particularly where complex local population dynamics (e.g., source-sink dynamics) exist. This study contributes to a growing body literature that suggests that the prediction of species responses and future conservation actions may best be assessed with a multi-scale approach that considers habitat quality and that the success of conservation actions may depend on assessing the influences of habitat factors at multiple scales.     

Is the population turnover of patchy‐distributed annuals determined by dormancy dynamics or dispersal processes?

In species with fragmented distribution, regional turnover dynamics is given by the processes of local population extinction and patch (re)colonization by migrants spreading from neighboring occupied patches. In plants with dormant stages (e.g. seeds) and limited dispersal capacity, regional dynamics based on dispersal processes can be overridden by pseudo-turnover determined by signals inducing or breaking dormancy (e.g. due to changes in habitat quality) resulting in a low importance of habitat configuration and size.
In this study, I investigated the turnover dynamics of 5 annual plant species growing on ant mounds of Lasius flavus over three years. I analyzed whether the grassland-scale dynamics of these annuals is influenced by dispersal processes, or alternatively, by pseudo-turnover of soil seed populations. For that purpose I 1) searched for populations formed from soil seeds only, 2) compared the relative contribution of the soil seed bank and seed rain for population restoration after disappearance from the vegetation and 3) investigated whether colonization and extinction events are affected by patch isolation. I assumed if population turnover was rather a result of the soil seed bank dynamics then spatial effects would be hard to detect.
In spite of the presence of populations formed from soil seed and the relatively more important soil seed bank for potential population reestablishment, turnover dynamics followed the predictions of metapopulation theory. Population appearance was more probable in larger and less isolated patches. Probability of disappearance increased with decrease of population size that was negatively influenced by the patch size and its isolation. These findings indicate dispersal processes to be important in the turnover dynamics and only limited contribution of soil seed populations. Their small effectiveness is probably related to the low chance of recurrent disturbance on the mound surface.     

生境破坏的模式对集合种群动态和续存的影响

构建了空间关联的集合种群模型,该模型不但包含了种群的空间结构信息,而且引入了破坏生境的全局密度和局部密度两个指标,它们描述了破坏生境的模式.模型揭示了破坏生境的空间分布格局复杂地影响了集合种群的动态和续存,破坏和未破坏生境斑块的均匀混合不利于集合种群的增长和续存,而生境类型聚集分布可以促进集合种群的快速增长和长期续存;对于两种斑块类型相对均匀混合的生境来说,均匀场假设可能会高估集合种群的续存,对于相对斑块类型高度聚集的生境,均匀场假设可能会低估集合种群的续存;物种的迁移范围也会影响集合种群的续存,迁移范围越大的物种越容易抵御生境的破坏而免遭灭绝.这意味着在生物保护中不能仅仅考虑生境的恢复和斑块质量的改善,生境结构的构建也是很重要的,加强生境斑块之间的连通性也有利于物种的长期续存.     

Voles on small islands: effects of food limitation and alien predation

Ecosystems of three trophic levels may be bottom-up (by food-plant availability) and/or top-down (by predators) limited. Top-down control might be of greater consequence when the predation impact comes from an alien predator. We conducted a replicated two-factor experiment with field voles (Microtus agrestis) during 2004-2005 on small islands of the outer archipelago of the Baltic Sea, south-west Finland, manipulating both predation impact by introduced American mink (Mustela vison) and winter food supply. In autumn 2004, we live-trapped voles on five islands from which mink had been consistently removed, and on four islands where mink were present, and provided half of these islands with 1.8 kg oats per vole. Body mass of female voles increased as a response to supplementary food, whereas both food supplementation and mink removal increased the body mass of male voles in subsequent spring. During winter, there was a positive effect of supplementary food, but in the subsequent summer, possible positive long-term impacts of food supplementation on field voles were not detected. Mink removal appeared not to affect density estimates of field voles during the winter and summer immediately after food addition. Trapping data from 2004 to 2005 and 2007 suggested, however, that in two out of three summers densities of voles were significantly higher in the absence than in the presence of mink. We conclude that vole populations on small islands in the archipelago of the Baltic Sea are mainly bottom-up limited during winter (outside the growing season of food plants), when food availability is low, and limited by mink predation during summer which slows population growth during the reproductive season of voles.     

Metapopulation dynamics: Does it help to have more of the same?

With the interest in conservation biology shifting towards processes from patterns, and to populations from communities, the theory of metapopulation dynamics is replacing the equilibrium theory of island biogeography as the population ecology paradigm in conservation biology. The simplest models of metapopulation dynamics make predictions about the effects of habitat fragmentation - size and isolation of habitat patches - on metapopulation persistence. The simple models may be enriched by considerations of the effects of demographic and environmental stochasticity on the size and extinction probability of local populations. Environmental stochasticity affects populations at two levels: it makes local extinctions more probable, and it also decreases metapopulation persistence time by increasing the correlation of extinction events across populations. Some controversy has arisen over the significance of correlated extinctions, and how they may affect the optimal subdivision of metapopulations to maximize their persistence time.     

Variability in primary productivity determines metapopulation dynamics

Temporal variability in primary productivity can change habitat quality for consumer species by affecting the energy levels available as food resources. However, it remains unclear how habitat-quality fluctuations may determine the dynamics of spatially structured populations, where the effects of habitat size, quality and isolation have been customarily assessed assuming static habitats. We present the first empirical evaluation on the effects of stochastic fluctuations in primary productivity—a major outcome of ecosystem functions—on the metapopulation dynamics of a primary consumer. A unique 13-year dataset from an herbivore rodent was used to test the hypothesis that inter-annual variations in primary productivity determine spatiotemporal habitat occupancy patterns and colonization and extinction processes. Inter-annual variability in productivity and in the growing season phenology significantly influenced habitat colonization patterns and occupancy dynamics. These effects lead to changes in connectivity to other potentially occupied habitat patches, which then feed back into occupancy dynamics. According to the results, the dynamics of primary productivity accounted for more than 50% of the variation in occupancy probability, depending on patch size and landscape configuration. Evidence connecting primary productivity dynamics and spatiotemporal population processes has broad implications for metapopulation persistence in fluctuating and changing environments.     

The fragmented population structure of the Sardinian chalk hill blue butterfly (Lepidoptera, Lycaenidae)

The endemic Sardinian chalk hill blue butterfly, Polyommatus coridon gennargenti, is considered vulnerable to extinction because of its low genetic variation and restricted distribution. The species also has a fragmented distribution, which follows the patchy distribution pattern of its larval host-plant. A preliminary investigation of the population structure of P. coridon gennargenti was carried out on a small network of four local populations by means of capture–recapture methods. Estimated population sizes and movement rates among the four adjacent local populations suggest that this taxon has a metapopulation structure composed of loosely connected small local populations. Natural fragmentation, isolation, and traditional land use contribute to the vulnerability of P. coridon gennargenti to extinction. Low effective population sizes and restricted movement between habitat patches lead to inbreeding and an increased vulnerability to extinction of this island population.     

Winter herbivory by voles during a population peak: the relative importance of local factors and landscape pattern

1. We studied the relative role of local habitat variables and landscape pattern on vole–plant interactions in a system with grey-sided voles ( Clethrionomys rufocanus (Sund.)) and their favourite winter food plant, bilberry ( Vaccinium myrtillus L.). The study was conducted during a vole peak year (1992–93) in a tundra area in northern Norway.
2. Using Mantel statistics we were able to separate the direct effects of the spatial patterning of habitats and the indirect effects due to spatial aggregations of similar habitats.
3. Results indicate that knowledge about the explicit spatial patterning of patches does not improve our understanding of the system. Instead, two local factors, vegetation height and bilberry biomass, explained more than 50% of the variation in cutting intensity in winter (defined as the proportion of above-ground shoots cut). Increasing vegetation height increased, and increasing bilberry biomass decreased, the cutting intensity.
4. The conclusion that grey-sided voles are able to distribute themselves relative to habitat quality was also partially supported by our estimated over-winter persistence by voles in the various habitats. Vole persistence was uncorrelated with vegetation height, the important predictor of autumn vole density, but tended to correlate with the deviation from the relation between vegetation height and autumn vole density. This conforms to the expectations from the theory of ideal-free habitat distribution.
5. The cue for vole habitat choice, i.e. vegetation height, indicates that either predation or freezing risk is important for voles when selecting over-wintering habitat.     

Fox predation on cyclic field vole populations in Britain

The diet of the red fox Vulpes vulpes L. was studied during three winter periods in spruce pklantations in Britain, during which time the cyclic field vole Microtus agrestis L. populations varied in abundance. Field voles and roe deer Capreolus capreolus L. were the two main prey species in the diet of the red fox. The contribution of lagomorphs to fox diet never exceeded 35% and species of small mammal other than field voles were of minor importance. The contribution of field voles was dependent on vole density. The non-linear density dependent relationship with a rather abrupt increase of field voles in fox did when vole density exceeded ca 100 voles ha⁻¹ was consistent with a prey-switching response. The contribution of field voles to fox diet during the low phase of population cycles was lower in Kielder Forest than in other ecosystems with cyclic vole populations. The number of foxes killed annually by forestry rangers was consistent with the evidence from other studies that foxes preying on cyclic small rodents might show a delayed numerical response to changes in vole abundance. Estimates of the maximum predation rate of the fox alone (200–290 voles ha⁻¹ of vole habitat year⁻¹) was well above a previously predicted value for the whole generalist predator community in Kielder Forest. Our data on the functional response of red foxes and estimates of their predation rates suggest that foxes should have a strong stabilising impact on vole populations, yet voles show characteristic 3-4 yr cycles.