Spatio-temporal patterns of habitat use in voles and shrews modified by density, season and predators

1.?Although the intrinsic habitat preferences of a species can be considered to be fixed, the realized habitat use depends on the prevailing abiotic and biotic conditions. Often the core habitats are occupied by dense and stable populations, while marginal habitats become occupied only at times of high density. In a community of interacting species, habitat uses of different species become inter-related, for example an increased density of a strong competitor forcing a weaker competitor to use more marginal habitats. 2.?We studied the spatio-temporal distribution patterns of three common small mammal species, the bank vole Myodes glareolus; the field vole Microtus agrestis; and the common shrew Sorex araneus, in a 4-year trapping study carried out on six large islands, each containing a mixture of three main habitat types (forest, field and clear-cut). We experimentally released least weasels (Mustela n. nivalis) to some of the islands to see how the focal species respond to increased predation pressure. 3.?Both vole species were largely restricted to their core habitats (bank voles to forests and field voles to fields) at times of low population density. With increasing density, the relative habitat use of both species increased in the clear-cut areas. The common shrew was a generalist in its habitat use at all population densities. 4.?The release of the weasels changed the habitat use of all study species. 5.?The vole species showed a stronger aggregated pattern than the common shrew, especially at low population density. The vole aggregations remained in the same localities between seasons, except in the case of bank voles after the weasels were released. 6.?Bank voles and field voles avoided each other at high density. 7.?We conclude that intrinsically differential habitat requirements and flexibility to modify habitat use facilitate the coexistence of the two competing vole species in mosaic landscapes consisting of boreal forests and open habitats.     

Effects of competition and season on survival and maturation of young bank vole females

In territorial microtines intra-specific density dependent processes can limit the maturation of individuals during the summer of their birth. This may have demographic consequences by affecting the number and the age distribution of breeding individuals in the population. Little is known about this process on a community level, though populations of many northern microtine species fluctuate in synchrony and are known to interfere socially with each other. We experimentally studied the influence of the field vole Microtus agrestis on maturation, breeding, space use and survival of weanling bank voles, Clethrionomys glareolus. Two additive competition experiments on bank vole populations were conducted in large outdoor enclosures, half of them additionally housing a field vole population. In a mid-summer experiment low population density and absence of older breeding females minimised intra-specific competition. Survival was not affected by the presence of field voles. Season had a significant effect on both the probability of maturation and breeding of the weanlings. Competition with field voles significantly delayed breeding, and coupled with seasonal effects decreased the probability of breeding. In a late-summer experiment breeding and survival of bank vole weanlings were studied for three weeks as part of a high density breeding bank vole population. Weanlings did not mature at all nor were their space use and survival affected by the presence of field voles. Our results show that competition with other species can also have an impact on breeding of immatures. In an extreme seasonal environment, even a short delay of breeding may decrease survival chances of offspring. Seasonal and competition effects together may thus limit the contribution of year born females to reproductive output of the population. Other studies have shown that adult breeding bank voles suffer lower survival in the presence of field voles, but this study showed no survival effects on the weanlings. Thus it might be beneficial for weanlings to stay immature especially in the end of the breeding season and postpone reproduction to the next breeding season if densities of competing species are high.     

Sheep grazing and rodent populations: evidence of negative interactions from a landscape scale experiment

Inter-specific competition, facilitation and predation influence herbivore assemblages, but no study has experimentally explored the interactions between large ungulates and small rodents. In a fully replicated, landscape scale experiment, we manipulated densities of domestic sheep in mountain pastures in Norway. We then determined population growth and densities of rodents by live trapping in each of the areas with different sheep densities. We found that the (summer) population growth rate and autumn density of the field vole (Microtus agrestis) was lower at high sheep density. This provides the first experimental evidence of negative interactions between an ungulate and small rodent species. There was no effect on the bank vole (Clethrionomys glareolus), whose diet differs from sheep. Sheep density, therefore, potentially alters the pattern of inter-specific population synchrony amongst voles. Our study shows that negative interactions between large ungulates and small rodents may be species-specific and negative population consequences for the rodent population appear above threshold ungulate densities.Electronic supplementary material is available for this article at     

Spatiotemporal dynamics of Puumala hantavirus in suburban reservoir rodent populations

The transmission of pathogens to susceptible hosts is dependent on the vector population dynamics. In Europe, bank voles (Myodes glareolus) carry Puumala hantavirus, which causes nephropathia epidemica (NE) in humans. Fluctuations in bank vole populations and epidemics in humans are correlated but the main factors influencing this relationship remain unclear. In Belgium, more NE cases are reported in spring than in autumn. There is also a higher incidence of human infections during years of large vole populations. This study aimed to better understand the link between virus prevalence in the vector, vole demography, habitat quality, and human infections. Three rodent populations in different habitats bordering Brussels city, Belgium, were studied for two years. The seroprevalence in voles was influenced first by season (higher in spring), then by vole density, vole weight (a proxy for age), and capture site but not by year or sex. Moreover, voles with large maximal distance between two captures had a high probability for Puumala seropositivity. Additionally, the local vole density showed similar temporal variations as the number of NE cases in Belgium. These results showed that, while season was the main factor influencing vole seroprevalence, it was not sufficient to explain human risks. Indeed, vole density and weight, as well as the local habitat, were essential to understanding the interactions in these host‐pathogen dynamics. This can, in turn, be of importance for assessing the human risks.     

Environmental change and disease dynamics: effects of intensive forest management on Puumala hantavirus infection in boreal bank vole populations

Intensive management of Fennoscandian forests has led to a mosaic of woodlands in different stages of maturity. The main rodent host of the zoonotic Puumala hantavirus (PUUV) is the bank vole (Myodes glareolus), a species that can be found in all woodlands and especially mature forests. We investigated the influence of forest age structure on PUUV infection dynamics in bank voles. Over four years, we trapped small mammals twice a year in a forest network of different succession stages in Northern Finland. Our study sites represented four forest age classes from young (4 to 30 years) to mature (over 100 years) forests. We show that PUUV-infected bank voles occurred commonly in all forest age classes, but peaked in mature forests. The probability of an individual bank vole to be PUUV infected was positively related to concurrent host population density. However, when population density was controlled for, a relatively higher infection rate was observed in voles trapped in younger forests. Furthermore, we found evidence of a "dilution effect" in that the infection probability was negatively associated with the simultaneous density of other small mammals during the breeding season. Our results suggest that younger forests created by intensive management can reduce hantaviral load in the environment, but PUUV is common in woodlands of all ages. As such, the Fennoscandian forest landscape represents a significant reservoir and source of hantaviral infection in humans.     

Maintenance of genetic diversity in cyclic populations-a longitudinal analysis in Myodes glareolus

Conspicuous cyclic changes in population density characterize many populations of small northern rodents. The extreme crashes in individual number are expected to reduce the amount of genetic variation within a population during the crash phases of the population cycle. By long-term monitoring of a bank vole (Myodes glareolus) population, we show that despite the substantial and repetitive crashes in the population size, high heterozygosity is maintained throughout the population cycle. The striking population density fluctuation in fact only slightly reduced the allelic richness of the population during the crash phases. Effective population sizes of vole populations remained also relatively high even during the crash phases. We further evaluated potential mechanisms contributing to the genetic diversity of the population and found that the peak phases are characterized by both a change in spatial pattern of individuals and a rapid accession of new alleles probably due to migration. We propose that these events act together in maintaining the high genetic diversity within cyclical populations.     

Interactive effects of past and present environments on overwintering success-a reciprocal transplant experiment

Life-history traits are influenced by environmental factors throughout the lifespan of an individual. The relative importance of past versus present environment on individual fitness, therefore, is a relevant question in populations that face the challenge of temporally varying environment. We studied the interacting effects of past and present density on body mass, condition, and survival in enclosure populations of the bank vole (Myodes glareolus) using a reciprocal transplant design. In connection with the cyclic dynamics of natural vole populations, our hypothesis was that individuals born in low-density enclosures would do better overwintering in low-density enclosures than in high-density enclosures and vice versa. Our results show that the effect of summer (past) density was strong especially on survival and body mass. The response of body mass to summer density was negative in both winter (present) density groups, whereas the response of survival probability was nonlinear and differed between the winter density groups. In particular, our data show a trend for higher overwintering success of individuals originating from the lowest summer densities in low winter density and vice versa. We therefore conclude that the capacity of individuals to respond to a change in density was constrained by the delayed density-dependent effects of environment experienced in the past. These effects have the potential to contribute to vole population dynamics. Possible mechanisms mediating the effects of past environment into present performance include both intrinsic and environmental factors.     

Does personality in small rodents vary depending on population density?

Personality means an individual's unique way of behaving and reacting to the environment. It is a stable and heritable trait, which is expressed consistently in different situations. The aim of our study was to develop novel tests to depict the personality structure of the bank vole Myodes glareolus, and to determine if the phase of the population cycle, i.e. population density, affects personality. We focused on some central aspects of bank vole behaviour: mobility, risk taking, exploratory behaviour, dominance, and aggressive behaviour towards pups. These behaviours were chosen because they directly affect bank vole survival or fitness or are classified as important factors of personality in other species. In total, 192 males from different populations went through four behavioural tests, in which 20 variables were measured. The tests were repeated after 3 weeks, which verified that all traits were stable, i.e. repeatable between trials. Three personality compounds emerged, named extroversion, novelty seeking and infanticide. Extroversion included dominance and mobility, while novelty seeking consisted of risk taking and exploration. Infanticide encompassed all indices measuring harmful behaviour towards pups. Mobility and dominance were connected, possibly because both seem to depend on condition. Time spent in captivity increased extroversion, which may be explained by good food, stable conditions and acclimation to strong social cues. Novelty seeking was connected to repeatability which could mean that novelty avoiding individuals adjust their behaviour to match new environments. Population density affected the infanticide trait but not novelty seeking or extroversion.     

Infanticide and Population Growth in the Bank Vole (Myodes glareolus): The Effect of Male Turnover and Density

One major intrinsic factor affecting recruitment of young into a population is infanticide, the killing of conspecific young by adult males. It occurs in most mammal species, like our study species the bank vole (Myodes glareolus), and is widely accepted as an adaptive behavior, which may increase male fitness via nutritional gain, decreased competition, or an increased access to mates. A turnover of males in a population increases the risk of infanticide owing to a disruption of social structures. In a controlled field study, we tested the effects of total male turnover and density on juvenile recruitment and female space use in experimental bank vole populations. Juvenile recruitment declined significantly in low‐density populations with male turnover, while growth of high‐density populations seemed unaffected. The females’ spatial behavior seemed unaffected by both male turnover and density. Our results suggest that male infanticide may considerably affect population growth and it is more likely to do so at lower densities.     

Regulation of vole populations by the nematode <Emphasis Type="Italic">Trichuris arvicolae</Emphasis>: insights from modelling

The goal of this study is to determine whether a parasitic nematode may regulate, or destabilise by inducing demographic cycles, its host populations. We explore three host–parasite systems through population dynamic models. The hosts considered are the fossorial water vole, Arvicola terrestris, the common vole Microtus arvalis and the bank vole Myodes (Clethrionomys) glareolus and the parasitic nematode is Trichuris arvicolae. Three differential equation-based mathematical models are developed including host immunity and the existence of trade-off between immunity and host survival. Using parameters estimated from field data and laboratory observations, all these models show that T. arvicolae can induce host population regulation but not demographic cycles. The regulation effect of the nematode is un-ambiguous for the water vole (reduction of 50.2% of the host population size), but less obvious for the common vole (5.9%) and even less for the bank vole (1.4%). Important biological parameters to be taken into account in such models are discussed. Experimental confirmation of the regulatory potential of the nematode and of the costs of mounting an immune response against this nematode are now required. Communicated by W. Lutz     

Spatial Variability of Resident and Nonresident Populations of Small Mammals on a Forest Plot

Biology Bulletin - Abstract—The resident population density and the numbers of nonresident common shrew (Sorex araneus), Laxmann’s shrew (S. caecutiens), and the bank vole...     

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

Indirect interaction between two competing species via a shared predator may be an important determinant of population and community dynamics. We studied the effect 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 effect 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 affected by weasel presence. The time spent in the risky and less risky area did not differ 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 affected 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-specific responses dominated. Besides a stronger escape response in the bank vole, the strongest individual differences were sex specific, i.e. males were more prone to take risks in space use and activity.     

Strong “bottom‐up” influences on small mammal populations: State‐space model analyses from long‐term studies

“Bottom‐up” influences, that is, masting, plus population density and climate, commonly influence woodland rodent demography. However, “top‐down” influences (predation) also intervene. Here, we assess the impacts of masting, climate, and density on rodent populations placed in the context of what is known about “top‐down” influences. To explain between‐year variations in bank vole Myodes glareolus and wood mouse Apodemus sylvaticus population demography, we applied a state‐space model to 33 years of catch‐mark‐release live‐trapping, winter temperature, and precise mast‐collection data. Experimental mast additions aided interpretation. Rodent numbers in European ash Fraxinus excelsior woodland were estimated (May/June, November/December). December–March mean minimum daily temperature represented winter severity. Total marked adult mice/voles (and juveniles in May/June) provided density indices validated against a model‐generated population estimate; this allowed estimation of the structure of a time‐series model and the demographic impacts of the climatic/biological variables. During two winters of insignificant fruit‐fall, 6.79 g/m² sterilized ash seed (as fruit) was distributed over an equivalent woodland similarly live‐trapped. September–March fruit‐fall strongly increased bank vole spring reproductive rate and winter and summer population growth rates; colder winters weakly reduced winter population growth. September–March fruit‐fall and warmer winters marginally increased wood mouse spring reproductive rate and September–December fruit‐fall weakly elevated summer population growth. Density dependence significantly reduced both species' population growth. Fruit‐fall impacts on demography still appeared after a year. Experimental ash fruit addition confirmed its positive influence on bank vole winter population growth with probable moderation by colder temperatures. The models show the strong impact of masting as a “bottom‐up” influence on rodent demography, emphasizing independent masting and weather influences; delayed effects of masting; and the importance of density dependence and its interaction with masting. We conclude that these rodents show strong “bottom‐up” and density‐dependent influences on demography moderated by winter temperature. “Top‐down” influences appear weak and need further investigation.     

Moose recruitment in relation to bilberry production and bank vole numbers along a summer temperature gradient in Norway

The plant stress hypothesis states that plant stress factors other than herbivory improve herbivore performance due to changes in the content of nutritive or defensive compounds in the plants. In Norway, the bilberry (Vaccinium myrtillus) is important forage for the bank vole (Myodes glareolus) in winter and for the moose (Alces alces) in summer and autumn. The observed peaks in bank vole numbers after years with high production of bilberries are suggested to be caused by increased winter survival of bank voles due to improved forage quality. High production of bilberries should also lead to higher recruitment rates in moose in the following year. We predict, however, that there is an increasing tendency for a 1-year delay of moose indices relative to vole indices with decreasing summer temperatures, because low temperatures prolong the period needed by plants to recover in the vole peak year, and thus positively affect moose reproduction also in the succeeding year. In eight out of nine counties in south-eastern Norway, there was a positive relationship between the number of calves observed per female moose during hunting and a bilberry seed production index or an autumn bank vole population index. When dividing the study area into regions, there was a negative relationship between a moose-vole time-lag index and the mean summer temperature of the region. These patterns suggest that annual fluctuations in the production of bilberries affect forage quality, but that the effect on moose reproduction also depends on summer temperatures.     

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.     

Density-dependent variation in body mass of voles

We studied inter-annual, spatial and sexual variation in the body mass of bank volesMyodes glareolus Schreber, 1780 and grey-sided volesMyodes rufocanus Sundevall, 1846 using live trappings from two grids on the southand north-facing slopes of a mountain valley in Southern Norway. Variation in spring density of the four populations was consistent with cyclic dynamics (n=7,s-values >0.5). Individuals caught on the south-facing slope were larger than those caught on the north-facing slope. Reproductively mature bank vole males were smaller than females, whereas reproductively mature grey-sided vole males were larger than females. Body mass was related to density in both species. In bank voles, we found a direct positive density dependence caused by a higher rate of survival at higher densities resulting from individual allocation of resources from reproduction to survival and growth. In grey-sided voles, we found a negative delayed density dependence resulting from grazing on preferred plants that determined the resource available for individual vole growth the following year.     

Population‐level manipulations of field vole densities induce subsequent changes in plant quality but no impacts on vole demography

Grazing‐induced changes in plant quality have been suggested to drive the negative delayed density dependence exhibited by many herbivore species, but little field evidence exists to support this hypothesis. We tested a key premise of the hypothesis that reciprocal feedback between vole grazing pressure and the induction of anti‐herbivore silicon defenses in grasses drives observed population cycles in a large‐scale field experiment in northern England. We repeatedly reduced population densities of field voles (Microtus agrestis) on replicated 1‐ha grassland plots at Kielder Forest, northern England, over a period of 1 year. Subsequently, we tested for the impact of past density on vole life history traits in spring, and whether these effects were driven by induced silicon defenses in the voles’ major over‐winter food, the grass Deschampsia caespitosa. After several months of density manipulation, leaf silicon concentrations diverged and averaged 22% lower on sites where vole density had been reduced, but this difference did not persist beyond the period of the density manipulations. There were no significant effects of our density manipulations on vole body mass, spring population growth rate, or mean date for the onset of spring reproduction the following year. These findings show that grazing by field voles does induce increased silicon defenses in grasses at a landscape scale. However, at the vole densities encountered, levels of plant damage appear to be below those needed to induce changes in silicon levels large and persistent enough to affect vole performance, confirming the threshold effects we have previously observed in laboratory‐based studies. Our findings do not support the plant quality hypothesis for observed vole population cycles in northern England, at least over the range of vole densities that now prevail here.     

Reproductive investment under fluctuating predation risk: Microtine rodents and small mustelids

Summary We studied the reproductive investment of microtine rodents (bank vole (Clethrionomys glareolus),Microtus epiroticus andMicrotus agrestis) in western Finland under predation risk from small mustelids. During 1984–1992, the yearly mean litter size of overwintered bank voles was smaller at high least weasel and stoat densities than at low densities (close to 3 versus 4–5). In addition, the annual mean litter size of young bank voles was negatively correlated to the least weasel density. In youngM. agrestis voles, the yearly late summer litter size was negatively associated with the autumn density of small mustelids. In the crash phase of the vole cycle (1989 and 1992), we removed small mustelids (mainly least weasels) from four unfenced areas in late April to late May and studied the reproduction of voles in four removal and comparable control areas (each 2–4 km²). Reduction of small mustelids significantly increased the proportion of pregnant bank vole females, but not that of pregnantMicrotus vole females. We conclude that predation risk apparently reduced reproductive investment of free-living bank vole females; these voles appear to trade their current parental investment against future survival and reproductive prospects. Accordingly, the presence of small mustelids (or their scent) may slow down the reproductive rate of voles. As antipredatory behaviours occurred on a large scale, our results add evidence to the hypothesis that crashes in multiannual vole cycles are driven by small mustelid predators.     

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.     

Impact of climate change on population dynamics of forest voles (<Emphasis Type="Italic">Myodes</Emphasis>) in northern Pre-Urals: The role of landscape effects

In recent years in northern Pre-Urals, the population dynamics of forest voles has undergone significant changes. In the foothill area, the abundance of the red-backed vole has decreased and that of the bank vole has increased significantly. As a result, the latter becomes the dominant species. In nearby lowland areas, the population of the bank vole has remained stable while the red-backed vole has increased. The main cause of these changes is the transformation of the environment under the influence of global climate change. This affects mainly foothill conifer forests and, to a lesser extent, lowland forests. As a consequence, responses of various vole species to these changes in different landscape areas are not identical.