Changes in population structure and reproduction during a 3-yr population cycle of voles

Cyclic changes in population growth rate are caused by changes in survival and/or reproductive rate. To find out whether cyclic changes in reproduction are an important part of the mechanism causing cyclic fluctuations in small mammal populations, we studied changes in the population structure and reproduction of field voles ( Microtus agrestis ), sibling voles ( M. rossiaemeridionalis ), bank voles ( Clethrionomys glareolus ), and common shrews ( Sorex araneus ) in western Finland during 1984–1992, in an area with 3-yr vole cycles. We also modelled the population growth of voles using parameter values from this study. The animals studied were collected by snap trapping in April, May, June, August, September, and, during 1986–1990, also in October. We found several phase-related differences in the population structure (age structure, sex ratio, proportion of mature individuals) and reproduction (litter size, length of the breeding season) of voles. In non-cyclic common shrews, the only significant phase-related difference was a lower proportion of overwintered individuals in the increase phase. According to the analyses and the vole model, phase-related changes in litter size had only a minor impact on population growth rate. The same was true for winter breeding in the increase phase. The length and intensity of the summer breeding season had an effect on yearly population growth but this impact was relatively weak compared to the effect of cyclic changes in survival. The population increase rates of Microtus were delayed dependent on density (8–12-month time lag). Our results indicate that cyclic changes in reproduction are not an important part of the mechanism driving cyclic fluctuations in vole populations. Low survival of young individuals appeared to play an important role in the shift from the peak to the decline phase in late summer and early autumn.     

Phase dependence in winter physiological condition of cyclic voles

Lack of food resources has been suggested as a factor which limits the growth of cyclic vole populations. During peak phases of the cycle, vole population growth typically ceases during late autumn or early winter, and is followed by a decrease in density over the winter. To investigate whether this decrease is due to increased mortality induced by a depletion of food resources, we studied overwinter food consumption and physiological condition of field voles ( Microtus agrestis ) in western Finland in both an increase and a decrease phase of a three-year population cycle. The growth rate of vole populations was negatively related both to prevailing vole densities and to densities six months earlier. The condition index of voles, as well as their blood levels of haematocrit, proteins, free fatty acids and immunoglobulin G, were positively related to population growth rate when populations were declining. When populations were increasing, these parameters tended to be negatively related to population growth rate. The overall physiological condition of voles was lower in the winter of the decrease phase as compared to the increase phase. The return rate of voles, a proxy of survival, was also lower in the decrease than in the increase phase of the cycle and positively related to haematocrit levels. Almost 90% of all green vegetation shoots were consumed by voles during the winter of the decrease phase while only two thirds were eaten in the increase phase. Our results suggest that the winter decrease phase of cyclic vole populations is associated with both a deterioration in the physiological condition of voles and a significant depletion of winter food resources. This implies that malnutrition induces poor physiological condition in voles, which in turn may increase mortality either directly through starvation or indirectly through increased susceptibility to predators and pathogens.     

Spatial synchrony in vole population fluctuations – a field experiment

Three mechanisms have been proposed to induce spatial synchrony in fluctuations of small mammal populations: climate‐related environmental effects, predation and dispersal. We conducted a field experiment in western Finland to evaluate the relative roles of these mechanisms in inducing spatial synchrony among cyclic populations of field voles Microtus agrestis. The study was conducted during the increase and peak phases of a vole population cycle on four agricultural field sites situated 1.5–7.0 km apart. Each field contained two 0.5‐ha fenced enclosures and one 1‐ha unfenced control area. One enclosure per field allowed access by small mustelid predators and the other by avian predators; all enclosures prevented the dispersal of voles. The unfenced control areas allowed access by all predators as well as dispersal by voles. Enclosed vole populations were in a treatment‐wise asynchronous phase before the predator access treatments were applied. The growth rates of all enclosed populations were tightly synchronized during the course of the experiment. Conversely, synchrony both among the unfenced populations and between the fenced and unfenced populations was practically non‐existent. During winter, in the increase phase of the cycle, vole populations in all treatments declined to low densities due to a seasonal effect of winter food depletion. During summer, in the peak year of the vole cycle, all populations fluctuated in synchrony. At this time, both small mustelids and birds of prey appeared to be abundant enough to induce synchrony. Dispersal was identified as a potential contributor to synchronization, but the magnitude of its effects could not be reliably discerned. Our results indicate that no single mechanism can account for the observed patterns of spatial synchrony among cyclic northern vole populations. Rather, spatial synchronization is induced by different mechanisms, namely seasonality and predation, acting successively during different seasons and phases of the vole cycle.     

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.     

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.     

Experimental tests of predation and food hypotheses for population cycles of voles

Pronounced population cycles are characteristic of many herbivorous small mammals in northern latitudes. Although delayed density-dependent effects of predation and food shortage are often proposed as factors driving population cycles, firm evidence for causality is rare because sufficiently replicated, large-scale field experiments are lacking. We conducted two experiments on Microtus voles in four large predator-proof enclosures and four unfenced control areas in western Finland. Predator exclusion induced rapid population growth and increased the peak abundance of voles over 20-fold until the enclosed populations crashed during the second winter due to food shortage. Thereafter, voles introduced to enclosures which had suffered heavy grazing increased to higher densities than voles in previously ungrazed control areas which were exposed to predators. We concluded that predation inhibits an increase in vole populations until predation pressure declines, thus maintaining the low phase of the cycle, but also that population cycles in voles are not primarily driven by plant-herbivore interactions.     

Migration and recovery of the genetic diversity during the increasing density phase in cyclic vole populations

In cyclic populations, high genetic diversity is currently reported despite the periodic low numbers experienced by the populations during the low phases. Here, we report spatio-temporal monitoring at a very fine scale of cyclic populations of the fossorial water vole (Arvicola terrestris) during the increasing density phase. This phase marks the transition from a patchy structure (demes) during low density to a continuous population in high density. We found that the genetic diversity was effectively high but also that it displayed a local increase within demes over the increasing phase. The genetic diversity remained relatively constant when considering all demes together. The increase in vole abundance was also correlated with a decrease of genetic differentiation among demes. Such results suggest that at the end of the low phase, demes are affected by genetic drift as the result of being small and geographically isolated. This leads to a loss of local genetic diversity and a spatial differentiation among demes. This situation is counterbalanced during the increasing phase by the spatial expansion of demes and the increase of the effective migration among differentiated demes. We provide evidences that in cyclic populations of the fossorial water voles, the relative influence of drift operating during low density populations and migration occurring principally while population size increases interacts closely to maintain high genetic diversity.     

Individual growth rates in natural field vole, Microtus agrestis, populations exhibiting cyclic population dynamics

Rodents that have multi-annual cycles of density are known to have flexible growth strategies, and the “Chitty effect”, whereby adults in the high-density phase of the cycle exhibit larger average body mass than during the low phase, is a well-documented feature of cyclic populations. Despite this, there have been no studies that have repeatedly monitored individual vole growth over time from all phases of a density cycle, in order to evaluate whether such variation in body size is due to differences in juvenile growth rates, differences in growth periods, or differential survival of particularly large or small voles. This study compares growth trajectories from voles during the peak, increase and crash phases of the cycle in order to evaluate whether voles are exhibiting fast or slow growth strategies. We found that although voles reach highest asymptotic weights in the peak phase and lowest asymptotes during the crash, initial growth rates were not significantly different. This suggests that voles attain larger body size during the peak phase as a result of growing for longer.     

Dynamic effects of predators on cyclic voles: field experimentation and model extrapolation

Mechanisms generating the well-known 3-5 year cyclic fluctuations in densities of northern small rodents (voles and lemmings) have remained an ecological puzzle for decades. The hypothesis that these fluctuations are caused by delayed density-dependent impacts of predators was tested by replicated field experimentation in western Finland. We reduced densities of all main mammalian and avian predators through a 3 year vole cycle and compared vole abundances between four reduction and four control areas (each 2.5-3 km(2)). The reduction of predator densities increased the autumn density of voles fourfold in the low phase, accelerated the increase twofold, increased the autumn density of voles twofold in the peak phase, and retarded the initiation of decline of the vole cycle. Extrapolating these experimental results to their expected long-term dynamic effects through a demographic model produces changes from regular multiannual cycles to annual fluctuations with declining densities of specialist predators. This supports the findings of the field experiment and is in agreement with the predation hypothesis. We conclude that predators may indeed generate the cyclic population fluctuations of voles observed in northern Europe.     

Age variation in a fluctuating population of the common vole

We analysed variation in age in a fluctuating population of the common vole (Microtus arvalis) in southern Moravia, Czech Republic, to test the assumption of the senescence hypothesis that the age of voles increases with increasing population density. Between 1996 and 1998, we monitored the demographic changes by snap-trapping and live-trapping in a field population passing through the increase, peak and decline phase of the population cycle. We used the eye lens mass method to determine the age of snap-trapped animals and those that died in live-traps. The average age of winter males was clearly higher after the peak phase breeding season than before it. No such phase-dependent shift in age, however, was observed in the female component. Male age continued to increase from autumn to spring over the pre-peak winter, and the highest age was in spring of the peak phase year. However, after the peak phase breeding season the highest age was achieved in winter, with the decline phase males during the next spring tending to be younger. The average age of females in spring populations was always lower than in winter populations. The average age of voles from live-traps was always higher than voles from snap-traps, particularly in winter and spring populations, suggesting the presence of senescent animals. Although the density-dependent changes in age are consistent with those observed for other voles, they provide only weak evidence that population cycles in the common vole are accompanied by pronounced shifts in individual age, particularly in female voles.Due to an error in the citation line, this revised PDF (published in December 2003) deviates from the printed version, and is the correct and authoritative version of the paper.     

Predator-induced changes in population structure and individual quality of Microtus voles: a large-scale field experiment

In small mammal populations with multiannual oscillations in density, observational data have revealed cyclic changes in population structure, reproduction, and individual quality, but mechanisms inducing these changes have remained an open question. We analysed data collected during a 3-year predator reduction experiment to find out the effects of predators on population structure, reproductive parameters, and individual quality of Microtus voles (the field vole M. agrestis and the sibling vole M. rossiaemeridionalis ) in western Finland. Voles were collected by snap trapping in April, June, August, and October during 1997–1999. The yearly reduction of predators from April to October had a clear positive effect on the abundance of sibling voles but did not significantly affect the densities of field voles. Predator reduction apparently also affected the age ratio and mean body size in late summer, as well as pancreatic weights of voles. However, all observed differences between predator reduction and control areas, except those in abundance, were small and may mainly reflect a generally higher survival leading to higher densities of voles in predator reduction areas. Our results also indicated a relative lack of high quality food at population peaks but not because of reduced foraging activity in the presence of predators. We conclude that the indirect effects of vole-eating predators on the population growth of main prey are small compared to the detrimental direct effects on prey survival. In the case of less preferred prey, indirect effects of predation through reduced interspecific competition may play a role at high densities.     

Experimental evidence that livestock grazing intensity affects cyclic vole population regulation processes

Grazing by domestic ungulates may limit the densities of small herbivorous mammals that act as key prey in ecosystems. Whether this also influences density dependence and the regulation of small herbivore populations, hence their propensity to exhibit multi-annual population cycles, is unknown. Here, we combine time series analysis with a large-scale grazing experiment on upland grasslands to examine the effects of livestock grazing intensity on the population dynamics of field voles (Microtus agrestis). Using log-linear modelling of replicated time series under different grazing treatments, we show that increased sheep densities weaken delayed density dependent regulation of vole population growth, hence reducing the cyclicity in vole population dynamics. While population regulation is commonly attributed to both top-down and bottom up processes, our results suggest that regulation of cyclic vole populations can be disrupted by the influence of another grazer in the same trophic level. These results support the view that ongoing changes in domestic grazing intensity, by affecting small mammal dynamics, can potentially have cascading impacts on higher trophic levels, and strongly influence the dynamics of upland grassland systems.     

Experimental tests of the role of predation in the population dynamics of voles and lemmings

• 1 Reasons for fluctuating populations of small mammals have been intensively investigated since the early days of modern ecology. Particular interest has been taken in vole populations exhibiting multiannual oscillations. Much empirical and theoretical work has been accomplished to find out the key factor(s) driving these population cycles and many reviews have been written about the results.
• 2 One of the most plausible processes for explaining regular fluctuations in small mammals is predation. Here I review the existing literature on the experimental studies of the role of predation in vole population dynamics in the hope that a critical examination of these studies will help researchers improve the design of future experiments.
• 3 Most predation manipulations have been done in exclosures, but there are also studies that have attempted to reduce or increase predator numbers in non‐fenced areas, islands and enclosures.
• 4 As the number of experimental studies has increased, their quality in terms of replication, use of controls and realistic spatial and temporal scales has also improved.
• 5 Most studies have found population‐level effects of predator manipulations on prey populations. The effects have varied from very weak to very strong, reflecting dissimilar experimental designs and the great variety of predator–prey interactions among different kinds of species in different landscapes. Most of these studies show that predation limits population growth of voles, and in some circumstances even regulate vole population fluctuations, but none of them clearly demonstrates that predation consistently changes fluctuation patterns of voles.
• 6 To be able to assess more reliably the true role of predation on (cyclic) population fluctuations of voles, more competent experiments are still needed not only over the geographical range of cyclic population dynamics, but also in areas of weakly or non‐cyclic populations of voles.

     

Are silica defences in grasses driving vole population cycles?

Understanding the factors that drive species population dynamics is fundamental to biology. Cyclic populations of microtine rodents have been the most intensively studied to date, yet there remains great uncertainty over the mechanisms determining the dynamics of most of these populations. For one such population, we present preliminary evidence for a novel mechanism by which herbivore-induced reductions in plant quality alter herbivore life-history parameters and subsequent population growth. We tested the effect of high silica levels on the population growth and individual performance of voles (Microtus agrestis) reared on their winter food plant (Deschampsia caespitosa). In sites where the vole population density was high, silica levels in D. caespitosa leaves collected several months later were also high and vole populations subsequently declined; in sites where the vole densities were low, levels of silica were low and population density increased. High silica levels in their food reduced vole body mass by 0.5% a day. We argue that silica-based defences in grasses may play a key role in driving vole population cycles.     

Predator–vole interactions in northern Europe: the role of small mustelids revised

The cyclic population dynamics of vole and predator communities is a key phenomenon in northern ecosystems, and it appears to be influenced by climate change. Reports of collapsing rodent cycles have attributed the changes to warmer winters, which weaken the interaction between voles and their specialist subnivean predators. Using population data collected throughout Finland during 1986–2011, we analyse the spatio-temporal variation in the interactions between populations of voles and specialist, generalist and avian predators, and investigate by simulations the roles of the different predators in the vole cycle. We test the hypothesis that vole population cyclicity is dependent on predator–prey interactions during winter. Our results support the importance of the small mustelids for the vole cycle. However, weakening specialist predation during winters, or an increase in generalist predation, was not associated with the loss of cyclicity. Strengthening of delayed density dependence coincided with strengthening small mustelid influence on the summer population growth rates of voles. In conclusion, a strong impact of small mustelids during summers appears highly influential to vole population dynamics, and deteriorating winter conditions are not a viable explanation for collapsing small mammal population cycles.     

Regulation of reproduction rate in a cyclic population of the red-backed vole,Clethrionomys rufocanus bedfordiae

Changes of the components of reproduction were analyzed quantitatively in a two-year cyclic population (which has two peaks in alternate years during a five-year census) of the red-backed vole, Clethrionomys rufocanus bedfordiae, with reference to its regulatory mechanism: (1) Variation in sex ratios was not associated with population phase or density, although a higher percentage of females in mature individuals was observed in the increase phase. (2) Females attained to sexual maturity at younger age and at lighter body weight than did males. All the youngest mature individuals were found in the low and the increase phases. Age and size at maturity became older and larger as the population went toward the peak phase. (3) Maturation rate was strongly associated with population phase and density; this component is an important and good parameter to predict population trend. Maturation rates were in the order, the low phase>the increase phase>the peak phase>the decline phase; the differences in the rates among these phases were significant. Maturation rate was somewhat depressed when the population density exceeded about 40 individuals/ha. Changes in age at maturity and in maturation rate are interpreted as derivative phenomena related to the population density and the capacity of the number of mature voles per unit area. (4) The maximum number of mature individuals were 26 males/ha and 29 females/ha; there was almost no increase of the number of mature voles at higher population densities over about 40 individuals/ha. The number of exclusive home ranges per hectare calculated from the observed range lengths did not differ much from the maximum number of mature voles of either sex. (5) Length of breeding period was shorter in the high-density years than in the low-density years; the breeding started earlier and ended earlier in the former than that in the latter. In the increase phase a few voles reproduced in winter. (6) The percentage of pregnant females was significantly lower in the peak phase than those in the other phases.     

Survival of cohorts in a fluctuating population of the vole Microtus townsendii

Survival patterns of cohorts are described during a population cycle of the vole Microtus townsendii near Vancouver, British Columbia, Canada. A two–year live–trapping study on both enclosed and unfenced populations showed that cohorts during the increase phase of growth lived longest and had the best survival. Smaller voles in the peak density spring cohort had poor survival, but survival increased during the peak density summer. Survival of cohorts in the decline phase breeding season was very poor. The suggestions are made that changes in spacing behaviour may cause changes in cohort survival and that the causes of rapid changes in survival need to be determined.     

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.     

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.     

Experimental demonstration of the antiherbivore effects of silica in grasses: impacts on foliage digestibility and vole growth rates

The impact of plant-based factors on the population dynamics of mammalian herbivores has been the subject of much debate in ecology, but the role of antiherbivore defences in grasses has received relatively little attention. Silica has been proposed as the primary defence in grasses and is thought to lead to increased abrasiveness of foliage so deterring feeding, as well as reducing foliage digestibility and herbivore performance. However, at present there is little direct experimental evidence to support these ideas. In this study, we tested the effects of manipulating silica levels on the abrasiveness of grasses and on the feeding preference and growth performance of field voles, specialist grass-feeding herbivores. Elevated silica levels did increase the abrasiveness of grasses and deterred feeding by voles. We also demonstrated, for the first time, that silica reduced the growth rates of both juvenile and mature female voles by reducing the nitrogen they could absorb from the foliage. Furthermore, we found that vole feeding leads to increased levels of silica in leaves, suggesting a dynamic feedback between grasses and their herbivores. We propose that silica induction due to vole grazing reduces vole performance and hence could contribute to cyclic dynamics in vole populations.