Responses of stoats and least weasels to fluctuating food abundances: is the low phase of the vole cycle due to mustelid predation?

Summary We studied responses of stoats and least weasels to fluctuating vole abundances during seven winters in western Finland. Density indices of mustelids were derived from snow-tracking, diet composition from scat samples, and vole abundances from snap-trapping. Predation rate was estimated by the ratio of voles to mustelids and by the vole kill rate by predators (density of predator x percentage of voles in the diet). We tested the following four predictions of the hypothesis that small mustelids cause the low phase of the microtine cycle. (1) The densities of predators should lag well behind the prey abundances, as time lags tend to have destabilizing effects. The densities of stoats fluctuated in accordance with the vole abundances, whereas the spring densities of least weasels tracked the vole abundances with a half-year lag and the autumn densities with a 1-year lag. (2) Predators should not shift to alternative prey with declining vole densities. The yearly proportion of Microtus voles (the staple prey) in the diet of stoats varied widely (range 16–82%) and was positively correlated with the winter abundance of these voles. In contrast, the same proportion in the food of least weasels was independent of the vole abundance. (3) The ratio of voles to small mustelids should be smallest in poor vole years and largest in good ones. This was also observed. (4) Vole densities from autumn to spring should decrease more in those winters when vole kill rates are high than when they are low. The data on least weasels agreed with this prediction. Our results from least weasels were consistent with the predictions of the hypothesis, but stoats behaved like semi-generalist predators. Accordingly, declines and lows in the microtine cycle may be due to least weasel predation, but other extrinsic factors may also contribute to crashes.     

Numerical response of small mustelids to vole abundance: delayed or not?

One of the most studied problems in population ecology has been to understand the relative roles of top–down and bottom–up forces in regulating animal populations. This has also been a key issue in studies of vole population dyna mics. Vole populations exhibit a wide variation of dynamics, from seasonal fluctuations to multiannual variations or cyclicity. One of the hypotheses to explain cyclic population dynamics is predation by the specialist predators. A common counterargument against the predation hypothesis has been the lack of conclusive observations of the time delay in the predators’ numerical response. We studied the interaction between voles and their specialist small mustelid predators, the stoat Mustela erminea and the least weasel Mustela n. nivalis, by modelling their interaction to data sets that cover large areas of Finland. Vole abundance was monitored with biannual trappings and their predators with snow‐tracking. Results show a high dependence of the predators on the voles, and this connection is generally tighter in weasels than in stoats. Weasel abundance is affected most strongly by the vole abundance in previous spring, 8.5– 10 months earlier, while in stoats the effect of autumn abundance of voles, 2.5–6 months earlier, was the strongest. These results, together with the observation that the weasels’ effects on voles are stronger after a time lag of 6–9.5 than 2–4.5 months, indicate the existence of a time lag in weasels’ numerical response. A time lag in the predators’ numerical response is a necessary condition for the predators to drive population cycles in its prey, and therefore our results support the specialist predation hypothesis.     

The role of food supply in the dispersal behaviour of juvenile Tawny Owls Strix aluco

We investigated the effects of food supply on decisions made by dispersing juvenile Tawny Owls Strix aluco in Kielder Forest, Northumberland, in 1996 and 1997. Field Voles Microtus agrestis were the main food of the owls and clear-cuts the main habitat for voles. A vole sign index was used to estimate vole abundance. In areas near to roosting owls, mean vole densities were 83 and 115 ha⁻¹ in 1996 and 1997, respectively. The prediction that birds would perform area-restricted searches when prey was more abundant was not confirmed. Moreover, we found no evidence that juveniles avoided conspecifics. Owls appeared to have an imperfect knowledge of the environment as they responded to variability in Field Vole densities by altering the time spent in different areas rather than by moving to areas with successively greater vole densities. Vole abundance explained 25.7% of the variation in the time spent in different areas. Movements did not decrease with time after dispersal, although the detection of such movements was prone to error. This study supports recent work suggesting that although dispersal may be initiated by a variety of proximate and ultimate factors, individual decisions made during dispersal may depend partly on environmental conditions encountered during the process itself.     

Field Vole Microtus agrestis abundance and Hen Harrier Circus cyaneus diet and breeding in Scotland

In many parts of the global range, voles form an important part of the diet of Hen Harriers Circus cyaneus , and breeding numbers are correlated with the abundance of these small mammals. In Scotland, however, little information is available on harrier diet in the spring and our understanding of causes of variation in harrier breeding density is complicated by human interference. In this paper we explore the relationship between Field Vole Microtus agrestis abundance and harrier spring diet, density and productivity in southern Scotland. Over three years, voles occurred on average in 67% of pellets, and 79% in years of high and intermediate vole abundance. From 1992, the number of breeding harriers increased following protection from illegal persecution. After accounting for this trend, harrier numbers correlated strongly with vole abundance. Harrier clutch size was also correlated with vole abundance. Although fledging success tended to be greater in years of vole increase than in years of vole decline, fledging success was not significantly correlated with the relative abundance of voles, or with the abundance of Meadow Pipits or Red Grouse chicks.     

Numerical and functional responses of Common Buzzards Buteo buteo to prey abundance on a Scottish grouse moor

Predators will often respond to reductions in preferred prey by switching to alternative prey resources. However, this may not apply to all alternative prey groups in patchy landscapes. We investigated the demographic and aggregative numerical and functional responses of Common Buzzards Buteo buteo in relation to variations in prey abundance on a moor managed for Red Grouse Lagopus lagopus scotica in south‐west Scotland over three consecutive breeding and non‐breeding seasons. We predicted that predation of Red Grouse by Buzzards would increase when abundance of their preferred Field Vole Microtus agrestis prey declined. As vole abundance fluctuated, Buzzards responded functionally by eating voles in relation to their abundance, but they did not respond demographically in terms of either breeding success or density. During a vole crash year, Buzzards selected a wider range of prey typical of enclosed farmland habitats found on the moorland edge but fewer Grouse from the heather moorland. During a vole peak year, prey remains suggested a linear relationship between Grouse density and the number of Grouse eaten (a Type 1 functional response), which was not evident in either intermediate or vole crash years. Buzzard foraging intensity varied between years as vole abundance fluctuated, and foraging intensity declined with increasing heather cover. Our findings did not support the prediction that predation of Red Grouse would increase when vole abundance was low. Instead, they suggest that Buzzards predated Grouse incidentally while hunting for voles, which may increase when vole abundances are high through promoting foraging in heather moorland habitats where Grouse are more numerous. Our results suggest that declines in their main prey may not result in increased predation of all alternative prey groups when predators inhabit patchy landscapes. We suggest that when investigating predator diet and impacts on prey, knowledge of all resources and habitats that are available to predators is important.     

Tawny owl prey remains indicate differences in the dynamics of coastal and inland vole populations in southern Finland

Some studies suggest that mild winters decrease overwinter survival of small mammals or coincide with decreased cyclicity in vole numbers, whereas other studies suggest non-significant or positive relationships between mild winter conditions and vole population dynamics. We expect for the number of voles to be higher in the rich and low-lying habitats of the coastal areas than in the less fertile areas inland. We assume that this geographical difference in vole abundances is diminished by mild winters especially in low-lying habitats. We examine these relationships by generalized linear mixed models using prey remains of breeding tawny owls Strix aluco as a proxy for the abundance of voles. The higher number of small voles in the coastal area than in the inland area suggest that vole populations were denser in the coastal area. Vole populations of both areas were affected by winter weather conditions particularly in March, but these relationships differed between areas. The mild ends of winter with frequent fluctuations of the ambient temperature around the freezing point (“frost seesaw”) constrained significantly the coastal vole populations, while deep snow cover, in general after hard winters, was followed by significantly lowered number of voles only in the inland populations. Our results suggest that coastal vole populations are more vulnerable to mild winters than inland ones. We also show that tawny owl prey remains can be used in a meaningful way to study vole population dynamics.     

Species‐specific limitation of vole population growth by least weasel predation: facilitation of coexistence?

Interspecific competition is usually understood as different species competing directly with each other for limited resources. However, predators can alter such competitive interactions substantially. Predation can promote the coexistence of species in a situation where it would otherwise be impossible, for example if a tradeoff between the competitive abilities and predation resistance of the prey species exists. The field vole Microtus agrestis and the sibling vole M. rossiaemeridionalis are sympatric grassland species, which compete for the same resources. At the population level sibling voles are suggested to be superior competitors to field voles, yet more vulnerable to predation. We tested the effects of predation on the two species in 0.5 ha outdoor enclosures by exposing vole populations to radio-collared freely-hunting least weasels Mustela nivalis nivalis for three weeks. Lethal and non-lethal impacts of predation limited population densities of both species during and after the experimental period, but the effect was more pronounced in sibling voles in which population densities decreased markedly during the treatment period and even after that. Field vole population densities remained stable under weasel predation, while densities increased in controls. Survival in both species was lower in treatment populations compared to controls, but the effect tended to be more pronounced in sibling voles and in females of both species. The average mass of adults in both species declined in the treatment populations. These results suggest that predation by least weasels can limit vole populations locally, even during favourable summer conditions, and have extended negative effects on the dynamics of vole populations. In addition, predation alleviated interspecific competition between the vole species and is, therefore, a potential factor enabling the coexistence of them.     

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.     

Rainfall, ambient temperature, and Clethrionomys californicus capture frequency

Sixty Western Red-backed Voles Clethrionomys californicus inhabiting an old-growth mixed conifer forest in north-western California (USA) were studied over 2 years to assess relationships among vole capture frequency, rainfall, and ambient temperature. Red-backed Voles were encountered more often and recapture rates per vole doubled with the tripling of yearly rainfall. In addition, more voles were captured during wet months than dry months. Analysed over weekly intervals, captures were positively correlated with the amount of weekly rainfall, a greater proportion of the known vole population was encountered during wet weeks than dry weeks, and increased weekly rainfall resulted in an increased proportion of the vole population captured. Significant relationships were not found between daily rainfall and vole captures, but both minimum and maximum daily ambient temperatures were lower when voles were trapped. Vole captures increased with decreases in daily and weekly minimum and maximum ambient temperatures. Weekly rainfall in combination with minimum weekly temperatures accounted for the greatest explanation of variability in vole capture frequencies. These results document that rainfall and ambient temperature have an impact on Western Red-backed Vole capture frequency; thus these weather variables should be addressed as covariates in analyses focused on capture data for this species.     

The predation risks of interspecific eavesdropping: weasel–vole interactions

Competing species benefit from eavesdropping on each other's signals by learning about shared resources or predators. But conspicuous signals are also open to exploitation by eavesdropping predators and should also pose a threat to other sympatric prey species. In western Finland, sibling voles Microtus rossiameridionalis and field voles M. agrestis compete for food and space, and both species rely upon scent marks for intraspecific communication. Both vole species are prey to a range of terrestrial scent hunting predators such as least weasels, however, the competitively superior sibling voles are taken preferentially. We tested in large out‐door enclosures whether field voles eavesdrop on the signals of its competitor, and whether they behave as though this eavesdropping carries a risk of predation. We presented field voles with scent marks from unknown conspecifics and sibling voles and measured their visitation, activity and scent marking behaviours at these scents under high (weasel present) and low (weasel absent) predation risk. Field voles readily visited both field and sibling vole scents under both high and low predation risk; however their activity at sibling vole scent marks declined significantly under increased predation risk. In contrast, predation risk did not affect field voles’ activity at conspecific scents. Thus, field voles were compelled to maintain eavesdropping on heterospecific scents under an increased risk of predation, however they compensated for this additional risk by reducing their activity at these risky scents. Scent marking rates declined significantly under high predation risk. Our results therefore reveal a hidden complexity in the use of social signals within multi‐species assemblages that is clearly sensitive to the potential for increased predation risk. The predation risks of interspecific eavesdropping demonstrated here represents a significant generalisation of the concept of associational susceptibility.     

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.     

典型草原区布氏田鼠鼠害防治的经济阈值

采用种群动态分析方法,分析了内蒙古典型草原区布氏田鼠防治经济阈值.结果表明,1995 ～2005年间布氏田鼠(Lasiopodomys brandtii)早春化学防治的经济阈值分别为36.4、48.8、45.2、39.6、51.2、51.7、48.6、47.2、45.4、40.8、40.1只/hm2,而2010 ～ 2012年间的经济阈值则为41.8、39.8、38.7只/hm2.1995～2012年间,布氏田鼠防治的经济阈值基本稳定在45只/hm2左右.布氏田鼠鼠害的防治经济阈值主要受牧羊放牧收益、灭鼠成本和灭鼠成效的影响,牧羊年均放牧收益与布氏田鼠早春防治经济阈值呈反比关系.根据2010～2012年间的调查结果,近年来布氏田鼠早春防治经济阈值的参考数值为40只/hm2.     

The impact of short-term predator removal on vole dynamics in an arctic-alpine landscape

During 1991–95, mammalian predators (weasel, Mustela nivalis , stoat, M. erminea , mink, M. vison , and red fox, Vulpes vulpes ) were excluded in late summers from a 2 ha piece of a north Norwegian mountain slope. The exclosure extended from an outpost of luxuriant sub-arctic birch forest to a typical arctic–alpine habitat complex, including productive willow scrublands, tundra heaths, dry ridges and snow-beds. The exclosure thus encompassed the entire range of habitat conditions encountered in a typical north Fennoscandian mountain and tundra landscapes. During 1991–95, the exclosure was predator-proof from late July to late September. In wintertime and in early summer, the exclosure was accessible to mammalian predators. Vole dynamics in the short-term exclosure were compared to dynamics in five reference areas with similar habitat conditions.
In 1991, when vole densities were rising in the area, neither collective vole densities nor densities of individual vole species differed significantly between the exclosure and the replicated controls. Spring densities of voles were never significantly different between the exclosure and the controls. With respect to autumnal densities of voles, however, the exclosure was a statistical outlier in the peak year 1992 and throughout the gradual decline phase of 1993–95. In the peak year, the difference in collective vole densities was modest (30%), but increased to two-fold during the first two decline years and was almost four-fold in the crash year of 1995. The strongest response was displayed by field voles ( Microtus agrestis ), hypothesized to be the pivotal prey species of weasels, especially by females and young individuals, i.e. by the functional categories especially sensitive to mammalian predation. These results are consistent with the hypothesis that predation plays a pivotal role for the regulation of herbivorous mammals in relatively productive arctic–alpine habitats.     

SHORT-TERM DEMOGRAPHIC RESPONSE OF THE RED-BACKED VOLE TO SPRUCE BEETLE INFESTATIONS IN ALASKA

Abstract: How small mammals are affected by habitat changes caused by forest insect epidemics is largely unknown. Our objective was to determine the influence of spruce beetle (Dendroctonus rufipennis) epidemics on the dynamics of northern red-backed vole (Clethrionomys rutilus) populations approximately 10 years post-infestation. We conducted a mark-recapture study on northern red-backed voles for 2 field seasons in the Copper River Basin, Alaska, USA, where recent beetle infestations were widespread. Using the robust sampling design, we produced estimates of vole abundance, survival, and recruitment in 3 locations that varied in their degree of beetle-induced spruce mortality. Vole abundance inversely related to the level of spruce mortality. Vole recruitment showed a larger contribution from both immigration and in situ reproduction in the low infestation site than in the medium and heavy infestation sites. No differences in vole survival were detectable across the 3 locations with varied beetle-induced spruce mortality levels. Measured vole food resources and protective vegetative cover did not vary greatly across infestation levels. Abundance and recruitment parameters indicate a negative change induced by spruce beetle infestations. However, the effect of beetles was not large enough to cause the variation in vole survival. Spruce mortality levels may need to be over 50% before greatly influencing the habitat and the demographics of northern red-backed voles.     

Seasonal changes in the numerical responses of predators to cyclic vole populations

Theoretical models predict that a delayed density-dependent mortality factor with a time lag of ca 9 months is able to drive 3–5-yr population cycles of northern voles. We studied numerical responses of predators in western Finland during 1986–92, in an area with 3-yr population cycles of voles. Abundances of small mammals were monitored in several farmland areas (each 3 km²) by snap-trapping in April, June, August, and October (only in 1986–90), and the abundances of avian, mammalian, and reptilian predators by visual censuses during trapping occasions. The 3-yr cycle studied was a cycle of Microtus voles (field vole M. agrestis and sibling vole M. rossiaemeridionalis ) and their small-sized predators (small mustelids and vole-eating birds of prey). The numerical responses of both migratory avian predators and small mustelids to changes in vole densities were more alike than different. In late summer (August), the time lag in the numerical response of all main predators was short (0–4 months), whereas longer time lags prevailed from spring to early summer. The length of the time lag in spring appeared to be related to the length of the winter, which indicates that strong seasonality may create longer time lags to the numerical response of predators at northern latitudes than at more southern latitudes. Our results suggest that, from spring to early summer, predation by migratory avian predators may act in concordance with mustelid predation to produce the long time lag necessary to drive the 3-yr cycle of voles, whereas almost direct density-dependent predation by all major predators in late summer may dampen spatial variation in prey densities.     

Spatial dynamics of Microtus vole populations in continuous and fragmented agricultural landscapes

Small mammal populations often exhibit large-scale spatial synchrony, which is purportedly caused by stochastic weather-related environmental perturbations, predation or dispersal. To elucidate the relative synchronizing effects of environmental perturbations from those of dispersal movements of small mammalian prey or their predators, we investigated the spatial dynamics of Microtus vole populations in two differently structured landscapes which experience similar patterns of weather and climatic conditions. Vole and predator abundances were monitored for three years on 28 agricultural field sites arranged into two 120-km-long transect lines in western Finland. Sites on one transect were interconnected by continuous agricultural farmland (continuous landscape), while sites on the other were isolated from one another to a varying degree by mainly forests (fragmented landscape). Vole populations exhibited large-scale (>120 km) spatial synchrony in fluctuations, which did not differ in degree between the landscapes or decline with increasing distance between trapping sites. However, spatial variation in vole population growth rates was higher in the fragmented than in the continuous landscape. Although vole-eating predators were more numerous in the continuous agricultural landscape than in the fragmented, our results suggest that predators do not exert a great influence on the degree of spatial synchrony of vole population fluctuations, but they may contribute to bringing out-of-phase prey patches towards a regional density level. The spatial dynamics of vole populations were similar in both fragmented and continuous landscapes despite inter-landscape differences in both predator abundance and possibilities of vole dispersal. This implies that the primary source of synchronization lies in a common weather-related environment.     

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.     

The Tien Shan vole (Microtus ilaeus; Rodentia: Cricetidae) as a new species in the Late Pleistocene of Europe

Grey voles (subgenus Microtus) represent a complex of at least seven closely related and partly cryptic species. The range of these species extends from the Atlantic to the Altai Mountains, but most of them occur east of the Black Sea. Using ancient DNA analyses of the Late Pleistocene specimens, we identified a new mtDNA lineage of grey voles in Europe. Phylogenetic analysis of mitochondrial DNA cytochrome b sequences from 23 voles from three caves, namely, Emine–Bair–Khosar (Crimea, Ukraine), Cave 16 (Bulgaria), and Bacho Kiro (Bulgaria), showed that 14 specimens form a previously unrecognized lineage, sister to the Tien Shan vole. The average sequence divergence of this lineage and the extant Tien Shan vole was 4.8%, which is similar to the divergence of grey vole forms, which are considered distinct species or being on the verge of speciation; M. arvalis and M. obscurus or M. mystacinus and M. rossiaemeridionalis. We estimated the time to the most recent common ancestor of the grey voles to be 0.66 Ma, which is over twice the recent estimates, while the divergence of the extant Tien Shan vole and the new lineage to be 0.29 Ma. Our discovery suggests that grey voles may have been more diversified in the past and that their ranges may have differed substantially from current ones. It also underlines the utility of ancient DNA to decipher the evolutionary history of voles.     

Variation in the diet composition of a generalist predator, the red fox, in relation to season and density of main prey

Diet composition of a generalist predator, the red fox (Vulpes vulpes) in relation to season (winter or summer) and abundance of multi-annually cyclic voles was studied in western Finland from 1983 to 1995. The proportion of scats (PS; a total of 58 scats) including each food category was calculated for each prey group. Microtus voles (the field vole M. agrestis and the sibling vole M. rossiaemeridionalis) were the main prey group of foxes (PS = 0.55) and they frequently occurred in the scats both in the winter and summer (PSs 0.50 and 0.62, respectively). There was a positive correlation between the PSs of Microtus voles in the winter diet of foxes and the density indices of these voles in the previous autumn. Other microtine rodents (the bank vole Clethrionomys glareolus, the water vole Arvicola terrestris and the muskrat Ondatra zibethicus) were consumed more in winter than in summer. The unusually high small mustelid predation by red foxes (PS = approx. 0.10) in our study area gives qualitative support for the hypothesis on the limiting impact of mammalian predators on least weasel and stoat populations. None of the important prey groups was preyed upon more at low than at high densities of main prey (Microtus voles). This is consistent with the notion that red foxes are generalist predators that tend to opportunistically subsist on many prey groups. Among these prey groups, particularly hares and birds (including grouse), were frequently used as food by foxes.     

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.