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.     

Dispersal,landscape and travelling waves in cyclic vole populations

Travelling waves (TW) are among the most striking ecological phenomena emerging in oscillating populations. Despite much theory, understanding how real‐world TW arise remains a challenge for ecology. Herein, we analyse 16‐year time series of cyclic vole populations collected at 314 localities covering 2500 km² in France. We found evidence for a linear front TW spreading at a speed of 7.4 km year^?1 along a north‐west/south‐east direction and radiating away from a major landscape discontinuity as predicted by recent theory. The spatial signature of vole dispersal was assessed using genetic data collected at 14 localities. Both data sets were handled using similar autocorrelation approaches. Our results revealed a remarkable congruence of the spatial extent and direction of anisotropy of both demographic and genetic structures. Our results constitute the first empirical evidence that effective dispersal is limited in the direction of TW while most of the individual exchanges occur along the wave front.     

Tuberculosis (Mycobacterium microti) in wild field vole populations

Vole tuberculosis (TB; Mycobacterium microti) is an understudied endemic infection. Despite progressing slowly, it causes severe clinical pathology and overt symptoms in its rodent host. TB was monitored for 2 years in wild field voles in Kielder Forest, UK. The prevalence of characteristic cutaneous TB lesions was monitored longitudinally at 4 sites, with individuals live-trapped and repeatedly monitored. A prevalence of 5.2% of individuals with lesions was recorded (n=2791). In a cross-sectional study, 27 sites were monitored bi-annually, with TB assessed by post-mortem examination for macroscopic lesions, and by culture and histopathology. Seventy-nine voles (10.78%; n=733) were positive for mycobacteria, with the highest prevalence in spring (13.15%; n=327). TB prevalence varied, with between 0% and 50% of voles infected per site. Prevalence increased with age (mass), and apparent seasonality was due to a higher proportion of older animals in spring. Survival analysis supported this result, with cutaneous lesions only manifesting in the advanced stages of infection, and therefore only being found on older voles. The body condition of individuals with lesions declined at the time when the lesion was first recorded, when compared to individuals without lesions, suggesting there may be an acute phase of infection during its advanced stage. Although predicted survival following the appearance of a cutaneous lesion was lower than for uninfected individuals, this was not significant.     

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.     

Disease dynamics in cyclic populations of field voles (Microtus agrestis): cowpox virus and vole tuberculosis (Mycobacterium microti)

The possible role of pathogens in rodent population cycles has been largely neglected since Elton's 'epidemic hypothesis' of 1931. To revisit this question, 12 adjacent, cyclic but out-of-phase populations of field voles (Microtus agrestis) in North East England were studied and the initial results are presented here. The prevalences of antibodies to cowpox virus and of clinical signs of Mycobacterium microti infection (vole tuberculosis) showed delayed (not direct) density dependence (with a lag of three to six months). This did not result from changes in population structure, even though there were such changes associated with the different phases of the cycle. The prevalences rose as vole numbers rose, and peaked as numbers declined. The apparent lag in the numerical response of infection prevalence to changes in host abundance is consistent with the hypothesis that diseases, singly or in combination, play a hitherto underestimated role in the dynamics of cyclic populations.     

The dynamics of health in wild field vole populations: a haematological perspective

1. Pathogens have been proposed as potentially important drivers of population dynamics, but while a few studies have investigated the impact of specific pathogens, the wealth of information provided by general indices of health has hardly been exploited. By evaluating haematological parameters in wild populations, our knowledge of the dynamics of health and infection may be better understood. 2. Here, haematological dynamics in natural populations of field voles are investigated to determine environmental and host factors associated with indicators of inflammatory response (counts of monocytes and neutrophils) and of condition: measures of immunological investment (lymphocyte counts) and aerobic capacity (red blood cell counts). 3. Individuals from three field vole populations were sampled monthly for 2 years. Comparisons with individuals kept under controlled conditions facilitated interpretation of field data. Mixed effects models were developed for each cell type to evaluate separately the effects of various factors on post-juvenile voles and mature breeding females. 4. There were three well-characterized 'physiological' seasons. The immunological investment appeared lowest in winter (lowest lymphocyte counts), but red blood cells were at their highest levels and indices of inflammatory response at their lowest. Spring was characterized by a fall in red blood cell counts and peaks in indicators of inflammatory response. During the course of summer-autumn, red blood cell counts recovered, the immunological investment increased and the indicators of inflammatory response decreased. 5. Poor body condition appeared to affect the inflammatory response (lower neutrophil and monocyte peaks) and the immunological investment (lower lymphocyte counts), providing evidence that the capacity to fight infection is dependent upon host condition. 6. Breeding early in the year was most likely in females in better condition (high lymphocyte and red blood cell counts). 7. All the haematological parameters were affected adversely by high population densities.     

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

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

Spatial dynamics in fluctuating vole populations

Summary Patterns and consistency of distribution, spatial and temporal components, and the extent of spatial density-dependence were compared between semi-cyclic and cyclic populations of the vole species Clethrionomys glareolus and Microtus agrestis in south-central and north Sweden. Cyclic populations were less clumped and only C. glareolus showed a consistency in distribution between years. Spatial variation contributed little to the distributions in cyclic populations while the spatial and temporal variations were of the same magnitude in the semi-cyclic populations. The latter populations could be subdivided into areas with different spatial and temporal components. The spatial density-dependence increased from increase to decline years in C. glareolus but not in M. agrestis, which differed conspicuously between reregions in population development. The data imply that spatial dynamics should be considered as much as temporal ones for non-cyclic populations, that the same regulating or limiting factors may be at work in both spatial and temporal components and that, in addition, social behaviour may be important in explaining spatial dynamics. However, the latter effects may be fairly species-specific.     

Cowpox virus infection in natural field vole Microtus agrestis populations: significant negative impacts on survival

1. Cowpox virus is an endemic virus circulating in populations of wild rodents. It has been implicated as a potential cause of population cycles in field voles Microtus agrestis L., in Britain, owing to a delayed density-dependent pattern in prevalence, but its impact on field vole demographic parameters is unknown. This study tests the hypothesis that wild field voles infected with cowpox virus have a lower probability of survival than uninfected individuals. 2. The effect of cowpox virus infection on the probability of an individual surviving to the next month was investigated using longitudinal data collected over 2 years from four grassland sites in Kielder Forest, UK. This effect was also investigated at the population level, by examining whether infection prevalence explained temporal variation in survival rates, once other factors influencing survival had been controlled for. 3. Individuals with a probability of infection, P(I), of 1 at a time when base survival rate was at median levels had a 22.4% lower estimated probability of survival than uninfected individuals, whereas those with a P(I) of 0.5 had a 10.4% lower survival. 4. At the population level, survival rates also decreased with increasing cowpox prevalence, with lower survival rates in months of higher cowpox prevalence. 5. Simple matrix projection models with 28 day time steps and two stages, with 71% of voles experiencing cowpox infection in their second month of life (the average observed seroprevalence at the end of the breeding season) predict a reduction in 28-day population growth rate during the breeding season from lambda = 1.62 to 1.53 for populations with no cowpox infection compared with infected populations. 6. This negative correlation between cowpox virus infection and field vole survival, with its potentially significant effect on population growth rate, is the first for an endemic pathogen in a cyclic population of wild rodents.     

Variation in predation risk and vole feeding behaviour: a field test of the risk allocation hypothesis

Many prey animals experience temporal variation in the risk of predation and therefore face the problem of allocating their time between antipredator efforts and other activities like feeding and breeding. We investigated time allocation of prey animals that balanced predation risk and feeding opportunities. The predation risk allocation hypothesis predicts that animals should forage more in low- than in high-risk situations and that this difference should increase with an increasing attack ratio (i.e. difference between low- and high-risk situations) and proportion of time spent at high risk. To test these predictions we conducted a field test using bank voles (Clethrionomys glareolus) as a prey and the least weasel (Mustela nivalis nivalis) as a predator. The temporal pattern and intensity of predation risk were manipulated in large outdoor enclosures and the foraging effort and patch use of voles were measured by recording giving-up densities. We did not observe any variation in feeding effort due to changes in the level of risk or the proportion of time spent under high-risk conditions. The only significant effect was found when the attack ratio was altered: the foraging effort of voles was higher in the treatment with a low attack ratio than in the treatment with a high attack ratio. Thus the results did not support the predation risk allocation hypothesis and we question the applicability of the hypothesis to our study system. We argue that the deviation between the observed pattern of feeding behaviour of bank voles and that predicted by the predation risk allocation hypothesis was mostly due to the inability of voles to accurately assess the changes in the level of risk. However, we also emphasise the difficulties of testing hypotheses under outdoor conditions and with mammals capable of flexible behavioural patterns.     

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.     

Surviving winter: Food,but not habitat structure,prevents crashes in cyclic vole populations

Vole population cycles are a major force driving boreal ecosystem dynamics in northwestern Eurasia. However, our understanding of the impact of winter on these cycles is increasingly uncertain, especially because climate change is affecting snow predictability, quality, and abundance. We examined the role of winter weather and snow conditions, the lack of suitable habitat structure during freeze‐thaw periods, and the lack of sufficient food as potential causes for winter population crashes. We live‐trapped bank voles Myodes glareolus on 26 plots (0.36 ha each) at two different elevations (representing different winter conditions) in southeast Norway in the winters 2013/2014 and 2014/2015. We carried out two manipulations: supplementing six plots with food to eliminate food limitation and six plots with straw to improve habitat structure and limit the effect of icing in the subnivean space. In the first winter, all bank voles survived well on all plots, whereas in the second winter voles on almost all plots went extinct except for those receiving supplemental food. Survival was highest on the feeding treatment in both winters, whereas improving habitat structure had no effect. We conclude that food limitation was a key factor in causing winter population crashes.     

Suppressed breeding in the field vole (Microtus agrestis): an adaptation to cyclically fluctuating predation risk

The densities of microtine rodents and their main predators,small mustelids, fluctuate synchronously in 3–5-year cyclesin central and northern Fennoscandia. Predation by small mustelidshas been suggested as one of the driving forces in microtinecyclicity, causing deep synchronous declines of several volespecies. We studied experimentally the effects of small mustelidson mating behavior, foraging, and breeding in nonwintered fieldvoles (Microtus agrestis) originating from a cyclic population.By using mustelid odors, we simulated a crash phase environmentwith high predation risk for breeding pairs of voles. In ourexperiments, 87% of the female field voles suppressed breedingwhen exposed to mustelid odors. Both female and male behaviorchanged, and no mating behaviors were observed under the simulatedpredation risk. Weights of both sexes decreased when exposedto mustelid odor, probably due to decreased foraging; weightsof the control females increased due to pregnancy; and no weightchanges occurred in control males. Decreased breeding and foragingpossibilities under high predation pressure may form the basisfor the ultimate explanation for breeding suppression. Thereare at least two different mechanisms for breeding suppression:either mating does not take place or malnutrition in femalesdoes not' allow breeding to occur. Delayed breeding under highrisk of predation, for whatever reason, could increase the probabilityof individuals, especially that of the females, to survive overthe crash to the next, safer breeding season when their youngwould have better possibilities to survive.     

How predation and landscape fragmentation affect vole population dynamics

Background

Microtine species in Fennoscandia display a distinct north-south gradient from regular cycles to stable populations. The gradient has often been attributed to changes in the interactions between microtines and their predators. Although the spatial structure of the environment is known to influence predator-prey dynamics of a wide range of species, it has scarcely been considered in relation to the Fennoscandian gradient. Furthermore, the length of microtine breeding season also displays a north-south gradient. However, little consideration has been given to its role in shaping or generating population cycles. Because these factors covary along the gradient it is difficult to distinguish their effects experimentally in the field. The distinction is here attempted using realistic agent-based modelling.

Methodology/Principal Findings

By using a spatially explicit computer simulation model based on behavioural and ecological data from the field vole (Microtus agrestis), we generated a number of repeated time series of vole densities whose mean population size and amplitude were measured. Subsequently, these time series were subjected to statistical autoregressive modelling, to investigate the effects on vole population dynamics of making predators more specialised, of altering the breeding season, and increasing the level of habitat fragmentation. We found that fragmentation as well as the presence of specialist predators are necessary for the occurrence of population cycles. Habitat fragmentation and predator assembly jointly determined cycle length and amplitude. Length of vole breeding season had little impact on the oscillations.

Significance

There is good agreement between our results and the experimental work from Fennoscandia, but our results allow distinction of causation that is hard to unravel in field experiments. We hope our results will help understand the reasons for cycle gradients observed in other areas. Our results clearly demonstrate the importance of landscape fragmentation for population cycling and we recommend that the degree of fragmentation be more fully considered in future analyses of vole dynamics.     

The effect of habitat size and predation on the time to extinction of prairie vole populations: simulation studies via SERDYCA

We present a spatially explicit individual-based model of rodent dynamics, customized for the prairie vole species, Microtus ochrogaster. The model strives to represent the complexity of intertwining factors that determine the spatio-temporal dynamics of small rodents. It is based on trophic relationships and incorporates important features such as territorial competition, mating behavior, density-dependent predation and dispersal out of the modeled spatial region. Vegetation growth and vole fecundity are dependent on climatic components. The results of simulations show that the model correctly predicts the overall temporal dynamics of the population density. Time-series analysis shows a very good match between the periods corresponding to the peak population density frequencies predicted by the model and the ones reported in the literature. The model is used to study the relation between persistence, landscape area and predation. We use the notions of average time to extinction (ATE) and persistence frequency to quantify persistence. While the ATE decreases with decrease of area, it is a bell-shaped function of the predation level: increasing for “small” and decreasing for “large” predation levels.     

捕食风险对东方田鼠功能反应格局的作用

植食性哺乳动物对食物斑块的选择和利用不仅取决于食物的可利用性,且与觅食环境潜存的各种风险紧密关联。捕食风险是否通过作用于动物觅食活动中的警觉影响其功能反应格局。在新鲜白三叶叶片构成的各类食物密集斑块上,测定东方田鼠觅食行为,建立功能反应模型,检验捕食风险对其功能反应格局的作用。结果发现,捕食风险能显著地延长东方田鼠的觅食决定时间,但其摄入率保持稳定,功能反应构型亦未发生改变,仍为Ⅱ型功能反应;除了对照组个体的采食时间随叶片大小增大无明显变动规律外,处理组个体的采食时间及对照组和处理组个体的处理时间、觅食中断时间均随叶片大小及口量的增大呈线性增高趋势,处理组个体的觅食中断时间明显大于对照组个体的;对照组和处理组个体的采食率均随叶片大小及口量呈非线性渐近递减趋势,但处理组个体的采食率较对照组个体的略有降低。结果揭示,在捕食风险压力下,虽然上述觅食参数变异能潜在地降低摄入率,但个体能通过改变觅食活动中各种警觉行为动作如降低嗅闻和静听监视动作的发生频次,增大视觉监视动作比重,以此缓冲捕食风险压力,维持摄入率。摄入率测定值与模型预测值的线性回归极显著,表明,功能反应模型具有良好的预测性。在可利用植物密集斑块,动物觅食活动中的警觉能缓冲捕食风险压力;动物摄入率是由植物大小调控的口量决定的,且受采食与处理食物竞争及觅食中断的制约;其功能反应仍属Ⅱ型功能反应。     

Cowpox virus infection in natural field vole Microtus agrestis populations: delayed density dependence and individual risk

1. Little is known about the dynamics of pathogen (microparasite) infection in wildlife populations, and less still about sources of variation in the risk of infection. Here we present the first detailed analysis of such variation. 2. Cowpox virus is an endemic sublethal pathogen circulating in populations of wild rodents. Cowpox prevalence was monitored longitudinally for 2 years, in populations of field voles exhibiting multiannual cycles of density in Kielder Forest, UK. 3. The probability that available susceptible animals seroconverted in a given trap session was significantly positively related to host density with a 3-month time lag. 4. Males were significantly more likely to seroconvert than females. 5. Despite most infection being found in young animals (because transmission rates were generally high) mature individuals were more likely to seroconvert than immature ones, suggesting that behavioural or physiological changes associated with maturity contribute to variation in infection risk. 6. Hence, these analyses confirm that there is a delayed numerical response of cowpox infection to vole density, supporting the hypothesis that endemic pathogens may play some part in shaping vole cycles.     

Metapopulation processes and persistence in remnant water vole populations

We examined the spatial distribution of water vole populations in four consecutive years and investigated whether the regional population processes of extinction, recolonisation and migration influence distribution and persistence. We examined how such regional processes are influenced by spatial variation in habitat quality. In addition, we assessed the relevance of metapopulation concepts for understanding the dynamics of species that deviate from classical metapopulation assumptions and developing conservation measures for them. Populations were patchy and discrete, and the patchy distribution was not static between years. Population turnover occurred even in the absence of predatory mink, which only influenced the network of populations at the end of the study. Most populations were clustered close together in the upper tributaries. Local population persistence was predominantly influenced by population size: large populations were more persistent. Recolonisation rates were influenced by isolation and habitat quality. The isolation estimates which best explained the distribution of water vole populations incorporated straight‐line distances, suggesting water voles disperse overland. The distribution of recolonised sites indicated that dispersing voles actively selected habitat on the basis of its quality. Water voles depart from some of the assumptions made by frequently used metapopulation models. In particular there is no clear binary distinction between suitable and non‐suitable habitat. Accounting for variation in habitat quality before investigating temporal changes in population distribution allowed us to demonstrate that the key metapopulation processes were important. The significance of regional population processes relative to local population processes may have increased in declining, fragmented populations compared to pristine regional populations. We hypothesise that although mink predation is likely to eventually cause regional extinction in many areas, metapopulation processes have delayed this decline. Consequently, conservation measures should take into account mink predation rates and regional population processes, before considering aspects of habitat quality.