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.     

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.     

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.     

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.     

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.     

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.     

Modeling spatiotemporal dynamics of vole populations in Europe and America

The mathematical models proposed and studied in the present paper provide a unified framework to understand complex dynamical patterns in vole populations in Europe and North America. We have extended the well-known model provided by Hanski and Turchin by incorporating the diffusion term and spatial heterogeneity and performed several mathematical and numerical analyses to explore the dynamics in space and time of the model. These models successfully predicted the observed rodent dynamics in these regions. An attempt has been made to bridge the gap between the field and theoretical studies carried out by Turchin and Hanski (1997) [23] and Turchin and Ellner (2000) [24]. Simulation experiments, mainly two-dimensional parameter scans, show the importance of spatial heterogeneity in order to understand the poorly understood fluctuations in population densities of voles in Fennoscandia and Northern America. This study shed new light upon the dynamics of voles in these regions. The nonlinear analysis of vole data suggests that the dynamical shift is from stability to chaos. Diffusion driven model systems predict a new type of dynamics not yet observed in the field studies of vole populations carried out so far. This has been termed as chaotic in time and regular in space (CTRS). We observed CTRS dynamics in several simulation experiments. This directs us to expect that dynamics of this animal would be de-correlated in time and simultaneously mass extinctions might be possible at many spatial locations.     

Genetic structure and colonization processes in European populations of the common vole, Microtus arvalis

The level of genetic differentiation within and between evolutionary lineages of the common vole (Microtus arvalis) in Europe was examined by analyzing mitochondrial sequences from the control region (mtDNA) and 12 nuclear microsatellite loci (nucDNA) for 338 voles from 18 populations. The distribution of evolutionary lineages and the affinity of populations to lineages were determined with additional sequence data from the mitochondrial cytochrome b gene. Our analyses demonstrated very high levels of differentiation between populations (overall FST: mtDNA 70%; nucDNA 17%). The affinity of populations to evolutionary lineages was strongly reflected in mtDNA but not in nucDNA variation. Patterns of genetic structure for both markers visualized in synthetic genetic maps suggest a postglacial range expansion of the species into the Alps, as well as a potentially more ancient colonization from the northeast to the southwest of Europe. This expansion is supported by estimates for the divergence times between evolutionary lineages and within the western European lineage, which predate the last glacial maximum (LGM). Furthermore, all measures of genetic diversity within populations increased significantly with longitude and showed a trend toward increase with latitude. We conclude that the detected patterns are difficult to explain only by range expansions from separate LGM refugia close to the Mediterranean. This suggests that some M. arvalis populations persisted during the LGM in suitable habitat further north and that the gradients in genetic diversity may represent traces of a more ancient colonization of Europe by the species.     

Linking demography and host dispersal to Trichuris arvicolae distribution in a cyclic vole species

Spatial structure in the distribution of pathogen infection can influence both epidemiology and host-parasite coevolutionary processes. It may result from the spatial heterogeneity of intrinsic and extrinsic factors, or from the local population dynamics of hosts and parasites. In this study, we investigated the effects of landscape, host dispersal and demography (population abundance and phase of the fluctuation) on the distribution of a gastro-intestinal nematode Trichuris arvicolae in the fossorial water vole Arvicola terrestris sherman. This rodent exhibits outbreaks occurring regularly in Franche-Comté (France). Thirteen out-of-phase populations were studied in autumn 2003. They exhibited highly different T. arvicolae prevalences. The heterogeneity in prevalences was not explained by population structure, landscape or vole abundance, but by the phase of the vole population fluctuations. Populations at the end of the high density phase showed null prevalence whereas populations in increase or outbreak phases exhibited higher prevalences. Population genetic analyses based on microsatellites revealed significant differentiation between vole populations, and higher dispersal rates of young voles compared with old ones. These younger individuals were also infected more frequently than older voles. This suggested a role of host dispersal in the distribution of T. arvicolae. However, there was a strong discrepancy between the spatial patterns of prevalence and of host genetics or demographic phase. Genetic differentiation and differences in demographic phase exhibited significant spatial autocorrelations whereas prevalence did not. We concluded that the distribution of T. arvicolae is influenced by vole dispersal, although this effect might be overwhelmed by local adaptation processes or environmental conditions.     

The role of vole populations in prevalence of the parasite (Echinococcus multilocularis) in foxes

Effects of population fluctuation of the gray-sided vole(Clethrionomys rufocanus) on the prevalence (infection rates) of the parasiteEchinococcus multilocularis in red fox(Vulpes vulpes) populations was investigated from 1985 to 1992 in eastern Hokkaido (Abashiri, Nemuro, and Kushiro area), Japan. This parasite needs two hosts to complete its life cycle; the gray-sided vole as its intermediate host and the red fox as its final host. We found that: (1) Infection rates in foxes depended on the current-year abundance of voles in all three study areas, particularly in Abashiri. (2) In addition to this direct density-dependence, delayed density-dependence between the infection rate and the prior-year abundance of voles was detected in Nemuro and in Kushiro. (3) The regional differences in density-dependence pattern were related to regional differences in the winter food habits of red foxes: in Abashiri the proportion of voles in the fox’s diet greatly decreases in winter, while the proportion remains high in winter in Nemuro and in Kushiro, probably because of shallower snowpack. These results suggest that infection rates in foxes in Abashiri were less influenced by the prior-year prevalence, since the infection cycle might be interrupted in winter, when voles became less important in fox’s diet. In contrast, the state of the prevalence may carry over from year to year in Nemuro and in Kushiro, because red foxes continue to eat a considerable amount of voles throughout year. The regionally contrasted results for the relationship between infection rate in foxes and vole abundance were parallel to the regional difference in fluctuation pattern of vole populations, which are highly variable in Abashiri area, but less variable in Kushiro-Nemuro area. Drastic change in vole populations appears to affect the host-parasite system.     

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.     

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.     

The dynamics of abundance and incidence of annual plant species during colonization in a desert

We studied colonization of annual plants in small-scale disturbances and undisturbed soil for four years in the northern Negev desert. The experiment consisted of 24 patches of I m²: eight undisturbed patches, eight 30 cm deep pits and eight 20 cm high mounds. Disturbance removed the seed bank from the pits and mounds. Rainfall was average during 1992 and 1993 (163.5 and 157.0 mm), very low in 1994 (97.5 mm) and very high in 1995 (283.0 mm). For all ca 100 species in the assemblage, we measured abundance, as the average local density in patches occupied by the species, and incidence, the proportion of patches occupied. Abundance and incidence were positively correlated in the four years of the study (R^2-= 0.71, 0.56. 0. 56 and 0.64). The relationship became steeper during the course of colonization. A minority of species colonized all patches rapidly and increased exponentially in abundance. These high incidence and abundance species responded little or not at all to variations in rainfall. Most of the species experienced frequent local extinctions and colonizations in few patches. These low abundance and low to medium incidence species responded strongly to rainfall by fluctuations in abundance. Differences per species between abundance and/or incidence in pits, mounds and matrix were evident in many species along the entire relationship. These were mostly in favor of pits. We propose that the positions and trajectories of the individual species in the abundance-incidence phase plane signify constraints on population growth along the abundance axis, and on colonization and population persistence along the incidence axis. Since species with lower incidence and abundance respond strongly to rainfall variation, we conclude that their local populations and spatial distribution are to a large extent site-limited. High-abundance and high-incidence species have few or weak constraints and experience density-independent population growth, which is only seed-limited. The causes of site limitation and its effect on population growth and on eotonization and extinction processes differ for different species. In a number of species, abundance and incidence may be limited by dispersal, in conjunction with dispersal mode and patch-specific seed capture. Based on our case study we suggest that the trajectories of the species in the abundance-incidence phase plane are a useful tool for investigating assemblage dynamics.     

Climate change affects colonization dynamics in a metacommunity of three Daphnia species

Climate change is expected to alter the range and abundance of many species by influencing habitat qualities. For species living in fragmented populations, not only the quality of the present patches but also access to new habitat patches may be affected. Here, we show that colonization in a metacommunity can be directly influenced by weather changes, and that these observed weather changes are consistent with global climate change models. Using a long‐term dataset from a rock pool metacommunity of the three species Daphnia magna, Daphnia longispina and Daphnia pulex with 507 monitored habitat patches, we correlated a four‐fold increase in colonization rate with warmer, drier weather for the period from 1982 to 2006. The higher colonization rate after warm and dry summers led to an increase in metacommunity dynamics over time. A mechanistic explanation for the increased colonization rate is that the resting stages have a higher exposure to animal and wind dispersal in desiccated rock pools. Although colonization rates reacted in the same direction in all three species, there were significant species‐specific effects that resulted in an overall change in the metacommunity composition. Increased local instability and colonization dynamics may even lead to higher global stability of the metacommunity. Thus, whereas climate change has been reported to cause a unidirectional change in species range for many other species, it changes the dynamics and composition of an entire community in this metacommunity, with winners and losers difficult to predict.     

The role of seasonality in the dynamics of deer tick populations

In this paper, we formulate a nonlinear system of difference equations that models the three-stage life cycle of the deer tick over four seasons. We study the effect of seasonality on the stability and oscillatory behavior of the tick population by comparing analytically the seasonal model with a non-seasonal one. The analysis of the models reveals the existence of two equilibrium points. We discuss the necessary and sufficient conditions for local asymptotic stability of the equilibria and analyze the boundedness and oscillatory behavior of the solutions. A main result of the mathematical analysis is that seasonality in the life cycle of the deer tick can have a positive effect, in the sense that it increases the stability of the system. It is also shown that for some combination of parameters within the stability region, perturbations will result in a return to the equilibrium through transient oscillations. The models are used to explore the biological consequences of parameter variations reflecting expected environmental changes.     

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 role of migration in mutant dynamics in fragmented populations

Mutant dynamics in fragmented populations have been studied extensively in evolutionary biology. Yet, open questions remain, both experimentally and theoretically. Some of the fundamental properties predicted by models still need to be addressed experimentally. We contribute to this by using a combination of experiments and theory to investigate the role of migration in mutant distribution. In the case of neutral mutants, while the mean frequency of mutants is not influenced by migration, the probability distribution is. To address this empirically, we performed in vitro experiments, where mixtures of GFP-labelled (“mutant”) and non-labelled (“wid-type”) murine cells were grown in wells (demes), and migration was mimicked via cell transfer from well to well. In the presence of migration, we observed a change in the skewedness of the distribution of the mutant frequencies in the wells, consistent with previous and our own model predictions. In the presence of de novo mutant production, we used modelling to investigate the level at which disadvantageous mutants are predicted to exist, which has implications for the adaptive potential of the population in case of an environmental change. In panmictic populations, disadvantageous mutants can persist around a steady state, determined by the rate of mutant production and the selective disadvantage (selection-mutation balance). In a fragmented system that consists of demes connected by migration, a steady-state persistence of disadvantageous mutants is also observed, which, however, is fundamentally different from the mutation-selection balance and characterized by higher mutant levels. The increase in mutant frequencies above the selection-mutation balance can be maintained in small ($N<N_c$) demes as long as the migration rate is sufficiently small. The migration rate above which the mutants approach the selection-mutation balance decays exponentially with $N/N_c$. The observed increase in the mutant numbers is not explained by the change in the effective population size. Implications for evolutionary processes in diseases are discussed, where the pre-existence of disadvantageous drug-resistant mutant cells or pathogens drives the response of the disease to treatments.