Field Vole Populations Research Articles

The vicious circle and infection intensity: The case of Trypanosoma microti in field vole populations

ObjectiveIn natural populations, infection and condition may act synergistically to trigger a vicious circle: poor condition predisposes to host infections, which further reduce condition, and so on. If this vicious circle originates from a reduced resistance to infection, it will not only result in greater proneness to becoming infected of those that are in poorer condition, but it may also cause infections of higher intensity. Here, we investigate the temporal relationship between host condition and intensity of infection by a specific pathogen using as a system the dynamics of the protozoan Trypanosoma microti in field vole (Microtus agrestis) populations. Methods and resultsWith two years of longitudinal data from three monthly-sampled populations, we evaluated if individuals acquiring a high intensity of infection previously had lower haematological indicators of condition (red blood cells [RBCs] and lymphocyte counts) than those that acquired lower infection intensities. Also, the association of these indicators with past and present trypanosome blood levels was investigated. The individuals that developed high levels of parasitaemia were those that previously had low lymphocyte counts. Greater intensity of infection corresponded with lower RBCs only in low to moderate weight females, and no effect of intensity of infection on lymphocyte counts was observed. However, delayed effects of high trypanosome intensity were seen on both RBCs and lymphocytes. ConclusionsThe vicious circle may also result in high infection intensity: individuals in poor condition are not only more likely to become infected by one pathogen; they may also be the most important source of infection for that and for other pathogens, and thus key protagonists for parasite dynamics.

Study of small mammal populations within two Barn owl corridors at Folly Farm

This study examines small mammal populations present within Barn owl corridors on Folly Farm, an Avon Wildlife Trust Reserve located near the village of Bishop Sutton in Bath and North East Somerset. Two corridors were chosen, the primary difference between the two sites being only one has undergone management (grazing). The focus of this study was the Microtus agrestis (Short-tailed field vole) population, the most frequently taken prey item by Barn owls. Apodemus sylvaticus (Wood mice) and Sorex araneus (Common shrew) populations are also discussed as they are frequently taken. Using Longworth live traps, 600 trap-nights data were collected from three sessions in November 2006, February and March 2007. Although M. agrestis was the most abundant species in both corridors, they were more prevalent in the un-grazed corridor (comprising 19 of the 31 individuals). In the corridor that had undergone management, fewer M. agrestis were captured (eight), although a higher species diversity and richness was recorded. Unusually for a grassland habitat, there were nearly as many A. sylvaticus as there were M. agrestis (seven compared with eight) in the grazed corridor. Some small mammal species not usually found in grassland habitats were captured; explanations for these seemingly anomalous results are discussed. Differences in population characteristics between the two corridors are discussed including: sex ratio, weights, seasonal variation and age structure. Pellet analysis from the nearby pair of Barn owls showed that they were preferentially hunting M. agrestis; the pellet data largely mirrored findings of the trapping data.

Genetically controlled differences in behaviour between cycling and non-cycling populations of field vole (Microtus agrestis)

Behavioural tests measuring locomotor activity of single individuals and groups of animals of the same sex have been performed on samples of Microtus agrestis from a cycling population in northern Sweden and a non-cycling population from south Sweden. The activity was higher for animals from the northern population. The differences were more pronounced for males than for females and more for group than for individual activity. The genetic control of this behavioural trait was confirmed by breeding tests. Pure-bred offspring from wild-trapped voles within each area did not deviate from the performance of their parents. The hybrid offspring had intermediate test values. An association between behaviour and population density phase is indicated for the cycling population, but a full cycle has not yet been followed.

Allozyme variation in natural populations of field vole (Microtus agrestis L.). I. Survey of the 'semi-stable' population in southern Sweden.

A ‘semi-stable’ population of field-vole, Microtus agrestis L., has been investigated for allozyme variation. Eight out of 18 loci analyzed were found to be polymorphic. A deficiency of heterozygotes was observed: 32 % in females and 35.4 % in males, indicating subdivision of the population. The average heterozygosity, H, was estimated to 0.22 for the 18 loci investigated.

Habitat Use and Diet Composition of Norwegian Lemmings and Field Voles in Central Norway

This study examined habitat use and diet composition of Norwegian lemmings (Lemmus lemmus) and field voles (Microtus agrestis), which occur together and potentially compete for resources in alpine areas of central Norway. Both species preferred habitats rich in herbaceous monocots and dicots and willow (meadows and willow meadows). However, lemmings spread into other habitats, particularly lichen heath, when populations were high. Lemmings showed a clear preference for monocots in their diet, eating mostly sedges (Carex and Eriophorum), whereas voles had a much more diverse diet that included equal amounts of, and more species of, monocots and dicots. Because relatively little overlap occurred either in habitat use (33‐57%, increasing overlap with lower densities of lemmings) or in diet (30‐51%), and because lemming populations were usually low, exploitative competition between the 2 species seemed unlikely. Nevertheless, aggressive interspecific interactions during occasional years with high lemming densities could still negatively influence populations of field voles.

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.

Parasite interactions in natural populations: insights from longitudinal data

The physiological and immunological state of an animal can be influenced by current infections and infection history. Consequently, both ongoing and previous infections can affect host susceptibility to another parasite, the biology of the subsequent infection (e.g. infection length) and the impact of infection on host morbidity (pathology). In natural populations, most animals will be infected by a succession of different parasites throughout the course of their lives, with probably frequent concomitant infections. The relative timing of different infections experienced by a host (i.e. the sequence of infection events), and the effects on factors such as host susceptibility and host survival, can only be derived from longitudinal data on individual hosts. Here we review some of the evidence for the impact of co-infection on host susceptibility, infection biology and pathology focusing on insights obtained from both longitudinal studies in humans and experiments that explicitly consider the sequence of infection. We then consider the challenges posed by longitudinal infection data collected from natural populations of animals. We illustrate their usefulness using our data of microparasite infections associated with field vole (Microtus agrestis) populations to examine impacts on susceptibility and infection length. Our primary aim is to describe an analytical approach that can be used on such data to identify interactions among the parasites. The preliminary analyses presented here indicate both synergistic and antagonistic interactions between microparasites within this community and emphasise that such interactions could have significant impacts on host-parasite fitness and dynamics.

Breeding structure in two field vole populations.

The breeding structure of the field vole (Microtus agrestis L.) was studied in two populations in the south of Sweden by the use of enzyme electrophoresis. The sampling sites were closely situated but sufficiently separated to make it unlikely for animals to move from one site to the other. The populations were Sampled in two different ways: from the first population, 62 animals were collected over a 17-month period, while at the other site 103 animals were captured within a time-span of less than two weeks. of 21 enzymes studied. 3 were informative about genetic variation at a single locus each (LDH, ME and PGM). The distribution of genotypes for the three polymorphic loci showed no significant deviation from the expected Hardy-Weinberg proportions in any of the populations. When the genotype proportions were calculated for different inbreeding coefficients, the most likely value for the inbreeding coefficient in these populations was well below 0.10. A high degree of inbreeding has earlier been reported to occur in the field vole, but in the present investigation no such evidence was found. Nor was there any variation in allele frequencies between the two populations, which—if present—could lead to a Wahlund effect under a less stringent sampling scheme.

Disease effects on reproduction can cause population cycles in seasonal environments

Recent studies of rodent populations have demonstrated that certain parasites can cause juveniles to delay maturation until the next reproductive season. Furthermore, a variety of parasites may share the same host, and evidence is beginning to accumulate showing nonindependent effects of different infections.We investigated the consequences for host population dynamics of a disease-induced period of no reproduction, and a chronic reduction in fecundity following recovery from infection (such as may be induced by secondary infections) using a modified SIR (susceptible, infected, recovered) model. We also included a seasonally varying birth rate as recent studies have demonstrated that seasonally varying parameters can have important effects on long-term host–parasite dynamics. We investigated the model predictions using parameters derived from five different cyclic rodent populations.Delayed and reduced fecundity following recovery from infection have no effect on the ability of the disease to regulate the host population in the model as they have no effect on the basic reproductive rate. However, these factors can influence the long-term dynamics including whether or not they exhibit multiyear cycles.The model predicts disease-induced multiyear cycles for a wide range of realistic parameter values. Host populations that recover relatively slowly following a disease-induced population crash are more likely to show multiyear cycles. Diseases for which the period of infection is brief, but full recovery of reproductive function is relatively slow, could generate large amplitude multiyear cycles of several years in length. Chronically reduced fecundity following recovery can also induce multiyear cycles, in support of previous theoretical studies.When parameterized for cowpox virus in the cyclic field vole populations (Microtus agrestis) of Kielder Forest (northern England), the model predicts that the disease must chronically reduce host fecundity by more than 70%, following recovery from infection, for it to induce multiyear cycles. When the model predicts quasi-periodic multiyear cycles it also predicts that seroprevalence and the effective date of onset of the reproductive season are delayed density-dependent, two phenomena that have been recorded in the field.

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.

Optimal onset of seasonal reproduction in stochastic environments: When should overwintering small rodents start breeding?

Theories for optimal life history strategies in variable environments have until now focused on cases where the individuals have either no information about the environment (models maximizing geometric mean fitness) or full information about the environment (models predicting optimal reaction norms). In this paper I investigate the optimal time for multivoltine organisms to commence seasonal reproduction in a more general and realistic case where animals perceive the state of their environment through cues that are measured with varying degrees of precision. If there were only a trade-off between early reproduction and high reproductive success, and if animals had perfect information about their environment, it would be optimal to commence reproduction when the rate of change in reproductive success relative to its current value equals the difference between population growth during the reproductive and non-reproductive seasons. This implies that reproductive success at the optimum is independent of when (but not how) the environment improves over the season. However, because it is optimal to respond conservatively to uncertain cues, we should expect higher reproductive success during years when breeding conditions improve early than when they improve late. Nevertheless, a phenotypic correlation between reproductive success and timing of reproduction will probably not be detectable in a stochastic environment. Data from a cyclic population of field voles (Microtus agrestis L.) in northern England show a negative correlation between reproductive success and timing of reproduction among out-of-phase locations. Such a pattern may occur when there is a convex trade-off between pre-breeding survival and timing of reproduction, or if animals precipitate reproduction to avoid senescence when the environment improves late.

Vole–vegetation interactions in an experimental, enemy free taiga floor system

Vole–vegetation interactions in a predation‐free taiga environment of northern Fennoscandia were studied by transferring vegetation from natural Microtus habitats into a greenhouse, where three habitat islands of about 30 m2 were created. The ‘islands’ were subjected to simulated summer conditions and a paired female field vole, Microtusagrestis, was introduced to each ‘island’. The development of the female and her young was followed by recurrent live trapping. The development of the vegetation was followed by recurrent marking and censusing of plant shoots at intervals of five days. In the next growing season, two ‘islands’ were subjected to a new grazing treatment to study the impacts of repeated grazing on the vegetation and on the growth and reproduction of voles. Plant biomasses were harvested at the end of each trial. In all trials, the biomasses of graminoids and non‐toxic herbs other than ferns, fireweeds and rosaceous plants were profoundly decimated. Even the biomass of a toxic herb Aconitum lycoctonum decreased largely at pace with the palatable herbs. The least preferred plant categories maintained their biomasses at control levels. Their neutral collective response was created by opposite species‐level trends. Species typical for moist and nutrient‐rich forests suffered from vole grazing, whereas the biomass of species adapted to disturbed habitats increased.In spite of the dramatic changes in the vegetation, the introduced female voles survived throughout the trials and reproduced normally. The young of their first litters survived well and reached the final weights typical for individuals starting to winter as immatures. We conclude that most of the plant biomass found on productive boreal forest floors is potential food for field voles and remains palatable for them even when subjected to recurrent, severe grazing. If nothing else than summer resources were limiting the growth of the field vole populations, the plants currently dominating moist and nutrient‐rich taiga floors could not survive in this habitat.

Contrasting dynamics of Bartonella spp. in cyclic field vole populations: the impact of vector and host dynamics.

Many zoonotic disease agents are transmitted between hosts by arthropod vectors, including fleas, but few empirical studies of host-vector-microparasite dynamics have investigated the relative importance of hosts and vectors. This study investigates the dynamics of 4 closely related Bartonella species and their flea vectors in cyclic populations of field voles (Microtus agrestis) over 3 years. The probability of flea infestation was positively related to field vole density 12 months previously in autumn, but negatively related to more recent host densities, suggesting a dilution effect. The 4 Bartonella species exhibited contrasting dynamics. Only B. grahamii, showed a distinct seasonal pattern. Infection probability increased with field vole density for B. doshiae, B. taylorii and BGA (a previously unidentified species) and with density of coexisting wood mice for B. doshiae and B. grahamii. However, only the infection probability of BGA in spring was related to flea prevalence. B. doshiae and BGA were most common in older animals, but the other 2 were most common in non-reproductive hosts. Generally, host density rather than vector abundance appears most important for the dynamics of flea-transmitted Bartonella spp., possibly reflecting the importance of flea exchange between hosts. However, even closely related species showed quite different dynamics, emphasising that other factors such as population age structure can impact on zoonotic risk.

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.

A role for vector-independent transmission in rodent trypanosome infection?

Within host–pathogen systems where vector-borne transmission is the primary route of infection, little or no attention has been paid to the relative importance of secondary or alternative routes of transmission. Here, by contrast, we report the results from a controlled longitudinal field-scale experiment in which the prevalence of fleas (Siphonaptera) was manipulated and the occurrence and distribution of a flea-borne protozoan ( Trypanosoma ( Herpetosoma) microti) in a natural field vole ( Microtus agrestis) population was monitored over a 2-year period. A non-systemic insecticide was applied to individual voles within two treatment grids and the prevalences of fleas and of T. microti were monitored on these and on two control grids. Blood samples were taken from all voles and PCR-based methods used to determine infection status. Insecticidal treatment was highly effective at reducing overall flea prevalence and recaptured animals (treated ca. 4 weeks previously) were very rarely infested ( ca. 3%, compared with 50–70+% normally). On the other hand, the probability of trypanosome infection was reduced in treated animals on experimental grids to only around one-third of that normally observed. This suggests that direct, as opposed to flea-borne, transmission may not only occur, it may also be of epidemiological importance. The possibility that the importance of such transmission routes may have been underestimated in ‘vector-borne’ infections more generally is discussed.

Vole cycles and predation in temperate and boreal zones of Europe

Summary Graham & Lambin (2002) have reported on a weasel‐reduction experiment, concluding that the impact of weasel predation on field vole survival was neither sufficient nor necessary to initiate and drive the cyclic decline of field vole populations in Kielder Forest, northern England. They also stated that their findings contradict conclusively the specialist predator hypothesis put forward to explain population cycles of voles in North Europe. Straightforward inferences from Kielder Forest to the northern boreal zone are misleading, because the population cycles of voles in Kielder Forest differ essentially from North European vole cycles. The low amplitude of the vole cycles in Kielder Forest, their restricted spatial synchrony in comparison to northern Europe and the virtual lack of interspecific synchrony in Kielder Forest suggest that there are essential differences between the mechanisms responsible for the two types of cyclic fluctuations of voles. The weasel‐reduction experiment may provide a misleading picture on the role of predators, even in the Kielder Forest cycle. The experimental reduction of weasels alone may not stop the population decline of voles, because competing larger predators are expected to increase their hunting in the weasel‐reduction areas. The small spatial scale of the experiment, which produced only slight, short‐term differences in weasel densities between reduction and control areas, also suggests that other predators could have compensated easily for the weasels that were removed. We propose a new version of the predation hypothesis to explain low‐amplitude population cycles of voles in temperate Europe, including the Kielder Forest. The interaction between generalist predators and vole populations might account for these cycles because generalists can have a functional response that is destabilizing in the neighbourhood of the equilibrium point. As most generalists are orders of magnitude larger than weasels, and thus need much more food for survival, generalist‐driven cycles should be characterized by high prey minima, as observed in Kielder Forest.

Effects of grazing intensity on small mammal population ecology in wet meadows

Summary Livestock grazing is common management practice in wet grasslands. However, knowledge of its effects on small mammals is limited. We studied the influence of grazing intensity on small mammals in general and field voles Microtus agrestis in particular in two Danish wet meadows, 1998–2000. Generally, grazing livestock had a negative effect on the peak biomass of small mammals, and the negative effect increased with grazing intensity, irrespective of whether pens were grazed by cattle or by sheep. More detailed analyses, however, revealed that an intermediate grazing intensity (approximately 400 kg ha −1 as maximum livestock biomass) actually seemed to benefit small mammals. This grazing intensity generally held small mammal biomasses and field vole population sizes that were similar to or larger than those on the ungrazed control, and markedly larger than those on the more heavily grazed pens. Additionally, field voles in the intermediate grazing intensity had more foetuses. Though a number of parameters may contribute to the observed patterns, we suggest that these primarily are caused by the livestock removing vegetation cover, thereby influencing the number and size of patches with high, dense vegetation in the vicinity of grass that is rejuvenated by grazing.

Population fluctuations of the wood lemmingMyopus schisticolor in eastern and western Finland

Olavi Eskelinen, Pertti Sulkava and Risto Sulkava From 1982 to 2003 we studied fluctuations in populations of the wood lemmingMyopus schisticolor (Liljeborg, 1844) in the Heinavesi (eastern Finland) and Keuruu regions (western Finland) by counting field signs and dead animals in standardized field surveys. We compared the population fluctuations of lemmings to those of other voles, owls and small mustelids in these regions. The lemming population in Heinavesi fluctuated regularly in 3-year cycles and in synchrony with the field vole population. Populations of owls also fluctuated in synchrony with wood lemming and field vole populations. In the Keuruu region, oscillations in the wood lemming population were irregular, and neither lemming and vole populations nor lemming and owl populations were correlated. Although direct mechanistic evidence is lacking, specialist predators such as weasels and owls probably cause the cyclicity in the field vole and wood lemming populations in the Heinavesi area. On the other hand, scarcity of high-quality habitats, unfavourable winter weather conditions and generalist predators may prevent the development of cyclicity in the wood lemming population of Keuruu.

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.

Habitat selection and home range size of field volesMicrotus agrestis in Słowiński National Park, Poland

Habitat preference, home range size and intra-specific overlap were investigated in summer 1998 among field volesMicrotus agrestis (Linnaeus, 1761) in Słowiński National Park (N Poland). Eight individuals (2 females, 6 males) were radio-tracked for one week in August. Field voles were shown to exhibit a marked preference for meadow and the ecotone between grassland and habitats with common reed, while avoiding alder forest and proper reedbeds. No significant differences between night and day in habitat-use of voles were noted. The results suggest that, at the end of the breeding season, it was food resources, rather than the risk of predation, played an important role in the voles’ utilisation of space. The home ranges of males were larger and more diverse than those of females; their sizes being correlated with body mass, such that heavier males had larger home ranges. This further suggests that intra-sexual competition exists between males for females. The low number of females influenced their spatial behaviour, as females had completely exclusive home ranges. Four males (out of six) had overlapping home ranges with other males; three of the overlaps were of less than 20%. Attributes of promiscuity (such as a 3.5:1 operational sex ratio of males to females, intra-sexual competition between males and the territorial exclusivity of females) influenced the social system. However, the period of radio-tracking during this study was too short to define accurately the social system in the field vole population.