The effect of variation in calcium intake on the growth of wood mice and bank voles

Summary Calcium intake by wild rodents varies with season and habitat. This may have important ecological consequences; several studies have suggested that calcium availability may limit growth and reproduction. We studied the effect on growth of varying the calcium intake of captive wood mice Apodemus sylvaticus (L.) and bank voles Clethrionomys glareolus (Schreber 1780). To determine whether effects observed in the laboratory could be detected in free-living animals, we also compared the body weights and lengths of free-living animals on calcium-poor gritstone areas with those of rodents on calcium-rich limestone habitats where the dietary calcium concentration was between 2 and 5 times higher. Captive wood mice fed high calcium (0.87%) diet grew at the same rate as mice fed low calcium (0.30%) diet but continued growing for longer, thereby achieving higher asymptotic weights. In contrast, captive bank voles fed the high calcium diet grew more slowly and had lower asymptotic weights than voles fed the low calcium diet. As expected from the laboratory growth study, the higher calcium intake of free-living wood mice on the limestone was associated with greater body size compared with mice on the gritstone. However, bank voles were also larger on the limestone, even though high calcium intake impaired growth in captive animals. The contrast between wood mice and bank voles in the effects of calcium on growth, the reason why impaired growth may not be apparent in bank voles from calcium-rich habitats and the ecological significance of these results are discussed.     

Cellular acidosis in rodents exposed to cadmium is caused by adaptation of the tissue rather than an early effect of toxicity

Proton (¹H) Nuclear Magnetic Resonance (NMR) spectroscopy was used to investigate the biochemical response of bank voles and wood mice (two wild rodent species frequently found on metal-contaminated sites) to chronic cadmium (Cd) insult. Similar effects, in terms of both metabolic changes (consistent with cellular acidosis) and induced metallothionin (MT) production were observed in all animals. These changes appeared to be an adaptation of the liver to toxic insult rather than onset of a toxic effect, and, in common with previous studies, were more marked in bank voles than wood mice. This may have reflected the greater Cd intake and assimilation of the former but was not explained by differences in concentrations of free (non MT-bound) Cd; concentrations of which were negligible in both voles and mice. Responses to Cd insult were detected in both species even though their bodies contained cadmium concentrations well below the World Health Organisation critical renal concentration of 200 μg/g dry mass.     

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.     

Transmission dynamics of a zoonotic pathogen within and between wildlife host species

The transmission dynamics of the cowpox virus infection have been quantified in two mixed populations of bank voles (Clethrionomys glareolus) and wood mice (Apodemus sylvaticus), through analyses of detailed time-series of the numbers of susceptible, infectious and newly infected individuals. The cowpox virus is a zoonosis which circulates in these rodent hosts and has been shown to have an adverse effect on reproductive output. The transmission dynamics within species is best described as frequency dependent rather than density dependent, contrary to the 'mass action' assumption of most previous studies, both theoretical and empirical. Estimation of a transmission coefficient for each species in each population also allows annual and seasonal variations in transmission dynamics to be investigated through an analysis of regression residuals. Transmission between host species is found to be negligible despite their close cohabitation. The consequences of this for the combining ability of hosts as zoonotic reservoirs, and for apparent competition between hosts, are discussed.     

The effect of varying calcium intake on calcium metabolism in wild rodent species

Calcium is essential for mammals but distributed heterogeneously in the environment and so the calcium content of the diet of wild small mammals can vary with habitat geology. The effect of varying the calcium intake of two wild rodent species, the granivorous wood mouse Apodemus sylvaticus and the herbivorous bank vole Clethrionomys glareolus , was investigated. Wood mice were similar to laboratory rodents in their calcium metabolism. Net calcium gut absorption efficiency was 11–15% in wood mice fed either high (0˙87%) or low (0˙30%) calcium diet. No more than the equivalent of 6% of the ingested calcium load was excreted in urine but this was sufficient to eliminate the equivalent of all the extra calcium absorbed across the gut when mice were fed the high calcium diet. In contrast, mean net calcium gut absorption efficiency in bank voles was high and increased from 28% to 42% when dietary calcium content was tripled. Urine was important for excreting calcium, the equivalent of up to 23% of intake being eliminated by this route. Despite this, bank voles fed the high calcium diet assimilated three times more calcium than voles fed the low calcium diet; this was in direct proportion to the three-fold difference in dietary calcium concentration. Possible implications for wild rodents in calcium-rich and calcium-poor habitats are discussed.     

Inference of cowpox virus transmission rates between wild rodent host classes using space-time interaction

There have been virtually no studies of 'who acquires infection from whom' in wildlife populations, but patterns of transmission within and between different classes of host are likely to be reflected in the spatiotemporal distribution of infection among those host classes. Here, we use a modified form of K-function analysis to test for space-time interaction among bank voles and wood mice infectious with cowpox virus. There was no evidence for transmission between the two host species, supporting previous evidence that they act as separate reservoirs for cowpox. Among wood mice, results suggested that transmission took place primarily between individuals of the opposite sex, raising the possibility that cowpox is sexually transmitted in this species. Results for bank voles indicated that infected females might be a more important source of infection to either sex than are males. The suggestion of different modes of transmission in the two species is itself consistent with the apparent absence of transmission between species.     

Evidence for different bottom-up mechanisms in wood mouse ( Apodemus sylvaticus ) and bank vole ( Myodes glareolus ) population fluctuations in Southern Norway

Animals that feed on forest tree seeds, such as Apodemus mice, increase in number after a mast year. At high latitudes, there is a similar delayed response by Myodes voles to high seed crops of bilberry (Vaccinium myrtillus), but here the mechanism is hypothesised to be increased forage quality, caused by a trade-off between reproduction and defence in the plants. Both Apodemus mice and Myodes voles eat berries, but only the latter feed on bilberry plants. Hence, only Myodes voles are predicted to respond to bilberry peak years. A second prediction is that the effect should last longer than any possible direct impacts of bilberries, because the plants would not be able to rebuild their defence until the succeeding summer. During a 21-year snap-trapping study of small rodents in Southern Norway, the spring population of bank vole (Myodes glareolus) was positively related to a bilberry seed index of the previous year, indicating increased winter survival, whereas the wood mouse (Apodemus sylvaticus) was not affected. Also the succeeding autumn population index of the bank vole was positively related to the bilberry index of the previous year, even when controlling for spring population levels. The wood mouse population responded to mast years of sessile oak (Quercus petraea), whereas seeds of Norway spruce (Picea abies) seemed to have some impact on both species. It is concluded that these rodents are mainly limited from below, but by different mechanisms for the granivorous and the herbivorous species.     

Small mammal populations in relation to hedgerow structure in an arable landscape

The population ecology of small mammals in hedgerows in arable farmland in eastern England is described. Features of hedgerows of importance to individual species are examined. Some 97% of the total 3042 mammals captured were wood mouse Apodemus sylvaticus , yellow-necked mouse Apodemus flavicollis , bank vole Clethrionomys glareolus and common shrew Sorex araneus . Small numbers of harvest mice Micromys minutus , field voles Microtus agrestis , pygmy shrews Sorex minutus and water shrews Neomys fodiens were also caught. Wood mouse, the most numerous species, showed a typical pattern of large numbers in autumn and winter, followed by a simultaneous decline over all hedges in early spring. Population changes were less clear in yellow-necked mouse and bank vole but the yellow-necked mouse was more scarce in the second year of study. Common shrews were most numerous in summer and declined rapidly in autumn. Hedgerow coppicing had a marked effect on yellow-necked mouse numbers but not on wood mouse. In an extensive survey of mammal numbers in relation to hedgerow features, ground cover was found to be the single largest factor influencing size of bank vole populations. Hedgerow condition (lack of gaps) was important to yellow-necked mice, which thrived only in well-established hedgerows. Wood mice appeared little influenced by the characteristics of the hedge. Common shrews were more abundant in hedgerows with adjacent permanent water.     

Spatiotemporal dynamics of Puumala hantavirus in suburban reservoir rodent populations

The transmission of pathogens to susceptible hosts is dependent on the vector population dynamics. In Europe, bank voles (Myodes glareolus) carry Puumala hantavirus, which causes nephropathia epidemica (NE) in humans. Fluctuations in bank vole populations and epidemics in humans are correlated but the main factors influencing this relationship remain unclear. In Belgium, more NE cases are reported in spring than in autumn. There is also a higher incidence of human infections during years of large vole populations. This study aimed to better understand the link between virus prevalence in the vector, vole demography, habitat quality, and human infections. Three rodent populations in different habitats bordering Brussels city, Belgium, were studied for two years. The seroprevalence in voles was influenced first by season (higher in spring), then by vole density, vole weight (a proxy for age), and capture site but not by year or sex. Moreover, voles with large maximal distance between two captures had a high probability for Puumala seropositivity. Additionally, the local vole density showed similar temporal variations as the number of NE cases in Belgium. These results showed that, while season was the main factor influencing vole seroprevalence, it was not sufficient to explain human risks. Indeed, vole density and weight, as well as the local habitat, were essential to understanding the interactions in these host‐pathogen dynamics. This can, in turn, be of importance for assessing the human risks.     

Traditional and diversified crops in South Moravia (Czech Republic): Habitat preferences of common vole and mice species

Substantial changes in the composition of crops in Central Europe during the last two decades (increasing areas of maize, rape and sunflower fields) have significantly influenced the structure and dynamics of animal communities, though there is a lack of data available for small rodents. In this study, we assessed the importance of these three crops for rodents and compared it with traditional crops (alfalfa, barley, wheat). We observed that herbivorous species (especially the common vole) do not live in crops which do not have green leaves near the ground (e.g. sunflower, maize), while mobile granivorous species can inhabit all types of crop. We confirmed the presumed differences in habitat preferences; however we rejected the hypothesis of a general increase of rodent abundance during the vegetative season in managed fields. We found that (1) maize and sunflower had no importance for common voles, but they were favored habitats for wood mice; (2) numbers of wood mice in rape decreased during the season, while abundances of common voles increased; (3) common vole populations tended to increase during the season in all suitable crops (alfalfa, barley, wheat, tendency in maize and rape); (4) wood mice populations seemed stable in all crops; i.e. without a seasonal increase. It can be concluded that even if the new crop fields are an important part of the agricultural landscape, they are only a temporal habitat for small mammals, especially granivorous species.     

The dynamics of murid gammaherpesvirus 4 within wild, sympatric populations of bank voles and wood mice

Murid gammaherpesvirus 4 (MuHV-4) is widely used as a small animal model for understanding gammaherpesvirus infections in man. However, there have been no epidemiological studies of the virus in wild populations of small mammals. As MuHV-4 both infects cells associated with the respiratory and immune systems and attempts to evade immune control via various molecular mechanisms, infection may reduce immunocompetence with potentially serious fitness consequences for individuals. Here we report a longitudinal study of antibody to MuHV-4 in a mixed assemblage of bank voles (Clethrionomys glareolus) and wood mice (Apodemus sylvaticus) in the UK. The study was conducted between April 2001 and March 2004. Seroprevalence was higher in wood mice than bank voles, supporting earlier work that suggested wood mice were the major host even though the virus was originally isolated from a bank vole. Analyses of both the probability of having antibodies and the probability of initial seroconversion indicated no clear seasonal pattern or relationship with host density. Instead, infection risk was most closely associated with individual characteristics, with heavier males having the highest risk. This may reflect individual variation in susceptibility, potentially related to variability in the ability to mount an effective immune response.     

Predation rate, prey preference and predator switching: experiments on voles and weasels

We studied the predation rate and prey selection of the least weasel ( Mustela nivalis nivalis ) on its two most common prey species in boreal environments, the bank vole ( Clethrionomys glareolus ) and the field vole ( Microtus agrestis ), in large outdoor enclosures. We also studied the response of weasels to odours of the two species in the laboratory. The enclosure experiment was conducted using constant vole densities (16 voles/ha) but with varying relative abundance of the two species. Weasels showed higher predation rates on bank voles, and males had higher predation rate than females. Females killed disproportionately more of the more abundant prey species, but they preferred bank voles to field voles when both were equally available. Overall, the predation rate also increased with increasing abundance of bank voles. Therefore our results are in agreement with earlier laboratory results showing preference for bank voles, even if no intrinsic preference for odours of either species was observed in our laboratory study. We suggest that the least weasel hunts according to prey availability, prey aggregation and suitability of hunting habitat, and that this causes the observed dependence of least weasels on field voles and emphasises the role of the field vole in the vole-weasel interaction in cyclic vole populations. Furthermore, our results suggest that predation by weasels may facilitate the coexistence of the two vole species via predator switching, and that it may cause the observed synchrony in dynamics between vole species.     

Infection intensity and infectivity of the tick-borne pathogen Borrelia afzelii

The 'trade-off' hypothesis for virulence evolution assumes that between-host transmission rate is a positive and saturating function of pathogen exploitation and virulence, but there are as yet few tests of this assumption, in particular for vector-borne pathogens. Here, I show that the infectivity (probability of transmission) of the tick-borne bacterium Borrelia afzelii from two of its natural rodent hosts (bank vole and yellow-necked mouse) to its main tick vector increases asymptotically with increasing exploitation (measured as bacterial load in skin biopsies). Hence, this result provides support for one of the basic assumptions of the 'trade-off hypothesis'. Moreover, there was no difference in infectivity between bank voles and yellow-necked mice despite bacterial loads being on average an order of magnitude higher in bank voles, most likely because ticks took larger blood meals from mice. This shows that interspecific variation in host resistance does not necessarily translate into a difference in infectivity.     

Reasons for arboreality in wood mice Apodemus sylvaticus and Bank voles Myodes glareolus

Although it is broadly accepted that small mammals often climb trees, only few studies explore arboreality in woodland rodents systematically. Here, we investigate the three-dimensional habitat use of wood mice Apodemus sylvaticus and bank voles Myodes glareolus at three different sites in Wytham Woods, Oxfordshire, under varying environmental conditions. A total of 12 trapping sessions was carried out between March and September 2003 and 2004. During each session, 100 Longworth live-traps with shrew escape holes were set in a 25-point-grid for 3 succeeding nights. Each time, 50 traps were placed on the ground, and 50 in surrounding trees at heights of 30–250 cm. Wood mice were significantly more arboreal than bank voles, and male wood mice spent significantly more time in trees than did females. Arboreality in bank voles occurred only under high population densities and food shortage, and both species were significantly more arboreal in woodland with dense understorey. Thus we conclude that while arboreality is predominantly a result of inter- and intra-specific competition, of the two species we studied, only wood mice, being more agile, can afford to utilize trees without getting caught by predators, and that sex differences are due to male territoriality. Estimates of population sizes and distribution, as well as studies of inter-specific interactions and socio-spatial behaviour are presumed to be affected by these results, and are currently likely to underestimate rodent numbers considerably.     

Infection with cowpox virus decreases female maturation rates in wild populations of woodland rodents

Sublethal effects of parasitic infection, such as reductions in reproductive rate, can significantly affect host population dynamics. Here we show that in wild populations of both Clethrionomys glareolus (bank vole) and Apodemus sylvaticus (wood mouse), females infected with cowpox virus are likely to delay maturation and therefore reproduction – in most cases until the following breeding season. Some infected bank voles do mature in their year of birth but still take longer than uninfected females. Together with our previous demonstration that individuals infected with cowpox virus in the summer survive better than uninfected individuals, these results support the prediction that hosts that develop an acute infection may best optimise their fitness by decreasing current reproduction to maximise the probability of surviving infection. Moreover, as the proportion of individuals infected increases with density, the reduction in host fecundity may have significant consequences for host dynamics.     

Infestation of mammals by Ixodes ricinus ticks (Acari: Ixodidae) in south-central Sweden

Infestation by Ixodes ricinus ticks on rodents, hares and cervids was examined at Bogesund, 10 km north of Stockholm, in south-central Sweden during 1991-1994 and on varying hares (Lepus timidus) at Stora Karlso and Gotska Sandon in the Baltic Sea during 1992-1993. At Bogesund, there were great differences between two consecutive years in the number of I. ricinus larvae infesting bank voles (Clethrionomys glareolus). The seasonal pattern of infestation by I. ricinus larvae and nymphs on bank voles was unimodal in 1991, with peaks in June-July and bimodal in 1992, with peaks in June and August. Male bank voles, compared to females and older voles, compared to young voles, harboured greater numbers of I. ricinus ticks. Apodemus mice, compared to bank voles, harboured greater numbers of I. ricinus ticks. Ixodes ricinus larvae engorged on Apodemus mice were heavier than larvae engorged on bank voles and resulted in larger nymphs. However, there was no difference in the proportions of viable nymphs resulting from larvae engorged on mice or voles. The ranges in the numbers of I. ricinus ticks infesting individual hosts were 1-451 for rodents, 16-2374 for hares and 428-2072 for roe deer (Capreolus capreolus). These ranges of tick numbers are estimated to represent potential blood losses from individual hosts of approximately 0.2-65% for rodents, 0.2-13% for hares and 0.3-9.0% for roe deer. Within the populations of all host species examined, the distributions of all stages of I. ricinus were clumped, with most host individuals harbouring few ticks and only a few individuals harbouring many ticks. The data suggest that, even though a small proportion of tick hosts may be severely affected, the direct effects of feeding by I. ricinus are unlikely to play an important role on mammal population dynamics.     

Dermatophytes in a population of bank voles and woodmice

A population of bank voles (Clethrionomys glareolus) and wood mice (Apodemus sylvaticus) inhabiting an oak wood in Somerset was examined for dermatophytes at monthly intervals for 2 years. The marked animals were frequently retrapped, allowing a study of host fungus relationship over a period of time. Microsporum persicolor (Sabouraud) Guiart er Grigorakis and Trichophyton mentagrophytes (Robin) Blanchard were isolated from both animal species, but M. persicolor predominated in bank voles and T. mentagrophytes in wood mice. In their most favoured host, both dermatophyte species often persisted for several months, but in the less favoured host they were never isolated at more than one sampling. Males of both animal species were infected more often than females.The existing evidence for the geophilic nature of both fungi is reviewed and shown to be very weak, especially for M. persicolor.This is the first report from Great Britain of T. mentagrophytes infection of wood mice not in contact with human habitation.     

Prion protein amino acid determinants of differential susceptibility and molecular feature of prion strains in mice and voles

The bank vole is a rodent susceptible to different prion strains from humans and various animal species. We analyzed the transmission features of different prions in a panel of seven rodent species which showed various degrees of phylogenetic affinity and specific prion protein (PrP) sequence divergences in order to investigate the basis of vole susceptibility in comparison to other rodent models. At first, we found a differential susceptibility of bank and field voles compared to C57Bl/6 and wood mice. Voles showed high susceptibility to sheep scrapie but were resistant to bovine spongiform encephalopathy, whereas C57Bl/6 and wood mice displayed opposite features. Infection with mouse-adapted scrapie 139A was faster in voles than in C57Bl/6 and wood mice. Moreover, a glycoprofile change was observed in voles, which was reverted upon back passage to mice. All strains replicated much faster in voles than in mice after adapting to the new species. PrP sequence comparison indicated a correlation between the transmission patterns and amino acids at positions 154 and 169 (Y and S in mice, N and N in voles). This correlation was confirmed when inoculating three additional rodent species: gerbils, spiny mice and oldfield mice with sheep scrapie and 139A. These rodents were chosen because oldfield mice do have the 154N and 169N substitutions, whereas gerbil and spiny mice do not have them. Our results suggest that PrP residues 154 and 169 drive the susceptibility, molecular phenotype and replication rate of prion strains in rodents. This might have implications for the assessment of host range and molecular traceability of prion strains, as well as for the development of improved animal models for prion diseases.     

Beyond the Mediterranean peninsulas: evidence of central European glacial refugia for a temperate forest mammal species, the bank vole (Clethrionomys glareolus)

This study details the phylogeographic pattern of the bank vole, Clethrionomys glareolus, a European rodent species strongly associated with forest habitat. We used sequences of 1011 base pairs of the mitochondrial DNA cytochrome b gene from 207 bank voles collected in 62 localities spread throughout its distribution area. Our results reveal the presence of three Mediterranean (Spanish, Italian and Balkan) and three continental (western, eastern and 'Ural') phylogroups. The endemic Mediterranean phylogroups did not contribute to the post-glacial recolonization of much of the Palaearctic range of species. Instead, the major part of this region was apparently recolonized by bank voles that survived in glacial refugia in central Europe. Moreover, our phylogeographic analyses also reveal differentiated populations of bank voles in the Ural mountains and elsewhere, which carry the mitochondrial DNA of another related vole species, the ruddy vole (Clethrionomys rutilus). In conclusion, this study demonstrates a complex phylogeographic history for a forest species in Europe which is sufficiently adaptable that, facing climate change, survives in relict southern and northern habitats. The high level of genetic diversity characterizing vole populations from parts of central Europe also highlights the importance of such regions as a source of intraspecific genetic biodiversity.