Recognition of interspecific familiar versus unfamiliar odours among bank voles and yellow-necked mice

Two experiments (laboratory and field-laboratory) were designed to determine whether individual bank volesClethrionomys glareolus (Schreber, 1780) and yellow--necked miceApodemus flavicollis (Melchior, 1834) could distinguish heterospecific odour cues from familiar and unfamiliar individuals. In the laboratory experiment each male bank vole was familiarized for 24 h with odour (cotton wool impregnated with urine and faeces) of male yellow-necked mice and yellow-necked mice were familiarized with odour of male bank voles. In the field-laboratory experiment the individual bank voles and yellow-necked mice captured at the same point were considered familiar and transfered to the laboratory. In laboratory, these individuals were tested in a box (for 5 h) affording them the choice between the odours of familiar and unfamiliar heterospecific males. Bank voles discriminated between familiar and unfamiliar yellow--necked mouse odours. Male yellow-necked mice seemed to have a similar ability to recognise odours of familiar bank voles. It is proposed that interactions between these two species occur not only on the species level, but also on the level of individual. This phenomenon (probably asymmetric) can play an important role in spatial orientation, and influence direct contacts between individuals of these species.     

Reproduction strategy in an island population of yellow-necked mice

A population of yellow-necked mice, Apodemus flavicollis, inhabiting Crabapple Island (NE Poland) was sampled from 1994–2002. The catch-mark-release method was applied. Sexually mature males and females (including pregnant ones) as well as immatures of each sex were identified. During the study period 3,036 mice were caught 10,672 times. The number of mice caught varied from 6 individuals (April 1999) to 272 (July 1996). The number of both mature females and mature males increased linearly with population size. Differences in the reproductive strategies of yellow-necked mouse and bank voles, Clethrionomys glareolus, are discussed. The respective strategies led to high variability in the population size of mice and much less variability in the case of the voles during the breeding season.     

The effect of heavy metal accumulation on metallothionein content in selected tissues of bank voles and yellow-necked mice caught near a steelworks and zinc smelter

The effect of cadmium, zinc, and copper accumulation on metallothionein content in the selected tissues of bank voles and yellow-necked mice trapped near the Sendzimir Steelworks in Krakow and the zinc smelter in Bukowno were analysed. The Borecka Forest was chosen as a control area. The highest cadmium concentration, 32.98 microg g(-1) dry weight, was detected in the kidneys of the bank voles caught in the Bukowno area. Zinc and copper concentrations in the tissues did not exceed the critical values. Metallothionein content in the liver and kidneys was associated with heavy metal accumulation in the tissues. The highest content of sulphydryl groups was detected in the livers of the bank voles trapped within the neighbourhood of the zinc smelter in Bukowno. The highest level of disulphide bonds was found in the kidneys of the bank voles from the same area.     

Winter breeding in three rodent species, the bank vole Clethrionomys glareolus, the yellow-necked mouse Apodemus flavicollis and the wood mouse Apodemus sylvaticus in southern Sweden

Winter breeding, as judged from heavy reproductive organs in both males and females, was observed in bank voles, yellow-necked mice and wood mice in south Sweden during the winter of 1976–1977. The breeding was probably a result of unusually favourable feeding conditions created by an extremely rich beech mast crop.     

Contrasting patterns of diversity and population differentiation at the innate immunity gene toll-like receptor 2 (TLR2) in two sympatric rodent species

Comparing patterns of diversity and divergence between populations at immune genes and neutral markers can give insights into the nature and geographic scale of parasite-mediated selection. To date, studies investigating such patterns of selection in vertebrates have primarily focused on the acquired branch of the immune system, whereas it remains largely unknown how parasite-mediated selection shapes innate immune genes both within and across vertebrate populations. Here, we present a study on the diversity and population differentiation at the innate immune gene Toll-like receptor 2 (TLR2) across nine populations of yellow-necked mice (Apodemus flavicollis) and bank voles (Myodes glareolus) in southern Sweden. In yellow-necked mice, TLR2 diversity was very low, as was TLR2 population differentiation compared to neutral loci. In contrast, several TLR2 haplotypes co-occurred at intermediate frequencies within and across bank vole populations, and pronounced isolation by distance between populations was observed. The diversity and differentiation at neutral loci was similar in the two species. These results indicate that parasite-mediated selection has been acting in dramatically different ways on a given immune gene in ecologically similar and sympatric species. Furthermore, the finding of TLR2 population differentiation at a small geographical scale in bank voles highlights that vertebrate innate immune defense may be evolutionarily more dynamic than has previously been appreciated.     

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.     

Yellow-necked mice (<Emphasis Type="Italic">Apodemus flavicollis</Emphasis>) and bank voles (<Emphasis Type="Italic">Myodes glareolus</Emphasis>) as zoomonitors of environmental contamination at a polluted area in Slovakia

Background  

Free-living wild rodents are often used as zoomonitors of environmental contamination. In the present study, accumulation of cadmium (Cd), copper (Cu), iron (Fe), and zinc (Zn) in critical organs of yellow-necked mice (Apodemus flavicollis) and bank voles (Myodes glareolus) trapped in a polluted area in Nováky, Slovakia was investigated.     

Comparison of spleen transcriptomes of two wild rodent species reveals differences in the immune response against Borrelia afzelii

Different host species often differ considerably in susceptibility to a given pathogen, but the causes of such differences are rarely known. The natural hosts of the tick‐transmitted bacterium Borrelia afzelii, which is one of causative agents of Lyme borreliosis in humans, include a variety of small mammals like voles and mice. Previous studies have shown that B. afzelii‐infected bank voles (Myodes glareolus) have about ten times higher bacterial load than infected yellow‐necked mice (Apodemus flavicollis), indicating that these two species differ in resistance. In this study, we compared the immune response to B. afzelii infection in these host species by using RNA sequencing to quantify gene expression in spleen. Gene set enrichment analysis (GSEA) showed that several immune pathways were down‐regulated in infected animals in both bank voles and yellow‐necked mice. Moreover, IFNα response was up‐regulated in B. afzelii‐infected yellow‐necked mice, while IL6 signaling and the complement pathway were down‐regulated in infected bank voles; differences in regulation of these three pathways between bank voles and yellow‐necked mice could thus contribute to the difference in resistance to B. afzelii between the species. This study provides knowledge of gene expression induced by a zoonotic pathogen in its natural host, and possible species‐specific regulation of immune responses associated with resistance.     

The Three Subtypes of Tick-Borne Encephalitis Virus Induce Encephalitis in a Natural Host,the Bank Vole (Myodes glareolus)

Tick-borne encephalitis virus (TBEV) infects bank voles (Myodes glareolus) in nature, but the relevance of rodents for TBEV transmission and maintenance is unclear. We infected colonized bank voles subcutaneously to study and compare the infection kinetics, acute infection, and potential viral persistence of the three known TBEV subtypes: European (TBEV-Eur), Siberian (TBEV-Sib) and Far Eastern (TBEV-FE). All strains representing the three subtypes were infective and highly neurotropic. They induced (meningo)encephalitis in some of the animals, however most of the cases did not present with apparent clinical symptoms. TBEV-RNA was cleared significantly slower from the brain as compared to other organs studied. Supporting our earlier findings in natural rodent populations, TBEV-RNA could be detected in the brain for up to 168 days post infection, but we could not demonstrate infectivity by cell culture isolation. Throughout all time points post infection, RNA of the TBEV-FE was detected significantly more often than RNA of the other two strains in all organs studied. TBEV-FE also induced prolonged viremia, indicating distinctive kinetics in rodents in comparison to the other two subtypes. This study shows that bank voles can develop a neuroinvasive TBEV infection with persistence of viral RNA in brain, and mount an anti-TBEV IgG response. The findings also provide further evidence that bank voles can serve as sentinels for TBEV endemicity.     

Movement behaviour of woodland rodents: looking from beyond small trapping grids

Live-trapping of rodents was conducted over a 12-ha plot on unevenly spaced trap lines, with inner lines forming a 3.5-ha grid of closely spaced traps. This design was used to estimate the probability that bank volesClethrionomys glareolus (Schreber, 1780) and yellow-necked miceApodemus flavicollis (Melchior, 1834) trapped in small grids are true residents rather than visitors from the surrounding area. On average, 12% of the voles and 19% of the mice were trapped within and beyond the grid in the same trapping sessions. As these were mainly wide-ranging males moving over the plot, home ranges of males may be underestimated on small grids. In total, 36% of voles and 39% of mice that were marked in spring-summer were trapped at least once in their life beyond the grid. Typically, these were individuals shifting home ranges and migrating to or from the grid. The size of lifetime ranges of rodents was significantly larger than temporary home ranges and may therefore be underestimated on small grids. “Single--capture” individuals were mainly true transients rather than visitors. Only 12% of voles and 15% of mice resided on the plot for longer time than in the grid.     

Between-year variation and spatial dynamics of Cryptosporidium spp. and Giardia spp. infections in naturally infected rodent populations

Prevalence and abundance of Cryptosporidium spp. and Giardia spp. infections were studied over the 8-year period in 3 species of rodents in N.E. Poland (bank vole Myodes glareolus-1523; yellow-necked mouse Apodemus flavicollis- 638; common vole Microtus arvalis- 419). Prevalence was 53.8, 28.1 and 62.3% respectively for Cryptosporidium spp. and 58.3, 24.4 and 74.2% respectively for Giardia spp. Prevalence and abundance of infection varied markedly across 8 years of the study with 1998 and 2002 being years of higher prevalence and abundance, following changes in the densities of host species. The distribution of intestinal protozoa in forest rodents did not vary in the 3 isolated sites during the 4-year study. In the case of Cryptosporidium, fewer older animals carried infection and infections of the oldest bank and common voles were relatively milder. In the case of Giardia in yellow-necked mice, infections were more common in older age classes (2 and 3). The two species showed significant co-occurrence and in animals carrying both species there was a strong significant positive correlation between abundance of infection with each. These data are discussed in relation to the parasite genotypes identified in this region and in respect of the role of various ecological factors in shaping of intestinal protozoa communities.     

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.     

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.     

Mast Pulses Shape Trophic Interactions between Fluctuating Rodent Populations in a Primeval Forest

How different functional responses of consumers exploiting pulsed resources affect community dynamics is an ongoing question in ecology. Tree masting is a common resource pulse in terrestrial ecosystems that can drive rodent population cycles. Using stable isotope (δ¹³C, δ¹⁵N) analyses, we investigated the dietary response of two fluctuating rodent species, the yellow-necked mouse Apodemus flavicollis and the bank vole Myodes glareolus, to mast events in Białowieża Forest (NE Poland). Rodent hair samples were obtained non-invasively from faeces of their predators for an 11-year period that encompassed two mast events. Spectacular seed crops of deciduous trees, namely oak Quercus robur and hornbeam Carpinus betulus, occur after several intermediate years of moderate seed production, with a post-mast year characterised by a nil crop. While a Bayesian isotopic (SIAR) mixing model showed a variety of potential vegetation inputs to rodent diets, the isotopic niche of the yellow-necked mouse was strongly associated with mast of deciduous trees (>80% of diet), showing no variation among years of different seed crop. However, bank voles showed a strong functional response; in mast years the vole shifted its diet from herbs in deciduous forest (∼66% of diet) to mast (∼74%). Only in mast years did the isotopic niche of both rodent species overlap. Previous research showed that bank voles, subordinate and more generalist than mice, showed higher fluctuations in numbers in response to masting. This study provides unique data on the functional response of key pulse consumers in forest food webs, and contributes to our understanding of rodent population fluctuations and the mechanisms governing pulse–consumer interactions.     

The effect of cowpox virus infection on fecundity in bank voles and wood mice.

Although epidemic infectious diseases are a recognized cause of changes in host population dynamics, there is little direct evidence for the effect of endemic infections on populations. Cowpox virus is an orthopoxvirus which is endemic in bank voles (Clethrionomys glareolus), wood mice (Apodemus sylvaticus) and field voles (Microtus agrestis) in Great Britain. It does not cause obvious signs of disease nor does it affect survival, but in this study we demonstrate experimentally that it can reduce the fecundity of bank voles and wood mice by increasing the time to first litter by 20-30 days. The pathogenic mechanisms causing this effect are at present not known, but this finding suggests that natural subclinical infection could have a considerable effect on the dynamics of wild populations.     

Predation on rodents in Białowieza primeval forest, Poland

Autumn and winter predation on bank vole Clethrtonomys glareolus and yellow-necked mouse Apodemus flavicollis was studied in 1985/86-88/89 in an 11 2 km² area of the Bialowieza National Park Rodents regularly increased in numbers from spring to autumn and decreased throughout winter Out of 23 species of predators, the most common were tawny owl Strix aluco (43-57 adult ind 10 km⁻²) weasel Mustela ntvahs (17-27 ind), buzzard Buteo buteo (12-16) and pine marten Martes martes (5-8) Voles and mice were the staple food for two specialists the stoat Mustela erminea and the weasel, and two generahsts the tawny owl and the pine marten The generalists exploited different alternative prey when rodents were scarce tawny owl -amphibians, marten - small mammals, and the red fox Vulpes vulpes - ungulate carcasses and hares The depth of snow and abundance of voles were two major factors shaping the contribution of voles to tawny owl and marten diets No such relationships were found for mice and generalist predators The predation by 8 species (tawny owl, buzzard, marten, weasel, stoat, polecat Mustela putortus fox, and raccoon dog Nyctereutes procyonoides) from 1 October to 15 April in 1986/87, 87/88, and 88/89 was estimated to be on average 28-35 voles and 14-17 mice ha Estimates suggested that three species were responsible for 86-95% of the total predation impact tawny owl (56-71%), weasel (11-21%) and marten (10-15%) The predation impact was similar to the annual decrease in rodent numbers from autumn till spring voles 35 (SD 111) lnds ha^-1in autumn and 8 (SD 2 6) lnds ha^-1in spring, and mice 24 (SD 16 3) mds ha⁻¹ in autumn and 3 (SD 2 5) in spring Predation, therefore, was regarded as the main agent of rodent mortality throughout autumn and winter     

Tick-borne zoonotic bacteria in wild and domestic small mammals in northern Spain

The prevalence and diversity of tick-borne zoonotic bacteria (Borrelia spp., Anaplasma phagocytophilum, Coxiella burnetii, and spotted fever group rickettsiae) infecting 253 small mammals captured in the Basque Country (Spain) were assessed using PCR and reverse line blot hybridization. Trapping sites were selected around sheep farms (study 1, 2000 to 2002) and recreational parks (study 2, 2003 to 2005). The majority of the studied mammals (162) were wood mice (Apodemus sylvaticus), but six other different species were also analyzed: yellow-necked mice (Apodemus flavicollis), shrews (Crocidura russula and Sorex coronatus), bank voles (Clethrionomys glareolus), domestic mice (Mus domesticus), and moles (Talpa europaea). The results showed an infection rate ranging from 10.7% to 68.8%, depending on the small mammal species. One C. russula shrew and one A. sylvaticus mouse gave positive reactions for A. phagocytophilum, and C. burnetii was detected in two domestic mice and one A. sylvaticus mouse in a farm. The DNA of Borrelia spp. was detected in 67 animals (26.5%), most of them presenting positive hybridization with the probe for Borrelia sp. strain R57, the new Borrelia species previously detected in small mammals in our region. Furthermore, a second PCR and reverse line blot hybridization specific for B. burgdorferi sensu lato revealed the presence of Borrelia afzelii in 6.3% of C. glareolus voles and 14.3% of S. coronatus shrews. All small mammals were negative for spotted fever group rickettsiae. These results highlight the relevance of small mammals as reservoirs of some zoonotic bacteria.     

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.     

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.     

Alteration of the chronic wasting disease species barrier by in vitro prion amplification

Chronic wasting disease (CWD) is a transmissible spongiform encephalopathy (TSE) of cervids now detected in 19 states of the United States, three Canadian provinces, and South Korea. Whether noncervid species can be infected by CWD and thereby serve as reservoirs for the infection is not known. To investigate this issue, we previously used serial protein misfolding cyclic amplification (sPMCA) to demonstrate that CWD prions can amplify in brain homogenates from several species sympatric with cervids, including prairie voles (Microtus ochrogaster) and field mice (Peromyscus spp.). Here, we show that prairie voles are susceptible to mule deer CWD prions in vivo and that sPMCA amplification of CWD prions in vole brain enhances the infectivity of CWD for this species. Prairie voles inoculated with sPMCA products developed clinical signs of TSE disease approximately 300 days prior to, and more consistently than, those inoculated with CWD prions from deer brain. Moreover, the deposition patterns and biochemical properties of protease-resistant form of PrP (PrP(RES)) in the brains of affected voles differed from those in cervidized transgenic (CerPrP) mice infected with CWD. In addition, voles inoculated orally with sPMCA products developed clinical signs of TSE and were positive for PrP(RES) deposition, whereas those inoculated orally with deer-origin CWD prions did not. These results demonstrate that transspecies sPMCA of CWD prions can enhance the infectivity and adapt the host range of CWD prions and thereby may be useful to assess determinants of prion species barriers.