Microtus Agrestis Research Articles

Changes in size of Baltic field voles over the last 50 years: are they really shrinking?

Using museum materials and recently trapped specimens of field voles (Microtus agrestis (Linnaeus, 1761)) from Lithuania and Estonia, we assessed temporal and latitudinal trends in body and skull size, comparing the periods 1980–1996 and 2014–2016. We measured four body and 23 skull characters, size-adjusting them using the geometric mean procedure. A pronounced decrease in the size of M. agrestis was noted in Estonia, where 23 out of 27 adjusted body and skull characters had decreased by up to 21.9%, with only the tail length, hind foot length, maximum height of mandibula excluding coronoid process and coronoid height of mandibula increasing significantly. Decreases were less marked in voles from Lithuania – most pronounced were a 6.1% decrease in adjusted body length, an 11.6% decrease in adjusted length of the braincase, a 3.85% decrease in the breadth of the braincase, measured at the widest part, a 2.9% decrease in condylobasal skull length and a 2.2% decrease in the height of the braincase. The coronoid height of the mandibula of Lithuanian individuals showed an 8.4% size increase. In both countries, the confounding effect of sex on the size changes of M. agrestis from 1980 to 2016 was much smaller than the effect of time period. Concluding, voles in Estonia became significantly smaller, while changes in the measured characters in Lithuania were heterogeneous.

A candidate tolerance gene identified in a natural population of field voles (Microtus agrestis).

The animal immune response has hitherto been viewed primarily in the context of resistance only. However, individuals can also employ a tolerance strategy to maintain good health in the face of ongoing infection. To shed light on the genetic and physiological basis of tolerance, we use a natural population of field voles, Microtus agrestis, to search for an association between the expression of the transcription factor Gata3, previously identified as a marker of tolerance in this system, and polymorphism in 84 immune and nonimmune genes. Our results show clear evidence for an association between Gata3 expression and polymorphism in the Fcer1a gene, with the explanatory power of this polymorphism being comparable to that of other nongenetic variables previously identified as important predictors of Gata3 expression. We also uncover the possible mechanism behind this association using an existing protein-protein interaction network for the mouse model rodent, Mus musculus, which we validate using our own expression network for M. agrestis. Our results suggest that the polymorphism in question may be working at the transcriptional level, leading to changes in the expression of the Th2-related genes, Tyrosine-protein kinase BTK and Tyrosine-protein kinase TXK, and hence potentially altering the strength of the Th2 response, of which Gata3 is a mediator. We believe our work has implications for both treatment and control of infectious disease.

Digesta kinetics in two arvicoline rodents, the field vole (Microtus agrestis) and the steppe lemming (Lagurus lagurus)

A large number of small mammals practice cecotrophy, i.e. ingesting a certain fraction of their own faeces typically termed ‘cecotrophs’. This behaviour is generally thought to limit metabolic losses of nitrogen, because a colonic separation mechanism (CSM) selectively accretes fine, nitrogen-rich particles (such as microbes) in the cecotrophs. Two types of CSM have been described, a wash-back CSM (in lagomorphs) where fluids wash through the colonic digesta in a retrograde manner into the caecum, resulting in a selectively prolonged solute marker retention in passage studies; and a mucus-trap CSM (in hystricomorph rodents) where microbes are trapped in mucus-filled anatomical structures in the colon mucosa (grooves/furrows/folds). In the mucus-trap CSM, no selective retention of any passage marker occurs. How the CSM operates in muroid rodents is not well explored, but both mucus-filled anatomical structures and a moderate degree of selective solute marker retention have been reported in the literature. Here we demonstrate selective solute marker retention in two muroid, arvicoline rodent species (field voles Microtus agrestis, body mass 28.6 ± 7.4 g, and steppe lemming Lagurus lagurus, 19.8 ± 2.0 g) on a pelleted high-fibre diet, where a solute marker was retained 20–55% longer than a particle marker (with mean retention times of 5.6 ± 0.5 vs. 4.8 ± 0.9 and 5.0 ± 1.5 vs. 3.3 ± 0.9 h, respectively). The animals achieved an apparent organic matter digestibility similar to that of much larger herbivores on diets of similar fibre content. In addition to a selective feeding behaviour and a high relative food intake, a digestive physiology that includes coprophagy, and a CSM using both mucus-trap and wash-back effects, are characteristic for herbivorous arvicoline rodents. The relative contributions of the two CSM components – whether they have additive or complementary effects – remain to be explored.

Los micromamíferos (Eulipotyphla, Chiroptera, Rodentia y Lagomorpha) del yacimiento del Pleistoceno Superior de la cueva de El Castillo (Cantabria, España)

El material de micromamíferos del yacimiento del Pleistoceno Superior de la cueva de El Castillo, objeto de estudio detallado en este trabajo, proviene de los niveles auriñacienses 18b y 18c (datados en 40.000-45.000 BP), nivel 19, y niveles musterienses 20b, 20c, 20d, 20e (datados en 41.000-49.000 BP), 21a y 21b. La asociación de micromamíferos es la siguiente: Erinaceus europaeus, Crocidura russula, Sorex coronatus, Sorex minutus, Neomys fodiens, Talpa europaea, Galemys pyrenaicus, cf. Miniopterus schreibersii, Chiroptera indet., Pliomys lenki, Microtus arvalis – Microtus agrestis, Microtus lusitanicus, Microtus oeconomus, Chionomys nivalis, Arvicola terrestris, Apodemus sylvaticus – Apodemus flavicollis y Lepus sp. La mayoría de estas especies están presentes en la fauna actual de Cantabria, excepto Pliomys lenki que se extinguió en el último tercio del Pleistoceno Superior, y Microtus oeconomus, que persistió en la península ibérica durante el Holoceno bien avanzado hasta su desaparición en tiempos históricos, y que actualmente está en regiones euroasiáticas más septentrionales. Hay una gran continuidad de la gran mayoría de los taxones en todos los niveles. La fauna en su conjunto parece indicar un medio predominantemente abierto, por lo general de praderas húmedas (y en mucha menor medida praderas secas) con una buena cobertura vegetal a nivel del suelo, en el que habría también algunas zonas arboladas o boscosas, y algún curso de agua. Los indicadores termófilos son escasos y poco abundantes, lo que podría indicar que el clima podría ser algo menos templado que en otros periodos del Pleistoceno Superior y quizás también que actualmente en la zona.

Биотопическое распределение тёмной полёвки Microtus agrestis на юго-восточной границе ареала

Биотопическое распределение тёмной полёвки Microtus agrestis на юго-восточной границе ареала

Which species of small mammals tolerate highly urbanized areas – the study in Warsaw agglomeration and surroundings

The degree of penetration of urban habitats by small terrestrial mammals was studied in Warsaw agglomeration and in adjacent areas up to 50 km from the city centre. Study material consisted of pellets of the tawny owl Strix aluco collected in 85 sites, which contained 15,152 remains of individuals of small mammals. The species that penetrated city agglomeration most intensively were: Apodemus agrarius, Mus musculus, Talpa europaea, Rattus norvegicus and Microtus subterraneus. Most central sites of these species were situated 1.3–2.3 km from the city centre. Microtus agrestis, Mustela nivalis, Arvicola amphibius, Neomys fodiens, Muscardinus avellanarius and Sicista betulina showed the lowest degree of penetration of an urban agglomeration (sites closest to the city centre: 8.2, 8.6, 8.6, 11.2, 17.8 and 20.2 km, respectively). Species, whose share among the owls’ prey decreased most with the distance from the city centre, were: A. agrarius and T. europaea. The reverse pattern was found for M. agrestis and M. avellanarius. Small terrestrial mammals are sensitive to the proceeding urbanization and the central part of Warsaw agglomeration is penetrated by only 1/3 of species of the local fauna.

Microtus arvalis and Arvicola scherman: Key Players in the Echinococcus multilocularis Life Cycle.

A broad range of rodent species are described as potential intermediate hosts for Echinococcus multilocularis, a wide-spread zoonotic cestode causing alveolar echinococcosis. However, little is known about the relative contribution of these species for parasite reproduction and the maintenance of its life cycle. In a comparative study in a high endemic region in Zurich, Switzerland, we investigated prevalence rates and fertility of E. multilocularis in the most abundant vole species as well as the predation rate of foxes on these species. To ensure that the fox families had access to different vole species and that these voles were exposed to the same environmental contamination with parasite eggs, we selected eight study plots where at least two rodent species co-occurred. The parasite prevalence in Microtus arvalis [11.0%, confidence intervals (CI) 8.9–13.4] was significantly higher than in Arvicola scherman (5.3%, 3.9–7.1) and Myodes glareolus (3.9%, 2.0–6.7). None of the, only 29 individuals of, Microtus agrestis was infected (0%, 0.0–9.8) and the species was excluded for further analyses. Logistic regression models for the prevalences revealed significant differences between nearby study plots and higher infection rates for females, heavier individuals, and individuals trapped during spring, when the prevalence in M. arvalis peaked up to 65% (CI 50–79) in one plot. Furthermore, we detected significantly higher percentages of fertile infections in M. arvalis and M. glareolus than in A. scherman (OR 11.2 and 6.4, respectively) and a significantly higher protoscolex number in M. glareolus (median 100,000) than in M. arvalis (13,500) and A. scherman (4,290). The most abundant fox prey remains were of the genera Microtus (12.3%, CI 8.4–17.2) and Arvicola (11.5%, 7.7–16.3), whereas Myodes was never recorded as prey (0.0–1.3%). We conclude that M. arvalis and to a lesser extent A. scherman can be regarded as key intermediate hosts in Western and Central European high-endemic regions whereas M. glareolus and M. agrestis play a marginal role. We, therefore, postulate that distribution models of these species could contribute to predict parasite occurrence on a more detailed spatial scale than models of the distribution of foxes which have a very broad and uniform distribution.

Diagnostic Criteria for Identification of Microtus s. l. Species (Rodentia, Arvicolidae) of the Ukrainian Carpathians

Abstract The present paper deals with the issues of diagnostics of morphologically similar vole species (Microtus s. l.) common in the fauna of the Ukrainian Carpathians. Three groups of characters have been analysed: external traits (linear body dimensions, coloration features, etc.), morphological and anatomical features of the skull (size of its structures, form of certain bones and sutures, etc.), and morphology of molar teeth (number and form of enamel lobes and triangles). The analysis of museum specimens of voles collected in the region of the Ukrainian Carpathians has shown that external and cranial non-metric characters allow reliable identification to genus level, while for species diagnostics it is necessary to use a complex of characters including structural features of molars and dimensions of skull structures. The height and width of the braincase have the largest diagnostic value among cranial characters for the sibling species complex Terricola subterraneus–Terricola tatricus, while for the pair of morphologically similar species Microtus agrestis–Microtus arvalis such value have the upper molars length, condylobasal length, and braincase height. The most significant, revised and newly described, diagnostic characters have been generalized into an identification key, especially convenient for use during work with collection materials.

Mammals in the diet of tawny owlStrix alucoin western part of Skierniewice Forest District (central Poland)

AbstractThe aim of the study was to describe the species diversity of small mammals in the western part of the Skierniewice Forest District (Central Poland) using tawny owl (Strix aluco) pellets. The landscape itself is a field and forest mosaic with small forest complexes. Four forest complexes with an area between 70 and 750 ha and surrounded by arable lands as well as loosely scattered buildings were chosen to carry out our work in. Owl pellets were collected in the years 2014–2016 and examined for small mammal remains employing standard protocols.Altogether, we identified 963 items belonging to 17 different mammalian prey species. The most numerous was the yellow-necked mouse,Apodemus flavicollis, which accounted for 33.5% of all identified items. As the second most important group, voles (Microtusspp.) accounted for 12.8% of all identified mammals. Unfortunately, we were unable to find species considered rare in central Poland, i.e. hazel dormouse,Muscardinus avellanarius, European water vole,Arvicola amphibiusand field vole,Microtus agrestis.In overall, the species composition of small mammal assemblages in the studied area was similar to adjacent regions.

Applying a biocomplexity approach to modelling farmer decision‐making and land use impacts on wildlife

Abstract The biocomplexity approach refers to a fully integrated social‐ecological systems (SES) simulation that represents bidirectional feedbacks between social and ecological components. This method is essential to accurately assess impacts of economy and policy on SES such as agroecosystems, where feedbacks between the drivers and impacts of cropping changes need to be simulated. Here we exemplify the biocomplexity approach using energy maize, which is becoming an important source of bioenergy in Europe, and thus, might cause a significant change in land use with knock on‐effects for wildlife. The integrated simulation tool consisted of a farmer decision‐making agent‐based model fully coupled to the Animal Landscape and Man Simulatin System (ALMaSS), an agent‐based simulation system for predicting impacts of land use on a range of Danish wildlife species: the brown hare (Lepus europaeus), the grey partridge (Perdix perdix), the skylark (Alauda arvensis), a carabid beetle (Bembidion lampros), a linyphiid spider (Erigone atra) and the field vole (Microtus agrestis). This was used to assess the impacts of increasing demand on energy maize on the six animal species. Two types of experimental scenarios were evaluated, with and without feedback between the social and ecological system. The assessment of species responses was based on changes in population size, abundance and occupancy. The response to the cultivation of energy maize was negative for three vertebrate species (skylark, hare and field vole) and positive for partridge and the two invertebrate species. The feedback scenarios showed that the incorporation of information from ecological system to the farmer decision‐making affected both a trend in area cultivated with energy maize as well as the animal responses. Synthesis and applications. Fully coupling agent‐based decision‐making and environmental simulation allows a detailed representation and integration of both social and ecological components of agricultural systems at proper spatial and temporal scales as well as of dynamic feedbacks between the two systems. By employing easy to interpret measures of changes in abundance and spatial occupancy of animal species, the simulation results could inform and simplify decision‐making on expected impacts of economy and policy regulations on wildlife.

Long-term changes of small mammal communities in heterogenous landscapes of Central Europe

Long-term dynamics of small mammal communities are perennial themes in population ecology. However, comprehensive studies on the effect of environmental factors on population dynamics are still rare. Here, we aimed to analyze long-term data on Central European communities of small mammals occurring in two habitats that greatly differed in their structure, successional stages, and forest management. We found a richer community structure in young spruce plantations compared to mature European beech forests. In young spruce plantations, Myodes glareolus and Apodemus flavicollis abundances increased and Sorex araneus abundances decreased during the study period as a result of forest growth and management. Community structure in mature beech forests did not change significantly during the study period. Apodemus flavicollis and Myodes glareolus showed 3- and 5-year population cycles, respectively, and their abundances were simultaneously positively correlated with relative abundance of masts. Weather also played a role, while the effect of snow cover was pronounced only in mountain areas where it negatively affected Microtus agrestis and Sorex araneus abundances, temperature positively and rainfall negatively influenced Myodes glareolus and Apodemus flavicollis abundances across both studied habitats. Our findings document that a complex of environmental factors significantly affects the structure and dynamics of small mammal communities in Central Europe, and both local biotic and abiotic factors should be considered in future studies.

Patterns of vole gnawing on saplings in managed clearings in Central European forests

Abstract Sustainable management of European forests aims to ensure economic targets (timber production) as well as ecological aims of the forest (maintenance of biodiversity). Smaller-sized clear-cutting followed by artificial planting creates a mosaic of small forest patches suitable for many small mammals including three possible pest species – the bank vole (Clethrionomys glareolus), the field vole (Microtus agrestis) and the common vole (Microtus arvalis). The vole gnawing pattern was studied on a number of small-sized clearings (up to 2 hectares) situated in managed forests in the Czech Republic (Central Europe). Damage by voles gnawing occurred almost in all study areas; mostly damaged were saplings on clearings at the age up to 5 years after planting, with herb layer dominated by grasses and situated above 700 m a.s.l. The field vole was identified as the main pest species and its density was identified as the most important predictor of gnawing occurrence even though its density on clearings was usually lower than that of the bank vole. Gnawing by voles caused direct mortality of saplings to a greater degree than other biotic factors including deer fraying and browsing; however, saplings were able to repress the effect of gnawing by natural re-grow of bark and the majority of damaged saplings survived, even though with significant stem deformations. While strong inter-annual variation in damage rate is reported in northern Europe, damage rates in Central European managed forests are lower (at about 3.5% per annum) but more consistent with only moderate inter-annual variation. As a result, despite the relatively low rate of damage which may occur in any given year, damage levels can accumulate over several years after planting with significant economic implications for forestry management.

Seasonal shift of diet in bank voles explains trophic fate of anthropogenic osmium?

Diet shifts are common in mammals and birds, but little is known about how such shifts along the food web affect contaminant exposure. Voles are staple food for many mammalian and avian predators. There is therefore a risk of transfer of contaminants accumulated in voles within the food chain. Osmium is one of the rarest earth elements with osmium tetroxide (OsO4) as the most toxic vapor-phase airborne contaminant. Anthropogenic OsO4 accumulates in fruticose lichens that are important winter food of bank voles (Myodes glareolus). Here, we test if a) anthropogenic osmium accumulates in bank voles in winter, and b) accumulation rates and concentrations are lower in autumn when the species is mainly herbivorous. Our study, performed in a boreal forest impacted by anthropogenic osmium, supported the hypotheses for all studied tissues (kidney, liver, lung, muscle and spleen) in 50 studied bank voles. In autumn, osmium concentrations in bank voles were even partly similar to those in the graminivorous field vole (Microtus agrestis; n=14). In autumn but not in late winter/early spring, osmium concentrations were generally negatively correlated with body weight and root length of the first mandible molar, i.e. proxies of bank vole age. Identified negative correlations between organ-to-body weight ratios and osmium concentrations in late winter/early spring indicate intoxication. Our results suggest unequal accumulation risk for predators feeding on different cohorts of bank voles.

Patterns of variation in Microtus arvalis and Microtus agrestis populations from Middle to Late Pleistocene in southwestern Europe

Fifteen paired fossil populations of Microtus arvalis and Microtus agrestis from southwestern Europe have been analysed from a morphological and morphometric point of view. The sites under consideration are located in the northern Iberian Peninsula and southern France, from the Middle Pleistocene to the end of the Late Pleistocene. The aim of this study is to stress once again the importance of keeping these two species separated in the fossil record in order to recognize specific trends of evolution and divergence and to obtain more precise information on palaeoclimatic and palaeoenvironmental conditions. It was possible to observe remarkable intraspecific differences between Middle and Late Pleistocene populations of both species. Furthermore, in synchronic co-specific populations from the Late Pleistocene, climatic and geographic conditions seem to exert a major influence in shaping intraspecific changes in dental pattern.

Laelapidae mites (Acari: Mesostigmata) infesting small rodents in the Curonian Spit, Lithuania

Laelapidae (Acari, Mesostigmata) mites are ecologically diverse and involve predators and parasites found in various habitats. In the present study, Laelapidae mites were collected from 236 small rodents of five species (the yellow-necked mouse Apodemus flavicollis, the harvest mouse Micromys minutus, the bank vole Myodes glareolus, the root vole Microtus oeconomus, and the field vole Microtus agrestis) in the Curonian Spit in 2013–2014. Five species of Laelapidae mites – Laelaps agilis, Hyperlaelaps microti, Haemogamassus nidi, Eulaelaps stabularis and Myonyssus gigas – were identified based on the morphological characters of adult females and males. The present study is the first detection of Laelapidae mites parasitizing small rodents in the Curonian Spit, Lithuania.

Intrachromosomal Rearrangements in Rodents from the Perspective of Comparative Region-Specific Painting.

It has long been hypothesized that chromosomal rearrangements play a central role in different evolutionary processes, particularly in speciation and adaptation. Interchromosomal rearrangements have been extensively mapped using chromosome painting. However, intrachromosomal rearrangements have only been described using molecular cytogenetics in a limited number of mammals, including a few rodent species. This situation is unfortunate because intrachromosomal rearrangements are more abundant than interchromosomal rearrangements and probably contain essential phylogenomic information. Significant progress in the detection of intrachromosomal rearrangement is now possible, due to recent advances in molecular biology and bioinformatics. We investigated the level of intrachromosomal rearrangement in the Arvicolinae subfamily, a species-rich taxon characterized by very high rate of karyotype evolution. We made a set of region specific probes by microdissection for a single syntenic region represented by the p-arm of chromosome 1 of Alexandromys oeconomus, and hybridized the probes onto the chromosomes of four arvicolines (Microtus agrestis, Microtus arvalis, Myodes rutilus, and Dicrostonyx torquatus). These experiments allowed us to show the intrachromosomal rearrangements in the subfamily at a significantly higher level of resolution than previously described. We found a number of paracentric inversions in the karyotypes of M. agrestis and M. rutilus, as well as multiple inversions and a centromere shift in the karyotype of M. arvalis. We propose that during karyotype evolution, arvicolines underwent a significant number of complex intrachromosomal rearrangements that were not previously detected.

From the animal house to the field: Are there consistent individual differences in immunological profile in wild populations of field voles (Microtus agrestis)?

Inbred mouse strains, living in simple laboratory environments far removed from nature, have been shown to vary consistently in their immune response. However, wildlife populations are typically outbreeding and face a multiplicity of challenges, parasitological and otherwise. In this study we seek evidence of consistent difference in immunological profile amongst individuals in the wild. We apply a novel method in this context, using longitudinal (repeated capture) data from natural populations of field voles, Microtus agrestis, on a range of life history and infection metrics, and on gene expression levels. We focus on three immune genes, IFN-γ, Gata3, and IL-10, representing respectively the Th1, Th2 and regulatory elements of the immune response. Our results show that there was clear evidence of consistent differences between individuals in their typical level of expression of at least one immune gene, and at most all three immune genes, after other measured sources of variation had been taken into account. Furthermore, individuals that responded to changing circumstances by increasing expression levels of Gata3 had a correlated increase in expression levels of IFN-γ. Our work stresses the importance of acknowledging immunological variation amongst individuals in studies of parasitological and infectious disease risk in wildlife populations.

Dampening of population cycles in voles affects small mammal community structure, decreases diversity, and increases prevalence of a zoonotic disease.

Long‐term decline and depression of density in cyclic small rodents is a recent widespread phenomenon. These observed changes at the population level might have cascading effects at the ecosystem level. Here, we assessed relationships between changing boreal landscapes and biodiversity changes of small mammal communities. We also inferred potential effects of observed community changes for increased transmission risk of Puumala virus (PUUV) spread, causing the zoonotic disease nephropatica epidemica in humans. Analyses were based on long‐term (1971–2013) monitoring data of shrews and voles representing 58 time series in northern Sweden. We calculated richness, diversity, and evenness at alpha, beta, and gamma level, partitioned beta diversity into turnover (species replacement) and nestedness (species addition/removal), used similarity percentages (SIMPER) analysis to assess community structure, and calculated the cumulated number of PUUV‐infected bank voles and average PUUV prevalence (percentage of infected bank voles) per vole cycle. Alpha, beta, and gamma richness and diversity of voles, but not shrews, showed long‐term trends that varied spatially. The observed patterns were associated with an increase in community contribution of bank vole (Myodes glareolus), a decrease of gray‐sided vole (M. rufocanus) and field vole (Microtus agrestis) and a hump‐shaped variation in contribution of common shrew (Sorex araneus). Long‐term biodiversity changes were largely related to changes in forest landscape structure. Number of PUUV‐infected bank voles in spring was negatively related to beta and gamma diversity, and positively related to turnover of shrews (replaced by voles) and to community contribution of bank voles. The latter was also positively related to average PUUV prevalence in spring. We showed that long‐term changes in the boreal landscape contributed to explain the decrease in biodiversity and the change in structure of small mammal communities. In addition, our results suggest decrease in small mammal diversity to have knock‐on effects on dynamics of infectious diseases among small mammals with potential implications for disease transmission to humans.

Endemic Hantavirus in Field Voles, Northern England.

We report a PCR survey of hantavirus infection in an extensive field vole (Microtus agrestis) population present in the Kielder Forest, northern England. A Tatenale virus–like lineage was frequently detected (≈17% prevalence) in liver tissue. Lineages genetically similar to Tatenale virus are likely to be endemic in northern England.

Microtus agrestis (Rodentia: Cricetidae)

Microtus agrestis (Linnaeus, 1761) is a relatively small microtine rodent commonly called the field vole. It has a compact body, blunt oval head, short round ears that barely protrude from the fur, and a short, bicolored, rather stiff tail. It is easily confused with sympatric or parapatric Microtus arvalis, M. oeconomus, and M. levis (M. rossiaermeridonalis) with indistinguishable juveniles. There is geographical variation of size and coloration ranging across Europe south from the Pyrenees to the Arctic coast and Alps eastward to the River Yenisei and Lake Baikal in Asia up to elevations of 2,100 m. It prefers wet meadow areas, riverside habitats, and forests with dense herbaceous cover. M. agrestis is considered to represent a trace of a 1st radiation of the genus Microtus in Europe.