Vole Species Research Articles

Brain Sexual Differentiation and Requirement of SRY: Why or Why Not?

Brain sexual differentiation is orchestrated by precise coordination of sex steroid hormones. In some species, programming of select male brain regions is dependent upon aromatization of testosterone to estrogen. In mammals, these hormones surge during the organizational and activational periods that occur during perinatal development and adulthood, respectively. In various fish and reptiles, incubation temperature during a critical embryonic period results in male or female sexual differentiation, but this can be overridden in males by early exposure to estrogenic chemicals. Testes development in mammals requires a Y chromosome and testis determining gene SRY (in humans)/Sry (all other therian mammals), although there are notable exceptions. Two species of spiny rats: Amami spiny rat (Tokudaia osimensis) and Tokunoshima spiny rat (Tokudaia tokunoshimensis) and two species of mole voles (Ellobius lutescens and Ellobius tancrei), lack a Y chromosome/Sry and possess an XO chromosome system in both sexes. Such rodent species, prototherians (monotremes, who also lack Sry), and fish and reptile species that demonstrate temperature sex determination (TSD) seemingly call into question the requirement of Sry for brain sexual differentiation. This review will consider brain regions expressing SRY/Sry in humans and rodents, respectively, and potential roles of SRY/Sry in the brain will be discussed. The evidence from various taxa disputing the requirement of Sry for brain sexual differentiation in mammals (therians and prototherians) and certain fish and reptilian species will be examined. A comparative approach to address this question may elucidate other genes, pathways, and epigenetic modifications stimulating brain sexual differentiation in vertebrate species, including humans.

Diversity of Thermogenic Capacity Predicts Divergent Obesity Susceptibility in a Wild Rodent.

The objective of the present study was to examine whether wild rodents exhibit diverse obesity susceptibility and what factors predispose subjects to this divergence in response to a high-fat diet (HFD). Sixty male and female Brandt's voles (Lasiopodomys brandtii) were fed an HFD for 8 weeks, and the upper (obesity prone [OP]) and lower (obesity resistant [OR]) one-third for mass gain were selected. Energy budgets and pathologic changes were measured. Another 30 males were fed a low-fat control diet (LFD) for 10 weeks and then fed an HFD for 12 weeks. The energetic parameters of the rodents on an LFD were analyzed for the correlation with body mass of the rodents on an HFD. OP voles had higher energy intakes, higher levels of noradrenaline-induced nonshivering thermogenesis, and a greater impairment of insulin tolerance than OR voles. Unlike laboratory rodents, there were no differences in physical activity or resting metabolic rate between these groups of voles. The thermogenic capacity during LFD feeding was the strongest predictor for mass gain during HFD feeding. This study suggests that a wild rodent species of Brandt's voles exhibits diverse obesity susceptibility in reaction to an HFD, providing a natural model to give insight into the mechanisms for divergent obesity susceptibility. This study also indicates that maximum thermogenic capacity has a predictive power for the development of obesity when an HFD was available.

Chromosomal Evolution in Mole Voles Ellobius (Cricetidae, Rodentia): Bizarre Sex Chromosomes, Variable Autosomes and Meiosis.

This study reports on extensive experimental material covering more than 30 years of studying the genetics of mole voles. Sex chromosomes of Ellobius demonstrate an extraordinary case of mammalian sex chromosomes evolution. Five species of mole voles own three types of sex chromosomes; typical for placentals: XY♂/XX♀; and atypical X0♂/X0♀; or XX♂/XX♀. Mechanisms of sex determination in all Ellobius species remain enigmatic. It was supposed that the Y chromosome was lost twice and independently in subgenera Bramus and Ellobius. Previous to the Y being lost, the X chromosome in distinct species obtained some parts of the Y chromosome, with or without Sry, and accumulated one or several copies of the Eif2s3y gene. Along with enormous variations of sex chromosomes, genes of sex determination pathway and autosomes, and five mole vole species demonstrate ability to establish different meiotic mechanisms, which stabilize their genetic systems and make it possible to overcome the evolutionary deadlocks.

Trap type and positioning: how to trap Savi’s pine voles using the tunnel system

AbstractSavi’s pine vole,Microtus savii, is the most widespread Italian vole species, an important rodent pest in agriculture and yet one of the least studied species. One of the reasons for this gap in knowledge is that members of this species are quite difficult to capture with standard trapping procedures, being fossorial and rarely active aboveground. For this reason, we developed a protocol that maximizes trapping success. This method requires the identification of active tunnel holes and the placement of traps directly in front of the exits. We also compared capture and recapture rates of Savi’s pine voles in three different trap types: Institut National de la Recherche Agronomique (INRA), Longworth and Ugglan. If properly equipped with food and nesting material, INRA, Longworth and Ugglan traps showed similar capture rates, but the recapture rate of Ugglan traps was the highest of the three kinds of traps. These results, in combination with the species’ fossorial and social habits, lead us to conclude that Ugglan traps are the best suited for studies on Savi’s pine voles. Our results may have implications for planning and implementing management strategies based on traps rather than rodenticides, as well as field studies on other fossorial small mammals.

Three Genetically Different Lineages of Yersinia pestis subsp. Microtus bv. Caucasica (0.PE2) Strains Circulate among Common Voles in Natural Plague Foci in the Caucasus

Gram-negative bacteria Y. pestis subsp. pestis of 0.ANT-4.ANT, 1.ORI, and 2.MED SNP types are the cause of numerous epidemic outbreaks, epidemics, and three plague pandemics, claiming hundreds of millions of human lives. At the same time, strains of the microtus subspecies that belong to the 0.PE SNP type circulating in populations of different species of voles (Microtus spp.) are able to cause only extremely rare human infections that are not transmitted from person to person. It is suggested that the clinical form of the infection can develop only in individuals with impaired immune status. Strains of Y. pestis bv. caucasica (0.PE2), one of the most ancient phylogenetic groups of subsp. microtus, are isolated on the territory of the following natural foci: the Transcaucasian highland (including the Leninakan (4), Pre-Sevan (5), and Zanzegur- Karabakh (6)) mesofoci and the Dagestan-highland (39). In addition to the enumerated areas, similar strains of Y. pestis are isolated in the territories of the Pre-Araks focus (7) bordering the Transcaucasian highland one. Previously, we showed that passport data on the phenotypic differences of strains of the biovar caucasica, isolated from different foci, corresponded to their MLVA25, CRISPR, and DFR genotypes. In the present work, a comparative analysis of the clustering ability of MLVA25- and CRISPR-typing methods with the “gold standard” of phylogenetic studies—SNP typing—has been conducted on 21 strains of Y. pestis subsp. microtus bv. caucasica (0.PE2). The analysis of the obtained results confirms the existence of three clonal clusters of strains corresponding to the natural plague foci—39, 4, and the group of foci 5–7. Only the SNP-typing method made it possible to separate branch of focus 5 isolates from a group of strains isolated in foci 5–7. In addition, this method made it possible to reveal a greater genetic heterogeneity of strains from focus 39, in contrast to the strains of foci 4–7. When analyzing the genomes of Y. pestis strains isolated in the territory of focus 39, a deletion (~20 kb) was detected in the CRISPR region of the Ypb locus. The absence of this locus can serve as a marker for the determination of a given population of Y. pestis strains.

Differences in Neural Response to Romantic Stimuli in Monogamous and Non-Monogamous Men.

In non-human animal research, studies comparing socially monogamous and promiscuous species of voles (Microtus) have identified some key neural differences related to monogamy and non-monogamy. Specifically, densities of the vasopressin V1a receptor and dopamine D2 receptors in subcortical reward-related and limbic areas of the brain have been linked to monogamous behavior in prairie voles (Microtus ochrogaster). Similar brain areas have been shown to be correlated with feelings of romantic love in monogamously pair-bonded humans. Humans vary in the degree to which they engage in (non-)monogamous behaviors. The present study examined the differences in neural activation in response to sexual and romantic stimuli in monogamous (n=10) and non-monogamous (n=10) men. Results indicated that monogamous men showed more reward-related neural activity when viewing romantic pictures compared to non-monogamous men. Areas with increased activation for monogamous men were all in the right hemisphere and included the thalamus, accumbens, striatum, pallidum, insula, and orbitofrontal cortex. There were no significant differences between groups in activation to sexual stimuli. These results demonstrate that the neural processing of romantic images is different for monogamous and non-monogamous men. There is some overlap in the neural areas showing increased activation in monogamous men in the present study and the neural areas that show differences in the vole models of monogamy and affiliation. Future research will be needed to clarify whether similar factors are contributing to the neural differences seen in monogamous and non-monogamous humans and voles.

Mammalian responses to windrows of woody debris on clearcuts: Abundance and diversity of forest-floor small mammals and presence of small mustelids

Forest harvesting often leaves excess woody debris on the forest floor that could provide habitat for small mammals and mustelid predators. A windrow or series of piles constructed from woody debris may connect patches of mature forest and riparian areas to allow small mammals and some of their predators to use clearcut openings. We tested two hypotheses (H) that woody debris arranged in windrows connecting reserves of uncut forest, on newly clearcut sites, would increase (H1) abundance of the major vole species and total abundance, species richness, and species diversity of the forest-floor small mammal community, and (H2) presence of small mustelids in response to abundance of small mammal prey; compared with sites of dispersed woody debris or uncut forest. We measured abundance and diversity of small mammals and the presence of small mustelids (American marten, Martes americana; short-tailed weasel, Mustela erminea; long-tailed weasel, M. frenata) from 2012 to 2016 in replicated treatments of woody debris in windrow and dispersed sites compared with uncut forest sites at two study areas near Elkhart and Golden in south-central British Columbia, Canada.At Elkhart, mean abundance of total voles and total small mammals per index-line were higher in the windrow than dispersed sites, and higher or similar to forest sites. At Golden, mean abundance of total voles was similar, but the dispersed and windrow sites had higher numbers of total small mammals than the forest sites. Mean species richness and diversity were highest in the windrow sites at both study areas. Thus, the predictions of H1 were supported, except for total voles at Golden. Mean abundance of the southern red-backed vole (Myodes gapperi), a principal prey species for mustelids, was higher in windrow than dispersed sites, and similar or lower than forest sites. M. gapperi, along with the long-tailed vole (Microtus longicaudus) dominated the overall vole population in windrows at Elkhart. M. longicaudus dominated the windrows and dispersed sites at Golden. Deer mice (Peromyscus maniculatus) and northwestern chipmunks (Neotamias amoenus) were at similar numbers in dispersed and windrow sites, but shrews (Sorex spp.) showed a positive response to windrows. Overall mean presence by marten and small weasels were, on average, 3.3–4.8 times higher in windrow than dispersed sites, and higher or similar to forest sites, which supported H2. Our study is the first to connect windrows to patches and larger units of uncut forest and to cover a 5-year period since harvest. Responses in mean total abundance, species richness, and diversity of small mammals in windrows were maintained throughout the 5-year period. This consistent result was likely related to the connectivity between windrows and uncut forests. Strategic management of post-harvest woody debris in a network of windrows or piles will help to maintain abundance and diversity of forest mammals, both predator and prey species, on clearcuts.

Impact of climate change on population dynamics of forest voles (Myodes) in northern Pre-Urals: The role of landscape effects

In recent years in northern Pre-Urals, the population dynamics of forest voles has undergone significant changes. In the foothill area, the abundance of the red-backed vole has decreased and that of the bank vole has increased significantly. As a result, the latter becomes the dominant species. In nearby lowland areas, the population of the bank vole has remained stable while the red-backed vole has increased. The main cause of these changes is the transformation of the environment under the influence of global climate change. This affects mainly foothill conifer forests and, to a lesser extent, lowland forests. As a consequence, responses of various vole species to these changes in different landscape areas are not identical.

Female Intrasexual Territoriality and its Potential Adaptive Significance: The Pampean Grassland Mouse as an Ecological Model Species

Territorial behaviour in female small mammals has been proposed as a mechanism to defend limited ecological resources or their pups against conspecific infanticidal or predators. Female territorial behaviour very often is associated with reproductive activity due to the fact that frequency and intensity of aggression are exhibited mainly when females are pregnant or lactating. In vole and mice species, female territoriality would be a counterstrategy to prevent the killing of their pups by conspecific breeding females. To study whether female territoriality is a strategy for pups or nest defence against infanticidal breeding females, and whether time invested in nursing young affects aggressive response of mothers, we used the Pampean grassland mouse (Akodon azarae) as an ecological model species. We conducted resident–intruder tests between lactating females. Differences in residency time (48 vs. 72 h) of focal females in their home territory were also included in the analysis. In all cases, the pups of both resident and intruder mothers were placed with the nesting material from their reproductive cages. Resident mothers were always more aggressive than intruders and they were even more aggressive when they spent more time nursing their pups. Contrarily, intruder females exhibited the greatest values of submissive behaviours. Our results show that female territoriality of A. azarae would represent a strategy to protect pups from potentially infanticidal females. We discuss the extent of female intrasexual territoriality and its potential adaptive significance in relation to strategies which lead to increase their reproductive success.

Prevalence, genetic identity and vertical transmission of Babesia microti in three naturally infected species of vole, Microtus spp. (Cricetidae)

BackgroundVertical transmission is one of the transmission routes for Babesia microti, the causative agent of the zoonotic disease, babesiosis. Congenital Babesia invasions have been recorded in laboratory mice, dogs and humans. The aim of our study was to determine if vertical transmission of B. microti occurs in naturally-infected reservoir hosts of the genus Microtus.MethodsWe sampled 124 common voles, Microtus arvalis; 76 root voles, M. oeconomus and 17 field voles, M. agrestis. In total, 113 embryos were isolated from 20 pregnant females. Another 11 pregnant females were kept in the animal house at the field station in Urwitałt until they had given birth and weaned their pups (n = 62). Blood smears and/or PCR targeting the 550 bp 18S rRNA gene fragment were used for the detection of B. microti. Selected PCR products, including isolates from females/dams and their embryos/pups, were sequenced.ResultsPositive PCR reactions were obtained for 41% (89/217) of the wild-caught voles. The highest prevalence of B. microti was recorded in M. arvalis (56/124; 45.2%), then in M. oeconomus (30/76; 39.5%) and the lowest in M. agrestis (3/17; 17.7%). Babesia microti DNA was detected in 61.4% (27/44) of pregnant females. Vertical transmission was confirmed in 81% (61/75) of the embryos recovered from Babesia-positive wild-caught pregnant females. The DNA of B. microti was detected in the hearts, lungs and livers of embryos from 98% of M. arvalis, 46% of M. oeconomus and 0% of M. agrestis embryos from Babesia-positive females. Of the pups born in captivity, 90% were born to Babesia-positive dams. Babesia microti DNA was detected in 70% (35/50) of M. arvalis and 83% (5/6) of M. oeconomus pups. Congenitally acquired infections had no impact on the survival of pups over a 3-week period post partum. Among 97 B. microti sequences, two genotypes were found. The IRU1 genotype (Jena-like) was dominant in wild-caught voles (49/53; 92%), pregnant females (9/11; 82%) and dams (3/5; 60%). The IRU2 genotype (Munich-like) was dominant among B. microti positive embryos (20/27; 74%) and pups (12/17; 71%).ConclusionA high rate of vertical transmission of the two main rodent genotypes of B. microti was confirmed in two species of naturally infected voles, M. arvalis and M. oeconomus.

Distribution and parameters of genetic polymorphism in northern red-backed vole (Clethrionomys rutilus) and bank vole (Clethrionomys glareolus) in West Siberia

This article presents data on the genetic variability of the northern red-backed vole and the bank vole that live sympatrically in West Siberia. The two species of voles have comparable, relatively high indices of genetic variability of inter simple sequences repeats DNA. The proportion of polymorphic DNA markers is 95–98%, and the Nei’s genetic diversity index is 0.33–0.35. A total of 47–58% of allozyme loci in the voles are polymorphic, and the average heterozygosity per locus is 0.058 in the northern red-backed vole and 0.054 in the bank vole. Interpopulation differentiation is less pronounced in the red-backed vole (FST 0.293) compared to the bank vole (FST 0.475). Individuals of the hybrid line of the bank vole with the mitochondrial haplotype of the red-backed vole have been found by PCR typing of cytochrome b gene fragment of mtDNA. The distribution boundary of the hybrid line of bank voles goes farther to the northeast than was shown in earlier works. The proportion of hybrid specimens range from 2 to 34%. The indices of genetic variability in the hybrid line of the bank vole are lower than those of the parental species.

Variants of tooth mesowear in Microtus voles as indicators of food hardness and abrasiveness

Methodological approaches to the description of variants and degrees of hypselodont tooth mesowear in voles are proposed on the basis of studies on the collection of skulls of two vole species trapped in the field (narrow-headed vole, n = 38; common vole, n = 22) and two species from laboratory colonies (narrow-headed vole, n = 46; root vole, n = 76). Trends in the manifestation of different mesowear variants have been analyzed in experiments on feeding root voles from the laboratory colony with “hard” and “soft” foods. It has been found that animals kept on low-abrasive diet show signs of wear due to tooth-to-tooth contact, such as low crown height, relatively obtuse wear angle and more upright position of m/1 in the jaw, shallow occlusal surface relief, and lateral wear facets. Chewing hard food items requires application of vertical occlusal pressure, which result in the formation of a depression in repair dentin, while denser dentin at the anterior enamel wall of prisms remains unworn.

New data on chromosomal variability, distribution of sibling species, and hybridization of 46-chromosomal forms of Microtus arvalis sensu lato (Rodentia, Arvicolinae) in the Upper Volga basin

New data are presented on the composition, intraspecific structure, and geographic distribution of the sibling species of common voles in the Upper Volga basin and on the occurrence frequency and temporal dynamics of the complex chromosomal rearrangement of autosome pair 5 in Microtus arvalis f. obscurus in populations from Nizhny Novgorod region. A total of 100 M. arvalis s. l. from 18 localities of the region have been identified by methods of chromosomal analysis (routine and AgNOR staining, C- and G-banding). The forms of M. arvalis s. l. distinguished in the sample include M. rossiaemeridionalis (n = 4), M. arvalis f. obscurus (n = 82), M. arvalis form arvalis (n = 11), and F1 hybrids between the last two forms (n = 3). These results confirm the concept of M. arvalis s. l. taxonomic diversity in the Upper Volga basin and contribute to the cadasters of M. rossiaemeridionalis, M. arvalis f. arvalis and M. arvalis f. obscurus. In addition, they allow a more accurate delimitation of the distribution boundaries of 46-chromosomal M. arvalis s. l. forms in the Upper Volga basin and are indicative of hybridization between them in Nizhny Novgorod region (Sokolsky district), where M. arvalis f. arvalis and F1 hybrids have been recorded for the first time.

Chromosomal and molecular studies of cryptic species of the subgenus Terricola (Rodentia, Arvicolinae, Microtus) in the Caucasian region: Analysis of new records

Using chromosomal and molecular (cytb) markers, the specific identity of 78 individuals of cryptic species of voles of the subgenus Terricola was ascertained. The animal samples were obtained at 13 localities of the Caucasian region, from Krasnodar krai to North Ossetia in the Greater Caucasus and in the Stavropol Upland (forest island in the steppe) in Ciscaucasia, which had not been covered earlier in genetic studies. In the total sample, two chromosomal forms (cryptic species), namely, Microtus (Terricola) majori (2n = 54, NF = 60) and M. (T.) daghestanicus (2n = 54, NF = 58), were identified. The specific identity of most animals tested was confirmed by karyological means, and for individuals from two localities on the south slopes of the Greater Caucasus (Adlerskii district of Krasnodar krai), it was confirmed exclusively by means of molecular (cytb) markers. The last two records were used for evaluation of the differential role of sibling-species of the subgenus Terricola in circulation of the pathogen in mountain loci of hemorrhagic fever with renal syndrome (HFRS) in the Western Caucasus. For the first time, using the example of M. (T.) majori from the Ciscaucasia, which was compared with those of the mountain part of the species’ natural habitat, the role of isolation factors in morphogenesis of the subgenus Terricola was studied. As a whole, the results obtained specify the character of the geographical distribution and biotope attachment of cryptic species of the subgenus Terricola in the Caucasian region.

Genetic variants in oxytocin receptor and arginine-vasopressin receptor 1A are associated with the neural correlates of maternal and paternal affection towards their child

There is extensive evidence in animal studies, particularly in vole species (Microtus), that oxytocin (OT) receptor and arginine-vasopressin (AVP) receptor 1a is critical for the regulation of maternal and paternal behavior, respectively. Human studies have gained insight into the relationship between both hormone receptor gene variants and behavior, but not between the variants and the underlying brain activity. To study this, we investigated the association between neural activation of the anterior prefrontal cortex (APFC) in mothers and fathers in response to their child smiling video stimuli to induce the positive affect related to attachment with their child, and genetic variants of OT receptor (OXTR) and AVP receptor 1A (AVPR1A). Overall, 43 mothers and 41 fathers participated, and each parent's child smiling was video recorded. Participants were then genotyped and underwent near-infrared spectroscopy to measure neural activation of the APFC while observing their own child smiling compared with an unfamiliar child. We found that the right inferior APFC was activated in response to child video stimuli in mothers and differential hemispheric activation of the inferior APFC in OXTR rs2254298-G/G mothers compared with -A carrier mothers, but not in fathers. Furthermore, we found a difference in the left inferior APFC activation between AVPR1A RS3-non-334 and -334 carrier fathers, but not mothers. Our results indicate a sex-dependent association between the genetic variants and the inferior APFC activations of maternal and paternal positive affect, analogous to the results reported in voles.

Genomes of Ellobius species provide insight into the evolutionary dynamics of mammalian sex chromosomes.

The X and Y sex chromosomes of placental mammals show hallmarks of a tumultuous evolutionary past. The X Chromosome has a rich and conserved gene content, while the Y Chromosome has lost most of its genes. In the Transcaucasian mole vole Ellobius lutescens, the Y Chromosome including Sry has been lost, and both females and males have a 17,X diploid karyotype. Similarly, the closely related Ellobius talpinus, has a 54,XX karyotype in both females and males. Here, we report the sequencing and assembly of the E. lutescens and E. talpinus genomes. The results indicate that the loss of the Y Chromosome in E. lutescens and E. talpinus occurred in two independent events. Four functional homologs of mouse Y-Chromosomal genes were detected in both female and male E. lutescens, of which three were also detected in the E. talpinus genome. One of these is Eif2s3y, known as the only Y-derived gene that is crucial for successful male meiosis. Female and male E. lutescens can carry one and the same X Chromosome with a largely conserved gene content, including all genes known to function in X Chromosome inactivation. The availability of the genomes of these mole vole species provides unique models to study the dynamics of sex chromosome evolution.

Seed preferences by rodents in the agri-environment and implications for biological weed control.

SummaryPost‐dispersal seed predation and endozoochorous seed dispersal are two antagonistic processes in relation to plant recruitment, but rely on similar preconditions such as feeding behavior of seed consumers and seed traits. In agricultural landscapes, rodents are considered important seed predators, thereby potentially providing regulating ecosystem services in terms of biological weed control. However, their potential to disperse seeds endozoochorously is largely unknown. We exposed seeds of arable plant species with different seed traits (seed weight, nutrient content) and different Red List status in an experimental rye field and assessed seed removal by rodents. In a complementary laboratory experiment, consumption rates, feeding preferences, and potential endozoochory by two vole species (Microtus arvalis and Myodes glareolus) were tested. Seed consumption by rodents after 24 h was 35% in the field and 90% in the laboratory. Both vole species preferred nutrient‐rich over nutrient‐poor seeds and M. glareolus further preferred light over heavy seeds and seeds of common over those of endangered plants. Endozoochory by voles could be neglected for all tested plant species as no seeds germinated, and only few intact seeds could be retrieved from feces. Synthesis and applications. Our results suggest that voles can provide regulating services in agricultural landscapes by depleting the seed shadow of weeds, rather than facilitating plant recruitment by endozoochory. In the laboratory, endangered arable plants were less preferred by voles than noxious weeds, and thus, our results provide implications for seed choice in restoration approaches. However, other factors such as seed and predator densities need to be taken into account to reliably predict the impact of rodents on the seed fate of arable plants.

Hierarchical spatial segregation of two Mediterranean vole species: the role of patch-network structure and matrix composition

According to ecological theory, the coexistence of competitors in patchy environments may be facilitated by hierarchical spatial segregation along axes of environmental variation, but empirical evidence is limited. Cabrera and water voles show a metapopulation-like structure in Mediterranean farmland, where they are known to segregate along space, habitat, and time axes within habitat patches. Here, we assess whether segregation also occurs among and within landscapes, and how this is influenced by patch-network and matrix composition. We surveyed 75 landscapes, each covering 78ha, where we mapped all habitat patches potentially suitable for Cabrera and water voles, and the area effectively occupied by each species (extent of occupancy). The relatively large water vole tended to be the sole occupant of landscapes with high habitat amount but relatively low patch density (i.e., with a few large patches), and with a predominantly agricultural matrix, whereas landscapes with high patch density (i.e., many small patches) and low agricultural cover, tended to be occupied exclusively by the small Cabrera vole. The two species tended to co-occur in landscapes with intermediate patch-network and matrix characteristics, though their extents of occurrence were negatively correlated after controlling for environmental effects. In combination with our previous studies on the Cabrera-water vole system, these findings illustrated empirically the occurrence of hierarchical spatial segregation, ranging from within-patches to among-landscapes. Overall, our study suggests that recognizing the hierarchical nature of spatial segregation patterns and their major environmental drivers should enhance our understanding of species coexistence in patchy environments.

The systematic position of Middle Pleistocene ground voles Microtus (Terricola) Fatio, 1867 (Arvicolinae, Rodentia) at Vergranne (Franche-Comté, France)

This odontometrical study of the first lower molar of the vole species Microtus vergrannensis from the Middle Pleistocene Vergranne karst filling (Franche-Comte, France) specifies the criteria that characterise M. vergrannensis with regard to the present-day species M. subterraneus and M. multiplex and the Cromerian species M. arvalidens. The findings suggest that M. vergrannensis may have derived from M. arvalidens during the Middle Pleistocene.

Factors influencing vole bark damage intensity in managed mountain-forest plantations of Central Europe

We studied the impact of vole bark gnawing in forest plantations dominated by European beech in two Czech mountain ranges (the Hrubý Jesenik Mts, the Moravskoslezske Beskydy Mts) with different habitat conditions. Of the four present vole species, only the field vole caused significant damage, the impact of the bank vole being inconclusive. In both ranges, the key factor determining the presence and abundance of voles (Microtus sp.) was the occurrence of grasses. Saplings in the Hrubý Jesenik Mts suffered significantly higher damage than those in the Moravskoslezske Beskydy Mts (13.6 vs. 3.3 % damaged seedlings), with degree of damage closely related to the abundance and spatial distribution of voles. We relate it to lower carrying capacity caused by poor herb layer and higher proportion of spruce monocultures surrounding the plantations in the Hrubý Jesenik Mts. Our results indicate that artificial beech regeneration is more successful in mixed and spruce forests with rich undergrowth (the Moravskoslezske Beskydy Mts) than in large spruce stands with reduced herb undergrowth (the Hrubý Jesenik Mts).