Gene conversion in the mitochondrial genome on interspecific hybridization in voles of the <Emphasis Type="Italic">Clethrionomys</Emphasis> genus

The phenomenon of interspecific hybridization accompanied by transfer of the mitochondrial genome from the northern red-backed vole (Clethrionomys rutilus) to the bank vole (Cl. glareolus) in northeastern Europe is well known already for 25 years. However, the possibility of recombination between homologous segments of maternal and paternal mtDNAs of the voles during fertilization was not previously studied. Analysis of data on variability of nucleotide sequences of the mitochondrial gene for cytochrome b in populations of red-backed and bank voles in the area of their sympatry has shown that as a result of interspecific hybridization, the mitochondrial gene pool of bank voles contains not only mtDNA haplotypes of red-backed vole females, but also mtDNA haplotypes of bank voles bearing short nucleotide tracts of red-backed vole mtDNA. This finding supports the hypothesis that an incomplete elimination of red-backed vole paternal mtDNA during the interspecific hybridization between bank vole females and red-backed vole males leads to the gene conversion of bank vole maternal mtDNA tracts by homologous ones of mtDNA of red-backed vole males.     

SHORT-TERM DEMOGRAPHIC RESPONSE OF THE RED-BACKED VOLE TO SPRUCE BEETLE INFESTATIONS IN ALASKA

Abstract: How small mammals are affected by habitat changes caused by forest insect epidemics is largely unknown. Our objective was to determine the influence of spruce beetle (Dendroctonus rufipennis) epidemics on the dynamics of northern red-backed vole (Clethrionomys rutilus) populations approximately 10 years post-infestation. We conducted a mark-recapture study on northern red-backed voles for 2 field seasons in the Copper River Basin, Alaska, USA, where recent beetle infestations were widespread. Using the robust sampling design, we produced estimates of vole abundance, survival, and recruitment in 3 locations that varied in their degree of beetle-induced spruce mortality. Vole abundance inversely related to the level of spruce mortality. Vole recruitment showed a larger contribution from both immigration and in situ reproduction in the low infestation site than in the medium and heavy infestation sites. No differences in vole survival were detectable across the 3 locations with varied beetle-induced spruce mortality levels. Measured vole food resources and protective vegetative cover did not vary greatly across infestation levels. Abundance and recruitment parameters indicate a negative change induced by spruce beetle infestations. However, the effect of beetles was not large enough to cause the variation in vole survival. Spruce mortality levels may need to be over 50% before greatly influencing the habitat and the demographics of northern red-backed voles.     

Soluble blood proteins and hemoglobin from red-backed and large- toothed voles

Electrophoretic pattern of serum proteins of northern red-backed and large-toothed voles was examined. Seven main protein zones were distinguished. In four of them variability was observed, possibly genetically determined. Polymorphism of transferrins was thoroughly studied. 6 alleles and only 7 phenotypes of this protein were found in the northern red-backed vole, while 3 alleles and 4 phenotypes were revealed in the large-toothed red-backed vole, two alleles being common. Distribution of phenotype frequencies observed in both species differs significantly from the expected value. The portion of heterozygous phenotypes is quite high in both species, being 0.304 and 0.400 in the northern red-backed and large-toothed red-backed voles, respectively. Hemoglobins of the species studied were identical in electrophoretic mobility and monomorphic.     

Impact of climate change on population dynamics of forest voles (<Emphasis Type="Italic">Myodes</Emphasis>) 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.     

Distribution and parameters of genetic polymorphism in northern red-backed vole (<Emphasis Type="Italic">Clethrionomys rutilus</Emphasis>) and bank vole (<Emphasis Type="Italic">Clethrionomys glareolus</Emphasis>) 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 (F _ST 0.293) compared to the bank vole (F _ST 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.     

Bot fly parasitism of the red-backed vole: host survival,infection risk,and population growth

Parasites can play an important role in the dynamics of host populations, but empirical evidence remains sparse. We investigated the role of bot fly (Cuterebra spp.) parasitism in red-backed voles (Myodes gapperi) by first assessing the impacts of the parasite on the probability of vole survival under stressful conditions as well as on the reproductive activity of females. We then identified the main factors driving both the individual risk of infection and the abundance of bot flies inside red-backed voles. Finally, we evaluated the impacts of bot fly prevalence on the growth rate of vole populations between mid-July and mid-August. Thirty-six populations of red-backed voles were sampled in the boreal forest of Québec, Canada. The presence and the abundance of parasites in voles, two host life history traits (sex and body condition), three indices of habitat complexity (tree basal area, sapling basal area, coarse woody debris volume), and vole abundance were considered in models evaluating the effects of bot flies on host populations. We found that the probability of survival of red-backed voles in live traps decreased with bot fly infection. Both the individual risk of infection and the abundance of bot flies in red-backed voles were driven mainly by vole abundance rather than by the two host life history traits or the three variables of habitat complexity. Parasitism had population consequences: bot fly prevalence was linked to a decrease in short-term growth rate of vole populations over the summer. We found that bot flies have the potential to reduce survival of red-backed voles, an effect that may apply to large portions of populations. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Population limitation of the northern red-backed vole in the boreal forests of northern Canada

1. Across the vast boreal forests of North America, no population cycles in Clethrionomys species occur. In Eurasia, by contrast, some Clethrionomys populations of the same species undergo regular 3-5-year cycles. We examined the effects of nutrients, food, competitors, predators and climate on population limitation in the northern red-backed vole (Clethrionomys rutilus Pallas) in the south-western Yukon to determine why this difference occurs. 2. From 1986 to 1996 we added food, reduced large mammal predators and excluded snowshoe hares (Lepus americanus Erxleben) from large plots and found that none of these manipulations affected red-backed vole abundance. Adding nutrients as nitrogen, phosphorus and potassium (NPK) fertilizer had a slight negative effect, probably acting through a reduction in dwarf shrub productivity caused by competition from grasses. 3. We monitored weasel populations directly through trapping and indirectly through snow tracking. Predation by these vole specialists was irrelevant as a limiting factor most of the time because voles in this area do not reach the densities needed to sustain weasel populations. Other boreal forest mammal and bird predators did not focus on red-backed voles. However, when red-backed vole populations increased in the forest and Microtus voles also increased in the meadows, weasel populations increased and may have temporarily depressed red-backed voles in winter. 4. We monitored one major potential food, white spruce seeds, but seed fall was not related to population changes in red-backed voles, even after mast years. 5. We assessed the impact of weather variables, and the average depth of the snow pack during winter (October-March) was correlated directly with vole demography, having both direct effects in that year and delayed effects in the following year. 6. Our long-term trapping data (1973-96) indicate that Clethrionomys populations fluctuated, with peaks following hare peaks by 2-3 years. 7. We propose that the key variable limiting these vole populations is overwinter survival, and this is a function of overwinter food from berries produced during the previous summer by dwarf shrubs. These shrubs may be stimulated by abundant moisture from winter snows or by periodic fertilization from large quantities of pellets produced at snowshoe hare peaks.     

Genetic diversity of the cytochrome b gene fragment haplotypes in red-backed vole <Emphasis Type="Italic">Myodes</Emphasis> (<Emphasis Type="Italic">Clethrionomys</Emphasis>) <Emphasis Type="Italic">rutilus</Emphasis> Pallas, 1779

For the first time, genetic analysis of the cytochrome b gene fragment haplotypes encoding the identical and the most common cytochrome b polypeptide (F1) in M. rutilus from eastern and Beringian maternal lineages was carried out. The F1 frequencies for the vole populations from Northern Priokhotye and the Kolyma basin were calculated. Considerable polymorphism of the cytochrome b F1 haplotypes within two major phylogroups of red-backed vole was supported by high molecular diversity indices for these clades. The proportion of genetic variation between the maternal lineages of F1 red-backed vole individuals (60.71%) was considerably higher than inter(24.44%) and intrapopulation (14.85%) components. The data obtained make it possible to advance a hypothesis on the convergence of the cytochrome b polypeptide structure upon sequence divergence of the corresponding gene.     

Spatial distribution of red-backed voles of the genus <Emphasis Type="Italic">Myodes</Emphasis> in the Khanka Plain,Primorskii Krai

The authors present new data on spatial-temporal distribution of the northern red-backed vole (Myodes rutilus Pallas) and the large-toothed redback vole (M. rufocanus Sundervall) for the main habitat types in the Khanka Plain, Primorskii Krai. Data on seasonal and long-term abundance for 2003-2005 are reported. The study was stimulated by contradictory data on the distribution of the Myodes voles in the Khanka Plain.     

Owl winter irruptions as an indicator of small mammal population cycles in the boreal forest of eastern North America

Contrary to what is observed in Fennoscandia, it seems to be widely accepted that small mammals do not exhibit multi-annual population cycles in the boreal forest of North America. However, in the last thirty years, irruptions of vole predators such as owls have been reported by ornithologists south of the North American boreal forest. While such southerly irruptions have been associated in Fennoscandia with periods of low abundance of small mammals within their usual distribution range, their possible cyclic nature and their relationships to fluctuations in vole densities at northern latitudes has not yet been demonstrated in North America. With information collected from existing data-bases, we examined the presence of cycles in small mammals and their main avian predators by using temporal autocorrelation analyses. Winter invasions of boreal owls ( Aegolius funereus ) were periodic, with a 4-yr cycle in Québec. Populations of one species of small mammal, the red-backed vole ( Clethrionomys gapperi ), fluctuated periodically in boreal forests of Québec (north to 48°N). Boreal owls show invasion cycles which correspond to years of low density of red-backed voles, the main food item for this owl species. In addition, winter observations of northern hawk owls ( Surnia ulula ) and great gray owls ( Strix nebulosa ) south of their usual range increased in years of low density of red-backed voles. Our results suggest that a 4-yr population cycle exists in the eastern boreal forest of North America for voles and owls, which is very similar to the one observed in Fennoscandia.     

Genetic Distinctiveness of the Korean Red-Backed Vole (Myodes regulus) from Korea, Revealed by Mitochondrial Cytochrome b Gene Sequences

To examine the taxonomic status of the Korean red-backed vole (Myodes regulus), the full cytochrome b sequences of 21 red-backed voles from Korea and northeast China were compared with the corresponding haplotypes from 12 species of Myodes and Eothenomys from GenBank. We identified five red-backed voles from Mount Changbai and Harbin as Myodes rufocanus and three from Harbin as M. rutilus, and we confirmed that the red-backed voles from Korea are M. regulus and not Eothenomys regulus. We found that M. regulus from Korea differed from the other five species of Myodes and that the interspecific distances between M. regulus and each of the two species from northeast China were 4.55% (M. rufocanus) and 11.1% (M. rutilus). We concluded that M. regulus is also genetically distinct and is an endemic species of Korea.     

A new intermediate host for Echinococcus multilocularis: The southern red-backed vole (Myodes gapperi) in urban landscape in Calgary,Canada

Human Alveolar Echinococcosis (HAE) is a potentially fatal parasitic disease caused by Echinococcus multilocularis, a cestode characterized by a sylvatic life-cycle involving several species of rodents and lagomorphs as intermediate hosts and canids as definitive hosts. Despite the wide distribution of the parasite in North America, the number of competent intermediate host species identified to date is still relatively small, and mainly includes the northern vole (Microtus oeconomus), brown lemming (Lemmus sibiricus), northern red-backed vole (Myodes rutilus), deer mouse (Peromyscus maniculatus) and meadow vole (Microtus pennsylvanicus).By monitoring the infections in rodents in the city of Calgary (Alberta, Canada), we have detected a case of severe alveolar echinococcosis in a southern red-backed vole (Myodes gapperi), a species never reported before as an intermediate host for this parasite. Observation of protoscolices in the intra-abdominal multilocular cysts indicates that M. gapperi could act as a competent intermediate host for the transmission of E. multilocularis.Since M. gapperi can be found in close proximity to, and within metropolitan areas, this species could play a role in the establishment and maintenance of the sylvatic life-cycle of E. multilocularis in urban landscapes, where the potential for zoonotic transmission is higher. The new intermediate host reported needs to be taken into account in future surveys and transmission models for this parasite.     

Density-dependent regulation in populations of red-backed voles (Myodes rutilus) in optimal and suboptimal habitats of south-west Siberia

In a population of red-backed voles (Myodes rutilus) that live in optimal habitats (mountain taiga of North-Eastern Altai) in the years of peak density we have observed total suppression of sexual maturation of young animals which is known to be the main mechanism of density regulation. Increase of voles' local density is accompanied by the increase of glucocorticoids in blood of mature and immature individuals of both sexes that argues for the important role of hypothalamic-pituitary-adrenal axis in density dependent regulation. Another population of red-backed voles from south-west Siberia that live in suboptimal habitats (Novosibirsk city vicinity), had significantly lower density. Here, the dynamics of demographic traits and endocrine status of the individuals did not correlate with interannual fluctuations of abundance and density. Even though, the possibility that in suboptimal conditions local density occasionally reaches the values sufficient for the induction of self-regulation cannot be excluded.     

Sexual maturation and age-related dynamics of corticosterone in Clethrionomys rutilus and Cl. rufocanus voles (Rodentia, Cricetidae) under experimental conditions

Differences in the mechanisms regulating reproduction between the northern red-backed vole (Clethrionomys rutilus) and large-toothed red-backed vole (Cl. rufocanus) have been revealed under vivarium conditions. In Cl. rufocanus, the date of birth is the most important ??signal?? factor for sexual maturation of male young of the year, while the effect of population density is significant only for males of the spring generation. Males of the summer generation fail to mature in the same year and are completely excluded from reproduction, which may be accounted for by a rise in the level of corticosterone (measured in fecal samples). Such a mechanism for regulating the numbers of reproductive individuals is absent in Cl. rutilus voles. Throughout the breeding season, males of this species respond to high population density by a decrease in the rate of sexual maturation. No definite relationship between sexual maturation and the level of adrenocortical activity has been revealed in Cl. rutilus.     

Effects of age and seasonal rhythm on the growth patterns of some small mammals in Finland and in Kirkenes, Norway

The intensity of growth of Sorex araneus L. and Clethrionomys glareolus Schreb. in the Oulu district of Finland is studied as a function of age and seasonal rhythm, and compared with the results of growth-rate measurements of Sorex araneus L., Clethrionomys rufocanus Sund. and Clethrionomys rutilus Pall. in Kirkenes, Norway. It is assumed that the postnatal development of the Common shrew with its growth and regression phases is to some extent controlled by an endogenous seasonal rhythm. The growth of the voles is not as clearly controlled by these rhythms as that of the Common shrew although the growth of the Bank vole and Northern red-backed vole is obviously considerably retarded in autumn and in winter.     

Experimental hybridization of voles of the genus Microtus s.l. M. socialis with species of the group arvalis (Mammalia,Rodentia)

The results of interspecific crosses of the social vole Microtus socialis with the Altai vole M. obscurus, the East European vole M. rossiaemeridionalis, and the Transcaspian vole M. transcaspicus are presented. The role of the sperm head structure in the reproductive isolation of this species was studied. Hybrids were obtained in five of the six crossing combinations. It is established that significant differences in the sperm head shape in the social vole and in arvalis group species do not prevent fertilization. The sterility of hybrids indicates the existence of postcopulative mechanisms of reproductive isolation.     

The complete mitochondrial genome of the Korean red-backed vole, Myodes regulus (Rodentia, Murinae) from Korea

We have determined the complete mitochondrial genome (NC_016427) of the Korean red-backed vole, Myodes regulus, which is distributed in South Korea. The total length of the M. regulus mitogenome is 16,379?bp, with a base composition of 33.0% A, 26.7% T, 27.1% C, and 13.2% G. The total length of the 13 protein-coding genes is 11,396?bp long.     

Fine-Scale Habitat Associations of Red-Backed Voles in Boreal Mixedwood Stands

Abstract: To provide habitat for late-successional wildlife species, new ecosystem-based forest management practices aim to retain elements of complex stand structure, including live residual trees, dead wood legacies, and advanced regeneration, within managed stands. Predicting the effectiveness of these strategies is a challenge for species whose habitat relationships may involve multiple factors and can vary among sites. For 2 years, we live-trapped a common, late-successional microtine rodent, the southern red-backed vole (Myodes [formerly Clethrionomys] gapperi), in 40 1.4-ha boreal mixedwood sites in Ontario, Canada. Using a neighborhood-scale modeling approach, we related red-backed vole capture locations to spatially referenced measures of overstory trees, shrubs and saplings, downed woody debris (DWD), and forest floor substrate. We further assessed how associations with these features varied with availability of the features within a site and as a function of stand management history. In spring, red-backed voles were associated with trap stations that had, within a 26-m radius, a dense shrub layer, abundant late-decay DWD, coniferous understory and litter, and possibly, understory vegetation associated with moist conditions. Positive associations with shrub cover, late-decay DWD, and a moisture-associated understory were most apparent in sites in which these elements were scarce (e.g., <1,500 stems/ha of hardwood saplings and short shrubs; <0.8% projected ground cover of late-decay DWD). The importance of late-decay DWD; shade-tolerant, coniferous understory composition; and substrate varied depending on a site's management history, with each feature having a strong positive effect in 47–64-year-old stands that were harvested using horse skidding and weaker effects in both 31–40-year-old stands that were clearcut with mechanical skidding and >80-year-old fire-origin stands. Our models of fine-scale habitat relationships for red-backed voles may be useful in establishing structural retention guidelines suitable for wildlife species dependent on late-successional habitat structure. In this regard, retaining abundant DWD and 10–30% live trees at harvest may be effective management strategies for providing favorable habitat conditions at localized scales.     

The numerical response of breeding Northern Saw-whet Owls Aegolius acadicus suggests nomadism

We used a 13-year time series of abundance estimates of breeding Northern Saw-whet Owls (Aegolius acadicus), and of small mammals from central Ontario, Canada, to assess the numerical response of the owls to small-mammal prey species. We found that the finite rate of increase of breeding owls was directly related to estimates of red-backed vole (Myodes gapperi) abundance. Thus, it appeared that the owls were nomadic, and made decisions about where to breed based on vole supply. The owls showed a much weaker response to deer mouse (Peromyscus maniculatus) abundance. Across all years, 55% of variation in owl rate of increase could be uniquely attributed to vole abundance, whereas only 3% could be attributed to mouse abundance. Consistent with the model of nomadism, there was only a weak relationship between the proportion of hatch-year owls caught at fall banding stations, and small-mammal abundance. Instead, it appeared that Northern Saw-whet Owls avoided years of widespread reproductive failure through the nomadic strategy of selecting breeding sites based on vole supply.