The biology of the voleClethrionomys rufocanus: A review

The biology of the gray-sided voleClethrionomys rufocanus in Hokkaido, concerning taxonomy, morphology, phylogeny, distribution, and natural history, is reviewed. Applied issues in forest management (damage, control and census) are also mentioned. AlthoughClethrionomys rufocanus of Hokkaido was originally identified as a distinct species,Evotomys (=nowClethrionomys) bedfordiae Thomas, 1905, current literature generally refers to the gray-sided vole of Hokkaido asClethrionomys rufocanus or asC. rufocanus bedfordiae (vernacular name, the Bedford’s red-backed vole). The gray-sided vole is the most common small mammal in Hokkaido. It inhabits open areas as well as forests, and mainly feeds on green plants. The gray-sided vole has a high reproductive potential; litter size: 4–7; gestation period: 18–19 days; maturation age: 30–60 days old. Although spring-born individuals usually attain sexual maturity in their summer/fall of birth, their maturation is sometimes suppressed under high densities. The breeding season is generally from April to October, but with some regional variation.Clethrionomys rufocanus has a rather specialized diet (folivorous), particularly during winter when it feeds on bamboo grass. Many predators specialize on the grey-sided vole in Hokkaido; even the red fox, which is a typical generalist predator, selectively feeds on this vole. Damage by voles’ eating bark used to be sever on forest plantations in Hokkaido. Censuses of small rodents have been carried out for management purpose since 1954.     

Reproductive investment under fluctuating predation risk: Microtine rodents and small mustelids

Summary We studied the reproductive investment of microtine rodents (bank vole (Clethrionomys glareolus),Microtus epiroticus andMicrotus agrestis) in western Finland under predation risk from small mustelids. During 1984–1992, the yearly mean litter size of overwintered bank voles was smaller at high least weasel and stoat densities than at low densities (close to 3 versus 4–5). In addition, the annual mean litter size of young bank voles was negatively correlated to the least weasel density. In youngM. agrestis voles, the yearly late summer litter size was negatively associated with the autumn density of small mustelids. In the crash phase of the vole cycle (1989 and 1992), we removed small mustelids (mainly least weasels) from four unfenced areas in late April to late May and studied the reproduction of voles in four removal and comparable control areas (each 2–4 km²). Reduction of small mustelids significantly increased the proportion of pregnant bank vole females, but not that of pregnantMicrotus vole females. We conclude that predation risk apparently reduced reproductive investment of free-living bank vole females; these voles appear to trade their current parental investment against future survival and reproductive prospects. Accordingly, the presence of small mustelids (or their scent) may slow down the reproductive rate of voles. As antipredatory behaviours occurred on a large scale, our results add evidence to the hypothesis that crashes in multiannual vole cycles are driven by small mustelid predators.     

Hypothalamo-pituitary neurosecretory system of the Northern redbacked vole Clethrionomys rutilus in the course of population cycle

Hypothalamo-pituitary neurosecretory system (HPNS) of the Northern redbacked vole, Clethrionomys rutilus was studied at different stages of the population cycle using paraldehyde-fuchsin staining and immunohistochemical revealing of vasopressin and oxytocin. We found at the stages of high voles number (peak and recession), an increase of vasopressin synthesis in the neurosecretory cells (NSC) of paraventricular (PVN) and supraoptic (SON) nuclei, as well as its active transport and release to the portal capillaries of the outer zone of median eminence (ME). At the stages of low voles number (depression and growth) was demonstrated that level of oxytocin synthesis in the NSC of SON was high and moderate in the NSC of PVN, which was accompanied by an extensive release of oxytocin to capillaries of the posterior pituitary (PP). Increased supply of vasopressin to portal blood flow of the vole pituitary in conditions of overpopulation is suggested to have highly stimulating influence on adrenocorticotropic function of pituitary, which negatively affects the reproductive function of the voles and leads to a decrease of their number. At the stages of low number of population in conditions favoring the life of the voles, the increased supply of oxytocin to the systemic blood flow stimulates the reproductive behavior of the voles, which results in rise of their population during this period.     

Functional features of microbial communities in the digestive tract of field voles (Microtus rossiaemeridionalis and Clethrionomys glareolus)

The nitrogen-fixating and cellobiohydrolase activity, the nitrogen (N) and carbon (C) contents, and the number of microorganisms in the prestomach, cecum, and colon of two vole species were studied: the southern vole (Microtus rossiaemeridionalis) and the bank vole (Clethrionomys glareolus), which is characterized by a mixed type of diet. The nitrogen-fixating activity in the cecum was found to be the highest in the voles compared with the mammals studied earlier. The seasonal dynamics of both nitrogenase and cellobiohydrolase activities was registered in the southern vole. The structure of the microbial complex in the southern vole is more varied and includes microorganisms associated with plant substrates.     

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.     

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.     

Reproductive compatibility of voles from separate continents (Mammalia: Clethrionomys

The North American Red-backed vole, Clethrionomys gapperi , and the Eurasian Bank vole, C. glareolus , are probably derived from a common ancestor. They have been isolated from each other for a minimum of 20,000 generations, probably many more. Interbreeding experiments in the laboratory show that in that time only partial reproductive isolation has developed. They interbreed as frequently as do pure strain pairs, and produce litters of approximately the same size. Hybrids exhibit reduced viability, but this may be partly an artifact produced by the laboratory rearing conditions. If they ever made contact in nature the most likely outcome appears to be selection against hybrids leading to full speciation and the establishment of contiguous allopatry. It is recommended that they be considered semispecies, in the terminology of Mayr (1963), and retain their separate names.     

Determinants of reproductive success in voles: space use in relation to food and litter size manipulation

Spacing behaviour of female mammals is suggested to depend on the distribution and abundance of food. In addition, food limitation has been found to constrain the reproductive success of females. However, whether females maximize their reproductive success by adjusting space use in relation to current food availability and reproductive effort (e.g. litter size) has not been experimentally studied. We examined these questions by manipulating simultaneously food resources (control vs. food supplementation) and litter sizes (control vs. plus two pups) of territorial female bank voles (Clethrionomys glareolus) in large outdoor enclosures. Females with supplementary food had smaller home ranges (foraging area) and home range overlaps than control females, whereas litter size manipulation had no effect on space use. In contrast, the size of territory (exclusive area) was not affected by food supplementation or litter size manipulation. As we have previously shown elsewhere, extra food increases the reproductive success of bank vole females in terms of size and proportion of weaned offspring. According to the present data, greater overlap of female home ranges had a negative effect on reproductive success of females, particularly on survival of offspring. We conclude that higher food availability increases the reproductive success of bank vole females, and this effect may be mediated through lower vulnerability of offspring to direct killing and/or detrimental effects from other females in the population. Moreover, it seems that when density of conspecifics is controlled for, home range sizes of females, but not territoriality, is related to food resources in Clethrionomys voles.     

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

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

Morphofunctional analysis of testes and sperm in the assessment of male reproductive success in the bank vole (Clethrionomys glareolus)

The morphofunctional analysis of testes and sperms in bank vole (Clethrionomys glareolus, Schreber, 1780) from a natural population is carried out to assess the reproductive potential of animals. It is shown that the reproductive success of males depends on the density of the population. Under physiological stress, such as a ??peak?? of the population size, the animals, against a background of accelerated aging, have activation of the hypothalamic-pituitary-adrenal axis, which contributes to oppression of the spermatogenesis process. The absolute weight of the testes is not always the determining factor in assessing the fertility of the animal. The informative indicators of the reproductive success of males and the population as a whole include the level of destructive changes in the endocrine and germinal regions of morphological defects of the testis and sperm.     

A possible discrepancy between the exposed and the whole population depending on range-size and trap-spacing in vole populations

Population Ecology - From a field study for the vole population (Clethrionomys rufocanus) in Hokkaido in the late summer of 1965, it has been proved that the range length may decrease from 25 to 18...     

Annual variation in hematological indices in a fluctuating population of bank vole (<Emphasis Type="Italic">Clethrionomys glareolus</Emphasis>)

The quantitative and structural hematological indices were studied in bank vole in different reproductive states (overwintered individuals, mature underyearlings, and immature underyearlings) in different years corresponding to different phases of the population cycle. The annual changes in certain hematological indices have been revealed for each reproductive state irrespective of the population cycle phase.     

Adaptation of the bank vole (Clethrionomys glareolus Schreber) to conditions of biogeochemical province with abnormally high content of nickel, cobalt and chromium

Morphophysiological characteristics and peculiarities of adrenal gland of bank vole (Clethrionomys glareolus) were studied in the area of natural biogeochemical province with abnormally high content of nickel, cobalt and chromium. The control population inhabited area with usual content of these elements. We used 4-factor analysis of variance to estimate the influence of geochemical conditions, phase of population cycle, sex and reproductive state on the morphophysiological characteristics of animals and functional activity of adrenal gland. Animals from area with high concentration of Ni, Co and Cr show an increase in relative mass of adrenal glands, fascicular zone of adrenal cortex, size of cells and their nuclei. All these changes can be considered as an evidence of increased secretion of glucocorticoids. It is shown that phase of population cycle influences fatness of animals, size of nuclei, cells and adrenal cortex. Females in comparison with males are characterized with higher indexes of liver and adrenal gland, as well as morphometric indexes of adrenal cortex. The maturation of animals is accompanied with increase in body mass, fatness and relative mass of adrenal glands, the size of cortex zone, nuclei and cells themselves. It is supposed that the effect of "geochemical factor" results in intensification of glucocorticoid secretion of adrenal costex, thus increasing non-specific resistance of animals inhabiting area with high concentration of heavy metals. Such factors as "phase of population cycle", "sex" and "reproductive state", influence mineralocorticoid activity, glucocorticoid and androgenic functions of adrenal cortex. Some factors show synergetic effect.     

Studies on the helminth parasites of voles and shrews from Wales

The incidence and degree of infestation of the Bank vole, Clethrionomys glareolus , the Skomer vole, C. skomerensis , the Common shrew, Sorex araneus and the Pygmy shrew, S. minutus have been studied from a rough grassland and woodland area, Aberystwyth and from Skomer Island in Wales. In addition, small numbers of the Short-tailed vole, Microtus agrestis and the Water shrew, Neomys fodiens were examined for helminth parasites, when they became available. Seven new host records and six new British records are listed. The number of species of helminths in shrews, which consisted largely of digeneans and cestodes, was greater than that in voles. This is undoubtedly linked with differences in the feeding habits of the two hosts.
In Aberystwyth, where the composition of the helminth fauna was found to be more varied than that from Skomer Island, one species of nematode showed evidence of seasonal variation in the degree of infestation of Clethrionomys glareolus and four species, one digenean, two cestodes and one acantocephalan in Sorex araneus. The factors affecting this seasonal fluctuation in parasite numbers are discussed.     

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.     

Environmental fluctuations facilitate species co-existence and increase decomposition in communities of wood decay fungi

Correlations between mast fruiting of bilberry Vaccinium myrtillus and peak levels of Clethrionomys-voles have been reported from both Norway and Finland, but there has been a discussion whether this is a bottom-up or a top-down relationship. In a multiple regression model, 65% of the variation in a bilberry production index calculated from game reports from southern Norway 1932–1977 could be explained by the berry index of the two preceding years and climate factors acting during key stages of the flowering cycle. High vole populations in previous years did not contribute to explain the fluctuation in berry production. I used the selected model and climate data to predict bilberry production for the period 1978–2004. Predicted berry indices of the current and previous year explained 38% and the total amount of precipitation in May–June explained 16% of the variation in a log-transformed snap-trapping index of bank vole Clethrionomys glareolus 1980–2004. The vole index was not related to any of the climate variables used to predict berry production. This pattern supports the hypothesis that vole cycles are generated by changes in plant chemistry due to climate-synchronized mast fruiting.     

The factors influencing the sound activity of forest voles]

The article is devoted to the effect of context on the acoustic activity of bank voles of 4 species (Clethrionomys glareolus, C. centralis, C. rutilus, and C. rufocanus) living in experimental groups. In addition to species differences and social state of a specimen in the group, the acoustic activities of vole is affected by such factors as locomotor activity of the vole itself and its partners (especially dominant ones) and aggression of surrounding voles.     

Variations of Some Physiological and Biochemical Indices in the Population of Red-Backed Vole (Clethrionomys rutilus)

We studied the changes in the population density of the red-backed vole (Clethrionomys rutilus Pall.) on the northern coast of the Sea of Okhotsk (60° N) during three population cycles (1980–1990). A total of 3111 animals were studied, including 1006 alive voles. For evaluation of the population stress and food deficit, a complex of biochemical (blood level of glucose and liver levels of glycogen and lipids) and physiological (blood content of leucocytes, spleen weight, etc.) indices was used. At a high population density, the influence of stress continues during the reproductive period, after its termination, and, supposedly, until the beginning of a new reproductive period, while at a low population density, the consequences of stress were expressed only in the second half of the reproductive period. The signs of starvation were recorded only in some semiadult voles in a high density population. It has been confirmed that stress acts as a mechanism involved in regulation of the population density of small rodents.     

Seasonal variation of immune response to heterologous erythrocytes in natural populations of red‐backed (Clethrionomys rutilus) and gray‐sided (C. rufocanus) voles in Western Siberia

We studied the seasonal variation of adaptive humoral immunity (AHI) in northern red‐backed vole (Clethrionomys rutilus Pallas, 1779, RBV) and gray‐sided vole (C. rufocanus Sundevall, 1846, GSV) in Tomsk region of Western Siberia. Immunoresponsiveness (IR) to sheep red blood cells was assessed by the number of antibody‐producing cells in the spleen. The use of a generalized linear model to analyze the effects of species, sex, year of research, and season of withdrawal of individuals from nature on IR showed a significant effect of species identity, season of animal capture, and the interaction of species with season. The RBV demonstrated higher immune responses during a year, and both species had higher IR in winter. Suppression of IR in spring was greater, started earlier, and lasted longer (March–May) in GSV. In RBV, immunosuppression was restricted to April. The significant negative within year correlations of IR with body mass and masses of reproductive organs in GSV indicated a trade‐off between AHI and growth and reproduction processes. A probable explanation for the difference between species in the seasonal variation of AHI may be related to the difference in tropho‐energetic requirements of each vole species. GSV is a predominantly herbivorous rodent and its thermoregulation seems less efficient than of RBV. The deeper spring immunosuppression in GSV may explain in part its higher mortality during the season of colds.     

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.