Historical biogeography at the crossroads of the northern continents: molecular phylogenetics of red-backed voles (Rodentia: Arvicolinae)

Evolutionary relationships of red-backed voles and their relatives were examined and used to test biogeographic hypotheses. Sequences of the mitochondrial cytochrome b gene were obtained for 25 individuals representing Alticola macrotis, Clethrionomys californicus, C. gapperi, C. glareolus, C. rutilus, and C. rufocanus. These were combined with 21 partial sequences from GenBank for C. regulus, C. rex, C. rufocanus, C. rutilus, Eothenomys imaizumii, E. melanogaster, Phaulomys andersoni, and P. smithii. Complete sequences of three species of Microtus (M. montanus, M. oeconomus, and M. pennsylvanicus), representative species of other arvicoline genera (Myopus, Synaptomys, Arvicola, Ellobius, Ondatra, Lemmus, Dicrostonyx, and Phenacomys), and a sigmodontine representative (Peromyscus) were included as outgroups. We used maximum parsimony, maximum likelihood, distance, and Bayesian based methods and conducted statistical tests on proposed hypotheses of phylogenetic relationships and biogeographic histories. A close relationship of species representing the genera Alticola, Clethrionomys, and Eothenomys was supported (Clethrionomyini); however, the genus Clethrionomys was paraphyletic with respect to both Alticola and Eothenomys. Three major clades were identified as Asian (Eothenomys andersoni, E. smithii, C. rex, C. regulus, and C. rufocanus), Trans-beringian (Alticola macrotis, C. californicus, C. gapperi, C. glarelolus, and C. rutilus), and Taiwanese (E. melanogaster). These results are consistent with the fossil record which indicates an initial diversification in Asia followed by colonization of the Nearctic on at least two occasions. The holarctic species, C. rutilus, appears to have either reinvaded Asia from North America or colonized North America more recently (late Pleistocene) than the two species of Clethrionomys (C. gapperi and C. californicus) that are endemic to North America (early to mid-Pleistocene). Finally, C. gapperi, appears to be comprised of an eastern and a western species, the former with affinities to the Asian C. glareolus and the latter more closely related to C. californicus.     

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.     

Gene-geographical variation and genetic differentiation in red-backed voles of the genus Clethrionomys (Rodentia,Cricetidae) in the Okhotskii region

Thirteen enzyme systems and three nonenzyme proteins were electrophoretically analyzed in red-backed voles of the genus Clethrionomys. In total, 25 loci were interpreted. Gene-geographic variation was studied and indices of genetic variability and differentiation were determined. By the distribution of electrophoretic variants of hemoglobin, C. rutilus was shown to be divided into two geographical groups (northern and southern). A low level of genetic differentiation was revealed in the island isolates of C. rutilus and C. rufocanus. Separation of C. rufocanus, C. rex, and C. sicotanensis into a superspecies complex was confirmed. A study of differential G- and C-banding on C. rutilus and C. rufocanus chromosomes did not reveal intraspecific variation of autosomes. In these species, karyotypes of voles from Kamchatka Peninsula were studied for the first time. They appeared to be morphologically similar to the karyotypes continental voles by both autosomes and sex chromosomes.     

紫貂冬季食性的分析

１９９１至１９９８年的三个冬季,在大兴安岭地区共收集紫貂粪样２２３个．食性分析结果表明,紫貂冬季食物主要为小型哺乳类（５４．１％）、植物浆果和种子（３２．４％）、鸟类（１２．５％）和昆虫（１．０％）．在紫貂选择的７种小型哺乳类中,主要以棕背（２７．３％）和红背（１９．２％）为食,其次为雪兔和冬眠的花鼠。对于鸟类,紫貂主要捕食花尾榛鸡（８．１％）,松鸦（０．７％）,大山雀（０．５％）和黑啄本鸟等。有２．２％的粪样中含有小型鸟的卵壳、紫貂的植物性食物主要为越桔浆果（２０．８％）和偃松种籽（８．８％）。昆虫中只有蚂蚁在紫貂食性中出现（１．０％）．紫貂冬季食物构成没有年度间差异（Ｐ＞０．０５）。通过捕食迹,我们还发现紫貂捕食黑嘴松鸡。虽然红背的捕获率（７９．４％）高于棕背（２．９％）,但食性分析结果却相反,说明紫貂更喜欢捕捉身体较大的鼠类。有较强气味的中虽有一定的数量,但在紫貂冬季食物中未出现过。     

Molecular phylogeny and biogeography of Oriental voles: genus Eothenomys (Muridae, Mammalia)

Oriental voles of the genus Eothenomys are predominantly distributed along the Southeastern shoulder of the Qinghai-Tibetan Plateau. Based on phylogenetic analyses of the mitochondrial cytochrome b gene (1143 bp) obtained from 23 specimens (eight species) of Oriental voles collected from this area, together with nucleotide sequences from six specimens (two species) of Japanese red-backed voles (Eothenomys andersoni and Eothenomys smithii) and five species of the closely related genus Clethrionomys, we revised the systematic status of Eothenomys. We also tested if vicariance could explain the observed high species diversity in this area by correlating estimated divergence times to species distribution patterns and corresponding paleo-geographic events. Our results suggest that: (1) the eight species of Oriental voles form a monophyletic group with two distinct clades, and that these two clades should be considered as valid subgenera--Eothenomys and Anteliomys; (2) Eothenomys eleusis and Eothenomys miletus are not independent species; (3) Japanese red-backed voles are more closely related to the genus Clethrionomys than to continental Asian Eothenomys taxa; and (4) the genus Clethrionomys, as presently defined, is paraphyletic. In addition, the process of speciation of Oriental voles appears to be related to the Trans-Himalayan formation via three recent uplift events of the Qinghai-Tibetan Plateau within the last 3.6 million years, as well as to the effects of the mid-Quaternary ice age.     

棕背(鼠平)和红背(鼠平)种间区分的分子方法

棕背鼠平(Myodes rufocanus)和红背鼠平(M.rutilus)的分布有重叠区且外形相似,在特定情况下存在种间区分困难,给两种鼠的数量调查带来不便和误判.本研究通过mtDNA控制区构建系统树、mtDNA控制区电泳和RAPD 3种分子生物学方法有效地对棕背(鼠平)和红背(鼠平)已知的8个样本和16个待定样本进行了准确鉴定.其中,mtDNA控制区电泳进行种问区分的方法具有简便、准确而又快捷的优点.     

Multi-annual density fluctuations and habitat size enhance genetic variability in two northern voles

In order to gain a better understanding of the consequences of population density cycles and landscape structure for the genetic composition in time and space of vole populations, we analyzed the multiannual genetic structure of the two numerically dominant, sympatric small rodent species of northernmost Fennoscandia. Red voles Myodes rutilus and grey-sided voles M. rufocanus were trapped in the subarctic birch forest along three fjords over five years. Along each fjord, there were four or five altitudinal transects each with five trapping stations. Spring and fall population densities were estimated from mark–recapture data. Grey-sided voles exhibited higher amplitude density fluctuations than red voles. Polymorphism at eight or nine microsatellite loci, determined in 1228 voles, was used to estimate local genetic diversity and differentiation among samples. Genetic diversity was higher in grey-sided voles than in red voles. Spring densities had no effect on local genetic diversity or on differentiation. The amplitude of density fluctuations and the extent of favorable habitat (sub-arctic birch forest) surrounding each site had a positive effect on genetic diversity, and the amplitude of density fluctuations had a negative effect on differentiation in red voles, for which fluctuating populations were compared with more stable populations. The harmonic mean of densities, reflecting average population sizes, had a negative effect on genetic diversity in red voles, but a positive effect in grey-sided voles, for which only fluctuating populations were compared. No other effects were significant for grey-sided voles. A temporal assignment test showed that the spatial structure was more stable in time for populations with more stable population dynamics. Altogether our results suggest that high amplitude density fluctuations lead to more gene flow and higher genetic diversity in vole populations.     

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.     

Laboratory breeding of the red-backed vole (Clethrionomys rufocanus bedfordiae)]

Laboratory matings were attempted to establish breeding colonies of red-backed voles (Clethrionomys rufocanus bedformidae) as experimental animals. For these mating, 10 pairs of red-backed voles which were captured in the Tohbetsu region of Hokkaido, Japan and their litters were used. In the results for two years, 1987 to 1988, the rates of pregnancy, birth and weaning were 35.4%, 94.5% and 79.5%, respectively. The mean litter size was 5:1 +/- 1.6 with a range of 1 to 9. The mean gestation period was 20.0 +/- 0.7 days with a range of 18 to 22. These results suggest that planned production of red-backed voles in the laboratory is possible. To determine intraregional variations of red-backed voles with a view to the establishment of a strain by inbreeding, restriction patterns of mitochondrial DNAs using seven restriction endonucleases were compared. Four different patterns were obtained from wild red-backed voles used in the present study.     

Seasonal changes in the energy metabolism of subarctic rodents

In widespread species, northern taiga voles, most significant differences in the intensity of energy metabolism (M), maximum (Mmax) and reserve (Mres) metabolism were observed at winter temperatures (-5-20 degrees C): Clethrionomys rutilus greater than C. rufocanus greater than Microtus oeconomus; differences in seasonal increase of Mmax and Mres exhibit an inverse proportion. Seasonal changes in M and Mmax in autochthonous tundra rodents indicate that Lemmus sibiricus belongs to a more eurybiont species as compared to Dicrostonyx torquatus. The main characteristic feature of seasonal adaptation of M in lemmings, as compared to voles, is the evident decrease of M value in winter which is accompanied by a more significant increase of Mmax and Mres. Operative pattern and high seasonal mobility of chemical thermoregulation in lemmings are suggested which account for adaptation of these animals mainly to short-term extreme effects of low temperatures.     

森林生态系统中5种啮齿动物秋季时间生态位

为探讨森林啮齿动物共存机制,于2006年9月,在黑龙江省海林林区,采用标志重捕法和室内饲养观察法研究了松鼠(Sciurus vulgaris)、花鼠(Eutamias sibiricus)、大林姬鼠(Apodemus peninsular)、棕背(Myodes rufocanus)和红背(M.rutilus)时间利用生态位以及种间的生态位叠度,分析了在资源利用时间上的分化。结果表明,这5种动物分化为白天活动和以夜间活动为主的两种生态类型。白天活动的松鼠、花鼠生态位宽度较窄,分别为0·679、0·618。以夜间活动为主的棕背、红背、大林姬鼠的生态位宽度较宽,分别为0·935、0·853、0·844。两种类型间竞争较小,生态位叠度指数在0·286以下。同一类型内种间生态位叠度指数较高,在0·711以上,为了减少竞争,同一类型内种间错开活动高峰时间或延长活动时间。     

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.     

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.     

Chromosomal mechanisms underlying the karyotype evolution of the oriental voles (Muridae, Eothenomys)

We have investigated the karyotype relationships of two oriental voles, i.e. the Yulong vole (Eothenomys proditor, 2n = 32) and the large oriental vole (Eothenomys miletus, 2n = 56) as well as the Clarke's vole (Microtus clarkei, 2n = 52), by a combined approach of cross-species chromosome painting and high-resolution G-banding comparison. Chromosome-specific painting probes were generated from flow-sorted chromosomes of E. proditor and hybridized onto metaphases of E. proditor, E. miletus and M. clarkei, leading to the establishment of genome-wide comparative chromosome maps. Our results demonstrate that Robertsonian translocations (centric fusions) have played a major role in the karyotype evolution of oriental voles with no obvious evidence for the involvement of tandem fusions as proposed previously and that the genome organizations of vole species are highly conserved. The comparative chromosome maps of these three vole species belonging to two phylogenetically distinct genera provide a framework for future studies on the karyotype evolution in voles.     

Patterns of coexistence: ectoparasites on small mammals in northern Fennoscandia

The total aestival ectoparasitic burden of six small mammal species ( Sorex araneus, Clethrionomys glareolus, C. rutilus, C. rufocanus, Microtus agrestis , and M. oeconomus ) was investigated in terms of frequency distribution, frequency of occurrence, species diversity and joint occurrences. The mammals were collected in northern Fennoscandia during peak density years. The frequency distribution of the ectoparasites was best described as negative binomial on C. glareolus, M. agrestis , and M. oeconomus but not so on S. araneus, C. rutilus and C. rufocanus. The distribution did not fit the Poisson distribution in any species. The percentage of S. araneus that had ectoparasites was 49%, and of the microtidae species, 73-96% had ectoparasites. The median number of ectoparasites on the vole species was between 2 and 9 specimens of 1 or 2 species. There was a significant, positive correlation between the number of ectoparasitic species and the total number of individuals on all host species. Pairs of ectoparasitic species occurring together more or less often than expected by chance were found on all host species. However, the pairs rarely repeated themselves on the same host species under different environmental conditions, or on other host species under similar circumstances. Differences in total infestation between reproductive categories and sexes were observed in M. agrestis but not in S. araneus and C. glareolus.     

A New Species of Chigger Mite (Acari: Trombiculidae) from Rodents in Southwest China

This paper describes a new species of chigger mite (Acari: Trombiculidae), Gahrliepia cangshanensis n. sp., from rodents in southwest China. The specimens were collected from Yunnan red-backed voles, Eothenomys miletus (Thomas, 1914), and a Chinese white-bellied rat, Niviventer confucianus (Milne-Edwards, 1871) in Yunnan Province. The new species is unique mainly in its number of dorsal setae (n=21), and it has the following features: fT (formula of palpotarsus)=4B (B=branched), fp (formula of palpal seta)=B/N/N/N/B (N=naked), a broad tongue-shaped scutum with an almost straight posterior margin, and 17 PPLs (posterior posterolateral seta) with a length of 36-43 µm. This chigger mite may also infect other rodent hosts and may be distributed in other localities.     

Mode of infection of Hokkaido virus (Genus Hantavirus) among grey red-backed voles, Myodes rufocanus, in Hokkaido, Japan

Hokkaido virus (HOKV) is a member of the genus Hantavirus, in the family Bunyaviridae. To investigate HOKV infection in the host Myodes rufocanus, the grey red-backed vole, 199 animals were captured at Tobetsu (October 2004 and July 2005) and Nakagawa (October 2004) in Hokkaido, Japan, for detection of antibody, antigen, and viral RNA. In the surveys in Tobetsu (2004) and Nakagawa (2004), seropositive animals were detected at a frequency of 6.0% (5/84) and 10.4% (5/48), respectively. No seropositive animals were detected in Tobetsu in 2005. Seroprevalence in males in Tobetsu and Nakagawa in 2004 was 25% (1/4) and 45.5% (5/11), respectively, which was higher than in females, at 5.0% (4/80) and 0% (0/37), respectively (P<0.01). These results suggest that male animals play an important role in the maintenance of HOKV in M. rufocanus. Two females were seronegative but viral RNA-positive, indicating that these animals had acute infections before antibody was produced. Another five infected animals in Nakagawa were all male and had high levels of antibodies and viral RNA, suggesting that they had persistent infections. Viral RNA copies in organs of infected animals in Nakagawa were quantified by real-time polymerase chain reaction. Two acutely infected animals had > or = 10 times the number of RNA copies in their lungs compared to those of persistently infected animals. In most cases, lungs or spleen had the highest RNA copy number, regardless of infection status.     

Behaviour and resource use of two competing vole species under shared predation risk

Indirect interaction between two competing species via a shared predator may be an important determinant of population and community dynamics. We studied the effect of predation risk imposed by the least weasel Mustela nivalis nivalis on space use, foraging and activity of two competing vole species, the grey-sided vole Myodes rufocanus, and the bank vole Myodes glareolus. The experiment was conducted in a large indoor arena, consisting of microhabitat structures providing food, shelter, trees for refuge and separated areas with high and low predation risk. Voles were followed for 5 days: 2 days before, 1 day during and 2 days after the presence of weasel. Our results suggest an effect of weasel presence on the vole community. Voles of both species shifted their activity from risky to less risky areas, climbed trees more often and were less active. Seed consumption was not affected by weasel presence. The time spent in the risky and less risky area did not differ between species, but bank voles spent more time in trees than grey-sided voles. Males of both species were more exposed to predation risk than females, i.e. generally spent more time in the risky area. Proportion of time spent in the risky area, the use of area, trees and food stations were sex dependent. Activity and use of trees were species dependent. We found no evidence for despotic distribution between our two species, although bank voles seemed to be more affected by coexistence, since they lost weight during the experiment. Based on our results we conclude that predator response was largely similar between species, while the sex-specific responses dominated. Besides a stronger escape response in the bank vole, the strongest individual differences were sex specific, i.e. males were more prone to take risks in space use and activity.