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.     

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.     

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.     

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.     

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.     

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.     

Circadian characteristics of corticosterone secretion in red-backed voles (Clethrionomys gapperi).

To provide necessary background for study of stress response in red-backed voles (Clethrionomys gapperi), the circadian and ultradian rhythm in corticosterone release was characterized. Animals were maintained under a 16h light, 8h dark cycle. A total of 55 males and 46 females provided 101 independent blood samples over a 6-month span. Samples were obtained at 1h to 2h intervals during the light and at 2h intervals during the dark. Using edited data (5 values beyond the upper 95% limit were removed), a significant time effect was found by analysis of variance (ANOVA) for both sexes at P < .001. The composite single cosine best describing the circadian wave-form for each sex consisted of three components (24h, 12h, and 6h), each significant at P < .05 (overall model P < .001). The 24h mean (mesor) was about 60% higher in females than males (646 ng/mL vs. 412 ng/mL, P = .01), with amplitudes of 429 and 298 ng/mL being proportional (66% vs. 72%) to the respective mesor. The predictable range of change within a 24h span (determined by the double amplitude of a 24h + 12h + 6h cosine model) was large: It was more than 1600 ng/mL for females and more than 900 ng/ mL for males. Highest values were found during the dark phase, with the 24h acrophase located at 2h into the dark span for both sexes. With the caveat of fewer samples obtained during dark than during light, the actual peak values for females occurred at 2h and for males at 6h into the 8h dark span. These results provide baseline information about the circadian time structure for serum corticosterone in red-backed voles under normal light-dark, low-stress conditions.     

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.     

Effects of cold,short day and melatonin on thermogenesis,body weight and reproductive organs in Alaskan red-backed voles

Summary This study examined whether cold, short day or melatonin causes reproductive regression and stimulates nonshivering thermogenesis in a subarctic rodentClethrionomys rutilus. Red-backed voles born and raised at 23°C and 22 h light per day (LD 22: 2) at Fairbanks, Alaska (65°N) were exposed in one of six groups to: 1) long day (LD 22:2), 23°C, injected daily with melatonin or saline 2 h before lights out, 2) long day, 3°C, injected daily with melatonin or saline, 3) short day (LD 8:16), 23°C or 3°C. Voles were tested for nonshivering thermogenesis (NST) prior to and after 8 wk exposure. Body weight, testes weight and female reproductive tract weight were assessed after 8 wk in long day and 12 wk in short day.NST was not altered by short day or melatonin but cold (3°C) caused an increase in NST which was similar in long day and short day.Body weight of males and females was not affected by short day but was decreased by melatonin.Short day did not alter mean testes weight (about 20% voles regressed) but reduced mean female reproductive tract weight (more than 40% voles regressed). Melatonin reduced testes weight and female reproductive tract weight (more than 50% of voles of both sexes regressed).The results suggest that in northern red-backed voles: 1) the pineal does not mediate seasonal changes in thermogenic capacity, 2) the pineal may mediate reduction of body weight and regression of reproductive organs but, in addition to daylength, other cues or factors may be important, 3) populations may exhibit variability in sensitivity of reproduction to photoperiod which could allow for opportunistic breeding.Abbreviations NST nonshivering thermogenesis - NE norepinephrine - RMR resting metabolic rate     

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.     

(鼲)属(啮齿目,仓鼠科)同域分布物种形态学鉴别特征组的筛选

现有的分类系统尚缺乏可用于减少䶄属物种种间鉴定不确定性的形态学鉴别特征。鉴于此,本研究旨在筛选出能够对同域分布的棕背䶄（Myodes rufocanus）, 红背䶄（M. rutilus）和堤岸䶄（M. glareolus）进行可靠鉴定的头骨形态指标和方法。为了达到以上目的,本文一方面筛选出能够用于种间鉴别的头骨和齿列形态特征,另一方面提出可用于鉴别以上三个物种的计算公式。对不同研究者提出来用于鉴别以上三个同域分布物种的35个特征进行筛选。头骨形态测量数据的获取需要花费较长的时间,而且结果变异很大。在本研究中,在分析中剔除15个形态特征,20个相对保守的特征被选择用于分析（包括来自头盖骨、牙齿和头骨其它部位的特征）。在20个特征中,有8个特征被选择出来,并使用Statistica 10 计算出判别公式。这些特征使准确鉴定不同个体各自所属种类成为可能。     

Effects of forage availability on growth and maturation rates in water voles

1. In populations of small mammals, food supplementation typically results in higher population densities, body weights, growth rates and reproductive rates. However, few studies have demonstrated a relationship between forage levels and demographic rates in wild populations in the absence of supplementation. 2. We examined the association of levels of available forage with individual growth rates and time to sexual maturity in eight re-introduced and three naturally occurring populations of water voles (Arvicola terrestris). 3. Range sizes were smaller at sites with higher population densities. Mean forage availability and individual growth rates covaried with range size at each site. 4. The weight at which water voles became sexually mature was 112 g for females and 115 g for males and did not vary between study sites. Differences in growth rates therefore translated into differences in the time taken to reach maturity between sites. 5. In the re-introduced populations, mean days to maturity varied inversely with mean range length. Females took 7 days (18%, range 40-47 days) longer and males 5 days (13%, range 40-45 days) longer to reach breeding condition at the sites with the shortest mean range lengths. 6. Evidence from this study suggests a possible mechanism by which increased population densities may reduce maturation rates in water voles through a reduction in mean range size, thereby limiting the availability of forage to each individual.     

Small Mammal Responses to Fine Woody Debris and Forest Fuel Reduction in Southwest Oregon

Abstract: Despite its importance for wildlife, most forests in the Pacific Northwest contain low volumes of large downed wood compared to fine woody debris (FWD). We used a replicated experiment to compare short-term responses of deer mice (Peromyscus maniculatus) and western red-backed voles (Clethrionomys californicus) among 3 arrangements of FWD: piled, lopped and scattered, and pile burning, a commonly used method of fuel reduction in commercial Douglas fir (Pseudotsuga menziesii) forests in southwest Oregon, USA. We assessed habitat use, density, and survival of mice and voles during 2 consecutive summers (Jun—Aug 1999 and 2000). Both mice and voles used FWD cover disproportionately from its availability, and they differed in their responses to specific FWD arrangements. Mice used piled FWD (proportional use = 37.0%, 90% CI = 33.0–44.0) 43% more than expected (26.0). Number of mice captured (x̄ = 1.9 mice, 90% CI = 1.5–2.5) and index of home range size (x̄ = 4.8 m, 90% CI = 0.7–8.9) at individual FWD piles decreased up to 16% and increased up to 50%, respectively, for each 1-m increase in distance from piles. Voles used all FWD cover classes in proportion to availability, but number of voles captured increased slightly (x̄ = 0.016 voles/m, 90% CI = 0.001–0.031) for each 1-m increase in distance from piles. Piled FWD had no discernable effect on population density and apparent survival of mice, but analyses had low power (0.25, 0.67). Our results suggest that piling FWD would benefit deer mice, whereas lopped and scattered FWD might benefit voles. Thus, a combination of methods to reduce fire risk should be considered to accommodate multiple small mammal species. (JOURNAL OF WILDLIFE MANAGEMENT 72(3):625–632; 2008)     

Protein polymorphisms and their genetic control in the red-backed vole, Clethrionomys rufocanus bedfordiae

Twenty enzymatic and non-enzymatic proteins in a wild population of red-backed voles, Cletrionomys rufocanus bedfordiae , were investigated by electrophoresis. Seven enzymatic and non-enzymatic protein systems were found to be polymorphic. Breeding data indicated that the mode of inheritance of the enzyme systems ME-1, ME-2, GPD and EST were consistent with a Mendelian law. Two systems, 6 PGD and SOD, were estimated to be genetically controlled from the electrophoretic patterns and mother-offspring comparison of phenotypes. In the Tf system two new additional phenotypes were observed, but their inheritance could not be elucidated. Gene frequencies at seven loci were also investigated in 88 animals. There was no significant deviation from Hardy-Weinberg equilibrium.     

Parental care in captive red-backed vole (Clethrionomys rutilus)

Parental behavior in ten pairs of male and female red-backed voles, Clethrionomus rutilus, was studied under laboratory conditions. Significant sex differences were found in total time spent in the nest, time spent by adults alone in the nest, grooming time, and nest-building activity; in half of the males under study, the level of paternal care was extremely low. These findings indicate different paternal contributions of female and male red-backed voles into the rearing of young, in agreement with the spatial-ethological structure of populations of this species. Parental behavior of C. rutilus is discussed in comparison with that of other species of the subfamily Microtinae.     

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.     

Small Mammal Mycophagy Response to Variations in Green-Tree Retention

Abstract: We studied the effects of 6 green-tree retention levels and patterns on the diets of northern flying squirrels (Glaucomys sabrinus), Townsend's chipmunks (Tamias townsendii), Siskiyou chipmunks (T. siskiyou), western red-backed voles (Myodes californicus), and southern red-backed voles (Myodes gapperi) using fecal pellet analysis. These rodents are truffle spore dispersers and prey for forest predators such as the northern spotted owl (Strix occidentalis caurina). Pretreatment diets showed differences in truffle and plant consumption among genera. Tree harvesting, especially in the 15% aggregated retention pattern, reduced frequency of Rhizopogon spores in the diet of voles, which may reflect a reduced ability of these animals to forage for Rhizopogon truffles, a decreased access to these truffles, or a reduction in Rhizopogon truffle abundance or frequency. Habitat island effects and edge effects provide conceptual frameworks for the reduction in consumption of Rhizopogon truffles by voles in green-tree aggregates. Overall, small mammal consumption of truffles showed little change in response to the treatments. Animals may be compensating for a locally declining food source by altering their foraging behavior. The long-term effect of this postulated behavioral compensation on small mammal energetics and population dynamics is unknown. Forest managers may reduce the impact of tree harvesting on these key forest ecosystem components by including green-tree aggregates within a dispersed retention matrix.     

Diet selection by red-backed voles<Emphasis Type="Italic">Clethrionomys gapperi</Emphasis>

Food supplementation studies often assume that animals will select artificial diets in their natural environment, and that high-protein, high-energy foods are the most appropriate supplement. These assumptions were tested in red-backed volesClethrionomys gapperi Vigors, 1830 using food-choice experiments with sunflower seeds, oats, and commercial diets in the laboratory and field. Preferred level of dietary protein was also examined using isocaloric diets that varied only in protein content (14%, 20% and 30%). Preferences exhibited in the above trials were subsequently examined relative to natural forage. Voles demonstrated a strong preference for sunflower seeds over oats, dried alfalfa, and rabbit, guinea pig, rat and cat food. Voles preferred the 14% protein diet over the 20% and 30% protein diets. Although sunflower seeds contain more than 20% protein, voles consistently preferred this food over natural forage, perhaps because of their high fat and energy content. This indicates that tradeoffs in protein content may be made to maximize energy. We suggest that red-backed voles will select sunflower seeds in their natural environment, and that their preference for low protein likely reflects their herbivorous diet. This study highlights the importance of ana priori understanding of species-specific preferences and requirements when designing food supplementation studies.     

The influence of weather on habitat use by small mammals

Summer habitat use by three species of forest small mammals was determined using tracking stations Nocturnal weather influenced habitat selection by deer mice and woodland jumping mice but not by red-backed voles Deer mice used all habitats equally on clear nights but were most active in mixed forest on cloudy, rainless nights and most active in a coniferous habitat on rainy nights Jumping mice were most active in mixed forest on clear and rainy nights but shifted to coniferous forest on cloudy dry nights Red-backed voles were most active in the coniferous habitat regardless of weather Microhabitat references within habitats reflected the same preferences as habitat selection Microhabitat selection by jumping mice also changes with weather The mechanism most likely responsible for the observed habitat selection changes is changing insect abundance associated with cloud cover and rainfall