Clethrionomys Species Research Articles

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.

Variation in mitochondrial DNA control region haplotypes in populations of the bank vole, Clethrionomys glareolus, living in the Chernobyl environment, Ukraine

Bank vole, Clethrionomys glareolus, specimens have been annually sampled from the radioactive Chernobyl, Ukraine, environment and nonradioactive reference sites since 1997. Exposed voles continually exhibit increased mitochondrial DNA haplotype (h) and nucleotide diversity (ND), observed in the hypervariable control region (1997-1999). Increased maternal mutation rates, source-sink relationships, or both are proposed as hypotheses for these differences. Samples from additional years (2000 and 2001) have been incorporated into this temporal study. To evaluate the hypothesis that an increased mutation rate is associated with increased h, DNA sequences were examined in a phylogenetic context for novel substitutions not observed in haplotypes from bank voles from outside Ukraine or in other species of Clethrionomys. Such novel substitutions might result from in situ mutation events and, if largely restricted to samples from radioactive environments, support an increased maternal mutation rate in these areas. The only unique substitution meeting this criterion was found in an uncontaminated reference site. All other substitutions are found in other haplotypes of the bank vole or in other species. Increased maternal mutation rates do not appear to explain trends in h and ND observed in northern Ukraine. Studies examining ecological dynamics will clarify the reasons behind, and significance of, increased levels of h in contaminated areas.

Genetic similarity of Puumala viruses found in Finland and western Siberia and of the mitochondrial DNA of their rodent hosts suggests a common evolutionary origin

A total of 678 small mammals representing eight species were trapped in western Siberia in 1999–2000 and assayed for the presence of hantaviruses. Eighteen animals, all Clethrionomys species, were antigen positive by enzyme-linked immunosorbent assay (ELISA). Small and medium genome segments were recovered by RT-PCR from six samples from Clethrionomys glareolus and three from Clethrionomys rufocanus. Sequence comparison and phylogenetic analysis revealed that these hantaviruses were Puumala virus and were similar to hantavirus strains from Finland. To confirm these data, partial nucleotide sequences of the rodent hosts’ cytochrome b genes were obtained, as well as several sequences from genes from rodents trapped at different localities of European Russia and western Siberia. The cytochrome b sequences of Siberian bank voles were similar to sequences of C. glareolus, trapped in Finland. These data suggest that the Puumala hantaviruses, as well as their rodent hosts, share a common evolutionary history. We propose that these rodents and viruses may be descendents of a population of bank voles that expanded northward from southern refugia during one of the interglacial periods.

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.

Differential responses of Clethrionomys species to forest disturbance in Europe and North America

In Holarctic forests, newly disturbed areas constantly appear as the result of clear-cutting and burning. Rodent communities in mature forests of Europe and North America are comparable, being dominated by a Clethrionomys species: Clethrionomys glareolus in Europe and Clethrionomys gapperi in America. In disturbed areas, however, they differ considerably, as C. glareolus persists on clearcuts in the Palearctic region, while in the Nearctic region, C. gapperi is replaced by Peromyscus species. Meta-analysis was applied to published data to summarize inter continenal differences. The aim of this paper is to explain why C. gapperi is not as successful as C. glareolus in colonizing disturbed areas, and to support one (or more) of the following hypotheses: (i) Peromyscus species are more suited to colonizing disturbed areas than other rodents; thus, the absence of Peromyscus species in Europe leaves the disturbed habitats free for C. glareolus; (ii) C. glareolus is more of a generalist and therefore better adapted for resettling such areas than C. gapperi; (iii) the long historical period of human management of forests has affected the niches of rodents, and thus their ability to colonize disturbed areas. The data analyzed indicate that the second hypothesis best explains the ultimate cause, while the third presents a probable proximate cause of the stated difference.

Life histories of Clethrionomys and Microtus (Microtinae)

AbstractAlthough there have been numerous life‐history reviews of mammals at high taxonomic levels (e.g. among families within orders), there are far fewer studies at lower taxonomic levels (e.g. among species within genera). Data on adult weights, litter size, gestation length, neonate weight, age and weight at weaning, growth rate to weaning, maximum life span, and length of the breeding season were compiled from the literature on five species of Clethrionomys and 33 species of Microtus. Variability in litter size and male body weights was not significantly different when compared between cyclic and non‐cyclic populations. Coefficients of variation were also calculated for the three species with the most data (C. gapperi, C. glareolus and M. pennsylvanicus). These values showed that the amount of intraspecific variation differed among traits as well as among species. Gestation length was the most invariable of all traits and variation in adult weights, neonate weight, gestation length, and litter size had similar values to those reported for Peromyscus maniculatus. Five and eight traits differed among Clethrionomys and Microtus species, respectively. Differences in litter size, adult weights and length of the breeding season were common to both genera. Male weight, gestation length and neonate weight as well as length of the breeding season were different between genera. Very few traits covaried within C. gapperi, C. glareolus or M. pennsylvanicus. Similarly, few traits covaried among all Clethrionomys populations. However, among all Microtus populations and Microtus species, 11 and 12 correlations were significant. Many of the patterns found in Microtus involved positive relationships between female weight and some other trait. These patterns have also been found by broader surveys at higher taxonomic levels. Large species of Microtus had larger offspring, a greater litter size and occurred in short‐season environments relative to small species of this genus.

Predicting Stable and Cyclic Populations of Clethrionomys

We develop a hypothesis predicting when populations consisting of territorial individuals will fill up the space available to them based on the idea of J. L. Brown of territorial establishment of birds in habitats of varying quality. The hypothesis has three main premises incorporating territoriality, heterogeneity of population space, and dispersal. These premises are claimed to be satisfied by Clethrionomys species. We analyse the biology of Clethrionomys in light of the hypothesis and show that differences in the degree of habitat quality may be important in determining whether populations will fill up population space or not. We present preliminary evidence suggesting that cyclic populations of Clethrionomys occur in areas where population space is less variable than it is where stable populations occur.

A Population Dynamics Model for Clethrionomys: Sexual Maturation, Spacing Behaviour and Dispersal

A mathematical model is developed and analyzed for studying the population dynamic consequences of the social system of Clethrionomys species. A patchy environment is assumed. The general version of the model incorporates density-dependent reproduction and survival; the specific version of the model for Clethrionomys assumes, in accordance with data, density independence in reproductive rate and survival of adults. Mature females are assumed to be territorial implying that maturation and dispersal of sexually immature females are regulated by the density of mature females.

Urine marking by male bank voles (Clethrionomys glareolus Schreber, 1780; Microtidae, Rodentia) in relation to their social rank

Available ecological data suggest that mature males of Clethrionomys species form stable hierarchical groups during the breeding season. The present laboratory work reports on the agonistic and urinary behaviour of paired, hierarchically naive, male bank voles (Clethrionomys glareolus) before, during, and after free interaction in large enclosures provided with individual burrows. In this situation, a generally stable dominance–subordination relationship is established. After a brief fighting episode, the subordinate is recognizable mainly by his avoidance behaviour out of his burrow. The subordinate's burrow itself becomes the focus of agonistic interactions. The staining of urine with unmetabolized vital dyes allowed differentiation of marking patterns. The correlation between these patterns and the hierarchical status of the animals is in accordance with the hypothesis that in bank voles, the urine of adult males contains chemical signals involved in maintaining their social organization. The spatial distribution of the urine marks of the dominant around the subordinate's nest suggests that they act as a territorial marking.

Comparative limb myology of four arvicolid rodent genera (mammalia, rodentia).

A comparative study of four genera of arvicolid rodents (Clethrionomys, Eothenomys, Alticola, and Synaptomys) presents the first complete description of limb myology for any member of this recently evolved, highly successful family. The study also identifies four forelimb and four hind-limb muscles that exhibit characters of value to systematic analyses within the group. In no instance was postcranial myology sufficient to distinguish among species of Clethrionomys or to distinguish Clethrionomys from Eothenomys. Moreover, in some instances Synaptomys, a genus traditionally presumed primitive within the family, possessed the apomorphic condition for a myological character when compared to the four genera of cricetine rodents that served for outgroup comparisons.

Gradients in density variations of small rodents: the importance of latitude and snow cover.

Microtine rodents are known to show extreme population variations (cycles) but non-cyclic populations have also been recognized during recent years. The cyclic populations have been widely thought to be regulated by intrinsic mechanisms. However, such predictions for cyclic populations are usually not applicable to non-cyclic ones and extrinsic factors may have to be included in any explanation.A hypothesis that the degree of fluctuations in small rodent numbers is related to the sustainable number of generalist predators was tested on mainly literature data by computing "indices of cyclicity" for local populations. These indices were related to latitude and snow cover (two measures) as these variables will affect the amount of alternative prey available for these generalists. Within Fennoscandia such indices for Clethrionomys glareolus and Microtus agrestis were clearly positively related to latitude and snow cover. The fraction of populations with summer declines in numbers, characterizing highly cyclic populations, increased in the same way. Cyclicity indices in Great Britain were similar to those in southern Fennoscandia, both areas being poor in snow, but were higher at the same latitudes in eastern Europe with more snow. Indices of density variations were generally low in North American Clethrionomys species and very variable in Microtus species.The gradients observed and differences between continents are interpreted as due to microtine-vegetation interactions in northern European areas poor in generalist predators but with important small mustelid predation, and to similar snowshoe hare-vegetation interactions in mainly Canada-Alaska, where small rodents may serve as alternative prey for numerically fluctuating hare predators, at least in the forests. Western European microtine populations, and probably many others, seem to be regulated by generalist predators.

Relationships of the Red-Backed Vole, Clethrionomys Rutilus (Pallas), in North America: Karyotypes of the Subspecies Dawsoni and Albiventer

Rausch, R. L., and V. R. Rausch (Department of Biological Sciences, University of Alaska, Fairbanks, Alaska 99701) 1975. Relationships of the red-backed vole, Clethrionomys rutilus (Pallas), in North America: karyotypes of the subspecies dawsoni and albiventer. Syst. Zool. 24:163-170.-Cytogenetic comparisons were made of northern red-backed voles of two subspecies, Clethrionomys rutilus dawsoni Merriam and C. r. albiventer Hall and Gilmore, as well as of intergrades of dawsoni X albiventer to the Fu generation. The diploid number was 56, and karyotypes were indistinguishable for all animals, with the exception of some individuals of C. r. albiventer (with 2n = 55) which were heterozygous for a chromosomal polymorphism evidently resulting from a Robertsonian rearrangement. All species of Clethrionomys for which karyotypes are known have 2n = 56, but two groups are distinguishable by the form of the Y-chromosome: in C. rufocanus (Sundevall), C. gapperi (Vigors), and C. occidentalis (Merriam), the Y is acrocentric, whereas in C. glareolus (Schreber) and C. rutilus, it is metacentric. Thus, the karyotypes of dawsoni and albiventer are indistinguishable from that of the Eurasian C. r. mikado (Thomas), and the different forms of the Y-chromosome separate C. rutilus and C. gapperi in North America. These findings further support the concept that C. rutilus is a holarctic species. [Red-backed vole; karyotypes.] Red-backed voles (genus Clethrionomys Tilesius, 1850) comprise a group of closely related species, some of which are so similar morphologically that their separation is difficult by means of external and cranial characters. The species occurring widely in arctic and subarctic North America has' been especially subject to changes in taxonomic status during the last century. The northern red-backed vole was first recognized as a holarctic species, Evotomys (= Clethrionomys) rutilus (Pallas, 1779), by Coues (1877). Without reference to Coues' work, Bailey (1897) expressed the same conclusion in his revision of the North American species of Evotomys, and recognized as well a second northern species, E. dawsoni Merriam, 1888. Miller (1898) considered that E. rutilus was restricted in distribution to the Palearctic and distin'-Present address: Department of Microbiology, Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Sask., Canada, S7N OWO. guished the species in northern North America as E. alascensis; he made no reference to E. dawsoni, although his specimens included some of those studied by Bailey. From the study of material from Alaska, Osgood (1904) determined that E. alascensis was a synonym of E. dawsoni. After Palmer (1928) established the priority of Clethrionomys Tilesius over Evotomys Coues, another arctic species, Clethrionomys albiventer Hall and Gilmore, 1932, was described from St. Lawrence Island, in the Bering Sea. A detailed study of C. dawsoni was made by Orr (1945), who recognized five subspecies, retaining albiventer as a distinct species. The concept that C. dawsoni and C. albiventer are conspecific with C. rutilus was accepted subsequently (Rausch, 1950; Manning, 1956; Bee and Hall, 1956). Bee also suggested (in Bee and Hall, 1956:117) that the nearctic C. gapperi (Vigors, 1830) is conspecific with C. rutilus. At the suggestion of the late Prof. Dr. Klaus Zimmermann, we undertook the

Xperimental studies of competitive interaction in a two-species system II. The behaviour of Mkrotus, peromyscus and Clethrionomys species

1. 1. The interactive behaviour of four species of microtine rodents was studied in the laboratory. The species were Clethrionomys gapperi and Peromyscus maniculatus from woodland habitat on the North American mainland; Microtus pennsylvanicus from grassland habitat on the same mainland and from a mixture of grassland and woodland habitat on Newfoundland; Clethrionomys glareolus from woodland habitat on mainland Britain, and from grassbracken habitat on a British island (Skomer). Two animals of the same group (controls) or of different groups (experimentals) were introduced simultaneously to an arena which contained grass in one half and maple saplings (woodland) in the other, and their behaviour was recorded for 30 min. 2. 2. Animals were aggressive to each other. Within each species the larger animal was almost always the dominant one. When animals of different species were tested together they interacted generally less frequently than did the controls, and the outcome in terms of dominance was not as predictable. 3. 3. When tested with Peromyscus or any of the Clethrionomys groups, both groups of Microtus from mainland and island occurred significantly more frequently in the grassland half of the arena than did the respective Microtus controls. Peromyscus occurred significantly more frequently in the woodland half when tested with mainland Microtus but not when tested with island Microtus. There were no significant differences in the distribution of the respective control and experimental animals of any of the Clethrionomys groups. But all the differences between controls and experimentais, whether statistically significant or not, were consistent with the hypothesis that two species have a mutually dispersive effect upon each other in relation to habitat occupied. 4. 4. In a separate experiment Peromyscus, born and reared in the laboratory in the presence of grass or maple or in the absence of both, were tested at a minimum age of 8 weeks either with Microtus or as controls. Although they did not differ from their controls, grass-exposed Peromyscus spent more time in the grass when tested with Microtus than did maple-exposed Peromyscus. This indicates that in young animals the early exposure to habitat features may be of over-riding importance. 5. 5. The relevance of the experimental results to events in the wild is discussed, and it is concluded that interactions at the individual level, involving aggressive encounters and possibly other factors, form the basis of the interactions which have been demonstrated at the population level in the wild.

The Eye Lens as an Age Indicator in Small Rodents

The age of specimens of two species of Clethrionomys has been found to be reflected by the weight of eye lenses and a method of age determination based upon this fact is discussed. The results obtained are in accordance with those obtained using the length of molar roots as the index but greater accuracy is obtained. The method may be of particular value for species in which molar root length cannot be ascertained. Acknowledgement We are greatly indebted to Prof. P. Brinck, Head of the Department of Ecology, Zoological Institute, Lund, for permission to use the rodent material and to Nordiskt Kollegium for terrester ekologi for a grant covering the cost of the field work. The study was carried out at Stensoffa Ecological Field Station.