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.     

Seasonal forcing on the dynamics ofClethrionomys rufocanus: Modeling geographic gradients in population dynamics

We interpret gradients in population dynamics of the gray-sided vole from the southwestern part of the island of Hokkaido to its northeastern part within the framework of a phenomenological model involving the relative length of summer and winter. In Hokkaido, as in other northern regions, both spring and fall is considered as short transition periods between the two main seasons — summer (the primary breeding season) and winter (the non-reproductive or secondary breeding season). We show that the geographic transition in dynamics may be understood as the combined consequence of different patterns of density-dependence during summer and winter, and geographically varying season lengths. Differences are shown to exist between summer and winter with respect to strength of density-dependence. Direct density-dependence, in particular, is stronger during winter than during summer. A model is presented to show how relative lengths of seasons can induce both stable and periodically fluctuating population dynamics. The results are compared and contrasted with what is otherwise known about the gradient in rodent dynamics in Fennoscandia.     

Mapping the regional transition to cyclicity inClethrionomys rufocanus: Spectral densities and functional data analysis

We study the regional transitions in dynamics of the gray-sided vole,Clethrionomys rufocanus, within Hokkaido, Japan. The data-set consists of 225 time series of varying length (most from 23 to 31 years long) collected between 1962 and 1992 by the Forestry Agency of the Japanese Government. To see clearly how the periodic behavior changes geographically, we estimate the spectral density functions of the growth rates of all populations using a log-spline method. We subsequently apply functional data analysis to the estimated densities. The functional data analysis is, in this context, analogous to a principal component analysis applied to curves. We plot the results of the analysis on the map of Hokkaido, to reveal a clear transition from relatively stable populations in the southwest and west to populations undergoing 3–4 year cycles in the northeast and east. The degree of seasonality in the vegetation and the rodent demography appear to be strongest in the cyclic area. We briefly speculate that the destabilization of the rodent dynamics is linked to increased seasonalforcing on the trophic interactions in which the gray-sided voles are involved.     

The population dynamics of the voleClethrionomys rufocanus in Hokkaido, Japan

Population dynamics of the gray sided-vole,Clethrionomys rufocanus, in Hokkaido, Japan were described on the basis of 225 time series (being from 12 to 31 years long); 194 of the time series have a length of 23 years or longer. The time series were classified into 11 groups according to geographic proximity and topographic characteristics of the island of Hokkaido. Mean abundance varied among populations from 1.07 to 21.07 individuals per 150 trap-nights. The index of variability for population fluctuation (s-index) ranged from 0.204 to 0.629. Another index for population variability (amplitude on log-10 scale) ranged from 0.811 to 2.743. Mean abundance and variability of populations were higher in the more northern and eastern regions of the island. Most populations, except for the southernmost populations, exhibited significant direct density-dependence in population growth. Detection rate for delayed density-dependence varied among groups from 0% to 22.6%. Both direct and delayed density-dependence tended to be stronger in the more northern and eastern populations. The proportion of cyclic populations was higher in the northern-eastern areas than that in the southern-western areas. There was a clear gradient from the asynchronous populations in southwest, to the highly synchronized populations in the northeast.     

Sexual differences in natal dispersal and philopatry of the grey-sided vole

The natal dispersal distance of the grey-sided vole,Clethrionomys rufocanus (Sundevall), was measured in a large outdoor enclosure (2.1 ha) in Hokkaido, Japan. Voles in about half of the enclosure (1 ha) were fed. Distance from the natal site to the site of reproduction was significantly greater in males (64.9 m) than in females (35.3 m). In males, 24.8% settled within one home range length of their natal site and 49.6% settled further than two range lengths from their natal site. In femles, the respective percentages were reversed: 51.2% and 22.0%. The timing of large movements (≥50 m) was related to body mass in both sexes. The population density was always higher on the fed grid than on the control grid, which resulted in the frequency of large movements being greater on the fed grid that on the control grid. Thus, the percentage of voles performing a large movement was not different between the grids in both sexes.     

Social organization of the voleClethrionomys rufocanus and its demographic and genetic consequences: A review

Recent findings on the relationship between social interaction and demographic process in the gray-sided voleClethrionomys rufocanus are reviewed with reference to the findings in other microtine rodents. Social behavior was particularly focused on spacing and dispersal, and their effects on population dynamics are discussed. Female territoriality can limit a population abundance as a density-dependent factor, although its regulatory effect is controversial. Female philopatry and male-biased dispersal should bring about the clumped distribution of female relatives and genetically random distribution of males during the breeding season. The sexual difference in dispersal patterns can contribute to the mating behavior of the vole; promiscuous mating and low frequency of incestuous mating. However, effects of social structure, including kinship, on reproduction and survival of individuals still remains to be clarified. Molecular markers may help to solve these issues and provide new field of population ecology in microtine rodents.     

Age distribution, sex ratio and mortality of the red foxVulpes vulpes in Tochigi, central Japan: an estimation using a museum collection

One hundred and thirty carcasses of the red fox were collected in Tochigi Prefecture, by the Tochigi Prefectural Museum, from 1981 to 1991. The young/adult ratio of the sample was 1.60, which suggests that the hunting pressure has been relatively low in this area. Six percent of the animals were 5 years or older which compares to those taken in Hokkaido, but is higher than those in Europe and North America. The sex ratio for all specimens had a tendency towards male bias (0.587), but this bias was higher for the adult (0.605) than for the young (0.576). Among young (0 year-old) foxes, more individuals were killed on roads than by trapping or shooting (P<0.02, chisquare test). This mortality pattern was caused by high mortality of young males (P<0.02). The proportions of adults killed by the three mortality factors were similar, though only one of the 14 foxes older than 4 years old was shot, probably due to age-linked activity patterns. Most road-kills of young foxes occurred in May when juveniles began exploiting and in November when sub-adults began dispersal. The ratios of road-kills for the whole sample and for adults alone were 42% and 34%, respectively. These high rates of road-kills suggest that the mortality pattern in Tochigi has been affected by factors characteristic of urban environments.     

Inter- and intra-population variations in diapause attribute of the two-spotted spider mite,Tetranychus urticae Koch, in Japan

Summary Populations of the two-spotted spider mite,Tetranychus urticae Koch collected from various localities and from various host plants in Japan showed wide variations in diapause attribute. Diapause percentages at 18°C/9L15D varied from nearly 100% in the north to 0% in the south-west. At intermediate latitudes the mites showed wide inter-population variations. Populations on herbaceous hosts in vinyl- or glass-houses gave significantly lower incidence of diapause than those on roses and deciduous fruit trees. Presence of winter hosts and better host quality under protected environments seemed to favour non-diapausing mites. The temperature threshold for diapause expression also varied widely among local populations. Northern populations consistently had higher and less variable thresholds than populations at intermediate latitudes with thresholds between 15 and 18°C. Inbred lines derived from a population in Kyoto exhibited a wide variation in diapause percentage at 18°C. These results show that diapause inT. urticae is a quantitative threshold trait and that populations in central Japan consist of a variety of genotypes with different diapause traits. This might provide a genetic source for adaptation to local and temporal variations in environmental conditions.     

Kin-related social organization in a winter population of the voleClethrionomys rufocanus

Kinship amongClethrionomys rufocanus was investigated during the winter of 1992/93 in a 3-ha enclosure using both molecular and catch-mark-release techniques. Forty-six adult voles (22 males and 24 females) having high heterozygosities, which were collected from several natural populations, were released into the enclosure on 29 September 1992. Most fall-born individuals of both sexes stayed in their natal site during the non-breeding period (December–March), although reproductively active females dispersed during the fall breeding season (October–November). These philopatric individuals aggregated and formed an maternal family in the winter. Several females which failed to reproduce were solitary during this season. Some individuals which were derived from several families also aggregated into a mixed lineage group. Survival rate of fall-born voles from earlier litters was higher than that from later ones. Maternal families broke up soon after the onset of spring reproduction. Most females established a territory near the wintering site and made a kincluster, in which close relatives neighbored each other. Maternal families in winter bring about female kin-clusters in spring, which may influence reproductive output in the breeding season.     

Regulation of reproduction rate in a cyclic population of the red-backed vole,Clethrionomys rufocanus bedfordiae

Summary Changes of the components of reproduction were analyzed quantitatively in a two-year cyclic population (which has two peaks in alternate years during a five-year census) of the red-backed vole,Clethrionomys rufocanus bedfordiae, with reference to its regulatory mechanism: (1) Variation in sex ratios was not associated with population phase or density, although a higher percentage of females in mature individuals was observed in the increase phase. (2) Females attained to sexual maturity at younger age and at lighter body weight than did males. All the youngest mature individuals were found in the low and the increase phases. Age and size at maturity became older and larger as the population went toward the peak phase. (3) Maturation rate was strongly associated with population phase and density; this component is an important and good parameter to predict population trend. Maturation rates were in the order, the low phase>the increase phase>the peak phase>the decline phase; the differences in the rates among these phases were significant. Maturation rate was somewhat depressed when the population density exceeded about 40 individuals/ha. Changes in age at maturity and in maturation rate are interpreted as derivative phenomena related to the population density and the capacity of the number of mature voles per unit area. (4) The maximum number of mature individuals were 26 males/ha and 29 females/ha; there was almost no increase of the number of mature voles at higher population densities over about 40 individuals/ha. The number of exclusive home ranges per hectare calculated from the observed range lengths did not differ much from the maximum number of mature voles of either sex. (5) Length of breeding period was shorter in the high-density years than in the low-density years; the breeding started earlier and ended earlier in the former than that in the latter. In the increase phase a few voles reproduced in winter. (6) The percentage of pregnant females was significantly lower in the peak phase than those in the other phases.     

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

Conclusion 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 m by the gross along with the rise from 20 to 100 in the density level per acre, and hence that an appreciable discrepancy, due to underestimation, may be produced in estimates of the exposed as compared to the whole population at an outbreaking density as high as 100 on a plan with trap-spacing 10 m. In consideration of this together with my preceding results, the strict terms that we may enough approximate the whole one by estimating the exposed seem likely to be that the ratio of range radius to trap spacing, supposing a range is circular, should be near 2 or more at either ordinary or outbreaking densities, to say in the concrete, that the trap spacing as close as 5 m or so in grid is desirable with this vole, perhaps with most other voles.     

On the mathematical basis of the variance-mean power relationship

The mathematical basis of a widely-known variance-mean power relationship of ecological populations was examined. It is shown that the log variance (S ²)—log mean, (m) plot is virtually delimited by two lines logS ²=logn+2 logm and logS ²=logm, thus increasing the chance that a linear regression line can be successfully fitted, without a profoundly behavioural background. This makes difficult the task of interpreting a successful fit of the power law regression and its parameterb in a biologically meaningful manner. In comparison with the power law regression, Iwao'sm ^*-m regression is structurally less constrained, i.e. has a wider spatial region in which data points can scatter. This suggests that a comparison between the two methods in terms of how good a fit is achieved for a particular data set is largely meaningless, since the power law regression may inherently produce a better fit due to its constrained spatial entity. Furthermore, it could be argued that a successful fit in Iwao's method, when found, is less taxed with mathematical arterfacts and perhaps more clearly linked to some biological mechanisms underlying spatial dispersion of populations.     

The effects and limits of territoriality on population regulation in grey red-backed voles,Clethrionomys rufocanus bedfordiae

Summary The effects of breeding territoriality on the stability of grey red-backed vole (Clethrionomys rufocanus bedfordiae) populations were investigated on a control grid and a grid on which the voles were fed, in an outdoor enclosure in Hokkaido, Japan. Vole populations were monitored by live trapping from 1984 to 1986: (1) Population density was 2–7 times greater on the experimental grid to which food was added than on the control grid. Reproductive output was more closely associated with the difference in density between grids than survival or dispersal (immigration and emigration) rates. (2) The number of adult females and pregnancy rate of the experimental population were significantly greater than those of the control one. The difference in the number of adult females between the populations was greater than that in pregnancy rate. (3) The proportion of successful litters and the number of weanlings per litter were not significantly different between the control and experimental population. (4) Adult females held territories on both the control and experimental grid; they were spaced out more than would be expected from random occupation. The territories overlapped more on the experimental grid than on the control grid. (5) Mean territory size of adult females on the experimental grid was about half of that on the control grid. The territory size was correlated negatively with population density. (6) The proportion of trap sites that were used by adult females was significantly greater on the experimental grid than on the control grid. This suggests that adult females on the experimental grid used the area more extensively. This factor, in association with territory size and overlapping of territory, was also important in causing the difference in the number of adult females between the grids. (7) These results call into question the hypothesis that territoriality stabilizes the density in populations ofClethrionomys.     

A ten-year study of population dynamics of citrus pests in the pesticide-reduced orchard

Summary To determine the effectiveness of a pest management system that uses pesticides at a low level, we censused populations of seven insect pests and three plant diseases from 1980 to 1989 in a citrus orchard which was managed with a pesticide-reduced and pesticide-free protocols, in Wakayama Prefecture, Japan. In the orchard, we controlled the pests solely by spraying petroleum oil once a year from 1980 to 1985, by not spraying insecticide in 1986, and spraying only germicide in 1987. The arrowhead scale population remained much lower level at which citrus trees begin to wither when petroleum oil was sprayed, whereas it rapidly increased and began to wither trees during the years without spraying petroleum oil. The Indian wax scale population rapidly increased only during a 2-year period and then declined. Although the infection level of the sooty mold was unusually high on the trees where the density of the scale was high, this pathogen did little damage to citrus trees. The population of the red wax scale gradually increased throughout the census period but did not reach the level at which citrus trees begin to be damaged. Other pests also caused negligible damages to citrus trees. The results indicated that the pesticide-reduced pest management system which was proposed by Inoue and Ohgushi (1976, 1977) is valid for the prevention of the outbreak of the arrowhead scale, and that is has the sufficient control efficiency for the other pests in citrus orchards. Contribution to the ecological studies of scale insect 3.     

Preference and performance linkage in aPhyllocolpa sawfly on the willow,Salix miyabeana, on Hokkaido

A leaf-folding sawfly in the genusPhyllocolpa (Hymenoptera: Tenthredinidae) attackingSalix miyabeana (Salicaceae) was studied near Sapporo, Hokkaido, along the Ishikari River in 1993. Host plant individuals were young trees 4–7 years old which were growing rapidly, producing some long shoots with large leaves. On a gradient of shoot length classes from 0–5 cm long to over 80 cm long, shoots were much more abundant in the shorter shoot length classes. However, attacks by ovipositing females increased as shoot length increase from 0 attacks on the shortest shoots to 5.17 attacks per shoot on the longest shoots. The frequency of attack per leaf increased from 0 to 0.13 over the same range of shoot lengths. This pattern of attack resulted in a high frequency of larval establishment in feeding sites, between 0.96 and 1.00, in all attacked shoot length categories. However, probability of survival to a late instar larva increased with shoot length and corresponded to the attack pattern, indicating a preference-performance linkage between female ovipositional decisions and larval survival. The patterns found for thisPhyllocolpa species are similar for galling sawflies in North America and Europe, especially in the genusEuura, members of which make stem, bud and leaf midrib galls. Extending the pattern to aPhyllocolpa species broadens identification of pattern and ultimately the generality of the emerging theory on populations of galling sawflies.     

Effects of gall volume on survival and fecundity of gall-making aphidsAdelges japonicus (Homoptera: Adelgidae)

Summary The number of larvae reaching maturity within the gall ofAdelges japonicus was positively related to gall volume, and the relationship between the number of mature larvae and gall volume did not change with different densities of colonized larvae. The population changes in the bud galls ofA. japonicus were surveyed by collecting the galls, which did not suffer predation or parasitism within the galls, from young artificial plantations ofPicea jezoensis over two years. In the year when the density of colonized larvae was high, they suffered a 42% mortality within the galls, whereas mortality was nearly zero in the low density year. The numbers of larvae per gall were positively correlated with gall volume. The regression lines of the number of colonized larvae on gall volume did not differ significantly in the regression coefficients between the two years, whereas the intercept was significantly higher in the year when the density of colonized larvae was higher. However, different within-gall mortality nullified this difference, and the regression lines of the number of mature larvae on gall volume had no significant difference both in the regression coefficients and the intercepts. This suggests that the number of mature larvae per gall was limited by available resources within the gall which were positively related to gall volume. In 25% of the galls in which mature larvae inhabited, the space within the galls were completely filled by the larvae, indicating that space was one of the limiting resources. Gall volume also affected the number of adults that emerged from the gall and the potential number of their progeny.     

Egg cluster size variation in relation to the larval food abundance inLuehdorfia puziloi (Lepidoptera: Papilionidae)

Summary Mean egg cluster size ofLuehdorfia puziloi yessoensis varied among habitats. The mean egg cluster size tended to be large when abundance of the larval food leaves expressed as the fresh weight of leaves per unit area at a given habitat was high. Since this variation was observed among closely located study plots (butterflies can easily move between study plots), the egg cluster size variation among habitats is likely to be a result of flexible response by females to varying food abundance for larvae.     

Temporal/spatial structure and the dynamical property of laboratory host-parasitoid systems

The effects of spatial structure in terms of local capacity, or the maximum number of larvae surviving competition at resource patches, and temporal structure in terms of the period vulnerable to parasitoid attack in host populations on the persistence of host-parasitoid systems were quantitatively evaluated by laboratory experiments and well-parameterized model analyses. One of two bruchid beetles,Callosobruchus maculatus andC. phaseoli, were used as a host with Heterospilus prosopidis used as the parasitoid.C. maculatus, in which few larvae survive competition to become adults in each bean, andC. phaseoli, in which many larvae become adults in each bean, along with two kinds of beans, the mung and the azuki, were combined to construct four (2×2) resource-herbivorous host-parasitoid systems that differed in local capacity and vulnerable period. The mung-C. maculatus system with the parasitoid was the most persistent, i.e., took the longest time for extinction of either the host or parasitoid to occur. Since this resource-herbivorous host combination exhibited the lowest local capacity and the shortest vulnerable period, these two conditions possibly promoted the persistence of the system. A model incorporating the host population structure supported the observed persistence. Furthermore, the possible contribution of the timing of density-dependent competition of the host on the host-parasitoid persistence is predicted.     

Spatial variation in female fertility related to interactions with flower consumers and pathogens in a forest metapopulation ofPrimula sieboldii

Antagonistic biological interactions with flower consumers and pathogens may influence reproductive success of flowering plants, affecting population dynamics and natural selection for floral traits. However, ecological and evolutionary consequences of the interactions may depend on both spatial and temporal patterns of the interactions. In a forest metapopulation ofPrimula sieboldii E. Morren, an endangered clonal plant species, we measured between-subpopulation patterns of seed sets and interactions with an influential flower consumer, a rove beetle,Eusphalerum bosatsu Watanabe, and a specific smut fungal pathogen,Urocystis tranzschelina (Lavrov) Zundel (Ustilaginales), for three years. Mean female fertility (seed set per flower) for individual subpopulations fluctuated moderately among years but was highly variable within each year among the five subpopulations studied. In two subpopulations, the impact ofEusphalerum beetle, was sufficiently large to result in almost complete failure in seed production over eight years including the three study and five previous preliminary observation years. In the two other subpopulations, seed set failure was caused by infection by the smut fungus. Infected capsules which constitute 10–30% of the capsules produced in the subpopulations were filled with ustilospores instead of seeds. In the subpopulation that escaped flower damage byEusphalerum beetles and smut fungal infection, seed sets of both pin and thrum flowers were much higher than in the other subpopulations. The spatial restriction of individual antagonistic agents to a part of subpopulations suggest that dispersal of the agents, as well as the mode of spatial subdivision of the plant population would be important for determining the overall effects of antagonistic interactions on plant performances at the metapopulation level.     

Population dynamics of a phytophagous lady-beetle,Epilachna vigintioctopunctata (Fabricius), living in spatio-temporally heterogeneous habitats. III. Effects of habitat structure on population dynamics

Temporal changes in the population size of a phytophagous lady-beetle were analyzed to identify mechanisms affecting lady-beetle population dynamics at different spatial scales. The study area (15 ha) included 18 habitat patches. The major host plants were potato for first generation larvae and eggplant for second generation larvae. The habitat patches were classified into three groups according to the major host plants in each patch: P-E patches (both host plants available), P patches (potato only), and E patches (eggplant only). The winter disappearance of adults in the whole study area, and larval mortality in E patches were apparently the most important factors disturbing the overall population density. Density-dependent movement of females appeared to have the greatest stabilizing effect on the yearly fluctuation of population density. Rate of increase of female adults from the first to the second generation,R, was generally higher on eggplants in E patches than in P-E patches because the adult density of the first generation was much higher in P-E patches. The yearly fluctuation of adult density in each generation tended to be less in patches with all habitat components necessary for the full life cycle (P-E patches). However, such patches were not favorable for first generation females, as indicated by the lower rate of increase from the first to the second generation. The density and stability of lady-beetle populations is discussed in relation to habitat structure.