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.     

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.     

The demography ofClethrionomys rufocanus: From mathematical and statistical models to further field studies

Until recently, most studies on microtines have focused on patterns in population dynamics or demography without providing a quantitative assessment of the robustness of the inferred patterns as well as a link between demography and population dynamics. Developments in statistical time-series analysis on the one hand and in capture-recapture statistical modelling on the other hand, now allow for improved analyses. We review some of the recent developments in the capture-recapture statistical methodology — restricting ourselves to methods most relevant to the demography of small mammals. A 5-years study of the gray-sided voleClethrionomys rufocanus in Hokkaido, Japan was used as an example to explore some models. We then provided a framework for further demographic analysis of microtine populations, includingC. rufocanus. Investigating the relative importance of the different demographic parameters (e.g. survival, maturation, dispersal) will require studies done on larger scale than is commonly done today, with more effort devoted to the low density phase. Special emphasis is given to study-design, and to experimental designs tailored to the study of specific demographic mechanisms.     

Genetic structure of Japanese populations of an ambrosia beetle,Xylosandrus germanus (Curculionidae: Scolytinae)

We examined the genetic structures of 13 Japanese populations of an ambrosia beetle, Xylosandrus germanus (Curculionidae: Scolytinae), to understand the effects of geographical barriers on the colonization dynamics of this species. The genetic structure was studied using portions of the mitochondrial cytochrome oxidase I (COI) gene. A phylogenetic analysis revealed three distinct lineages (clades A, B and C) within X. germanus. Clade A contained 21 haplotypes from all 13 populations; whereas clade B contained eight haplotypes from Hokkaido (Sapporo and Furano), Iwate and Nagano populations; and clade C contained only a single a haplotype from the Hokkaido (Furano) population. In the analysis of molecular variance (amova ), the greatest amount of genetic variation was detected between populations in Hokkaido and those in Honshu and other southern islands. Between these two groups of populations, all the values of the coefficient of gene differentiation were significantly larger than zero, except for the Hokkaido (Sapporo) versus Nagano comparison. Our results confirm that for X. germanus, gene flow has been interrupted between Hokkaido and Honshu since the last glacial maximum.     

Population genetic structure of Sorex unguiculatus and Sorex caecutiens (Soricidae, Mammalia) in Hokkaido, based on microsatellite DNA polymorphism

We investigated the genetic structure of Sorex unguiculatus and Sorex caecutiens populations in Hokkaido, Japan, using hypervariable microsatellite DNA markers. We used five microsatellite loci to type 475 S. unguiculatus individuals from 20 localities on the Hokkaido mainland and four localities from each of four offshore islands (and 11 shrews from one locality in southern Sakhalin for a particular analysis). We used six microsatellite loci to type 240 S. caecutiens individuals from 13 localities on the Hokkaido mainland. Genetic variation was high in mainland populations of both species and low in the island populations of S. unguiculatus. Allelic richness and island size were positively correlated for S. unguiculatus, suggesting that genetic drift occurred on those islands due to small population size. In addition, four insular populations of S. unguiculatus were genetically differentiated from the mainland populations, although clear phylogeographic clustering was not confirmed among populations on the Hokkaido mainland for either S. unguiculatus or S. caecutiens. Heterozygosity excess was observed in more than half of the populations including the mainland populations of the two species, suggesting recent bottleneck events in these populations. Population dynamics of the shrews might be explained by a metapopulation scheme. According to autocorrelation analysis, the extent of non-random spatial genetic structure was approximately 100 km. Isolation by distance was observed in S. unguiculatus, but not in S. caecutiens although there is a positive trend. The lack of correlation for S. caecutiens might have been due to small sample size. Thus, no obvious differences in population genetic structure were found between the two species on the Hokkaido mainland in the present study, while previous investigations using mitochondrial DNA sequences inferred that these two species might have rather different biogeographic histories.     

Mechanisms of density dependence in fluctuating vole populations: deducing annual density dependence from seasonal processes

Based on recent advances in time-series analyses of ecological dynamics using statistical and mathematical models, we summarise our recent results on the seasonal processes in the annual population dynamics of the grey-sided vole Clethrionomys rufocanus (Sundevall, 1846) in Hokkaido, Japan, and report additional analyses on annual and seasonal density dependence. Annual direct density dependence was strong in almost all populations. In contrast, delayed density dependence was generally weak, although clear delayed density dependence was detected in some of the studied populations. Although seasonal density dependence was observed both in winter and summer, direct density dependence was much more profound during winter; thus, winter density dependence contributed most to the overall annual direct density dependence. We found no correlation between the seasonal components of annual direct density dependence; however, the corresponding seasonal components for annual delayed density dependence were positively correlated. We conclude that winter conditions influence the strength of annual direct density dependence most profoundly. Moreover, we conclude that direct density dependence during summer and winter may be generated by different mechanisms, whereas delayed density dependence seems to be generated by a common mechanism. Candidate mechanisms are discussed in relation to general knowledge of northern rodent populations and to specific insights provided by earlier studies of grey-sided voles in Hokkaido.     

The role of vole populations in prevalence of the parasite (Echinococcus multilocularis) in foxes

Effects of population fluctuation of the gray-sided vole(Clethrionomys rufocanus) on the prevalence (infection rates) of the parasiteEchinococcus multilocularis in red fox(Vulpes vulpes) populations was investigated from 1985 to 1992 in eastern Hokkaido (Abashiri, Nemuro, and Kushiro area), Japan. This parasite needs two hosts to complete its life cycle; the gray-sided vole as its intermediate host and the red fox as its final host. We found that: (1) Infection rates in foxes depended on the current-year abundance of voles in all three study areas, particularly in Abashiri. (2) In addition to this direct density-dependence, delayed density-dependence between the infection rate and the prior-year abundance of voles was detected in Nemuro and in Kushiro. (3) The regional differences in density-dependence pattern were related to regional differences in the winter food habits of red foxes: in Abashiri the proportion of voles in the fox’s diet greatly decreases in winter, while the proportion remains high in winter in Nemuro and in Kushiro, probably because of shallower snowpack. These results suggest that infection rates in foxes in Abashiri were less influenced by the prior-year prevalence, since the infection cycle might be interrupted in winter, when voles became less important in fox’s diet. In contrast, the state of the prevalence may carry over from year to year in Nemuro and in Kushiro, because red foxes continue to eat a considerable amount of voles throughout year. The regionally contrasted results for the relationship between infection rate in foxes and vole abundance were parallel to the regional difference in fluctuation pattern of vole populations, which are highly variable in Abashiri area, but less variable in Kushiro-Nemuro area. Drastic change in vole populations appears to affect the host-parasite system.     

Effects of acorn masting on population dynamics of three forest-dwelling rodent species in Hokkaido,Japan

The effects of the abundance of acorns of the oak, Quercus crispula, on the population dynamics of three rodent species (Apodemus speciosus, A. argenteus, and Clethrionomys rufocanus) were analyzed using time series data (1992–2006). The data were obtained in a forest in northern Hokkaido, Japan, by live trapping rodents and directly counting acorns on the ground. Apodemus speciosus generally increased in abundance following acorn masting. However, the clear effect of acorn abundance was not detected for the other two rodent species. Acorns of Q. crispula contain tannins, which potentially have detrimental effects on herbivores. Apodemus speciosus may reduce the damage caused by acorn tannins with tannin-binding salivary proteins and tannase-producing bacteria, whereas such physiological tolerance to tannins is not known in the other two rodent species. The differences in the effects of acorns between the three species may be due to differences in their physiological tolerance to tannins.     

Genetic variation and differentiation of the two river sculpins,Cottus nozawae andC. amblystomopsis,deduced from allozyme and restriction enzyme-digested mtDNA fragment length polymorphism analyses

Genetic differentiation of the two sibling species,Cottus nozawae andC. amblystomopsis, from the northern part of Japan (Hokkaido Island and the Tohoku District) was investigated using allozyme variations and restriction fragment length polymorphisms of mitochondrial DNA. Although the two species are morphologically very similar, previously being thought to be a single species, they have different life-cycles;C. nozawae has a fluvial life-cycle with a small number of large-sized eggs, whereasC. amblystomopsis is an amphidromous species with a large number of small-sized eggs. Four populations ofC. amblystomopsis from Hokkaido Island and 24 populations ofC. nozawae (22 from Hokkaido Island and 2 from the Tohoku District) were sampled and examined Intrapopulational differentiation in the two species was measured by examining several indexes, including proportion of polymorphic loci (P), mean heterozygosity (H) and nucleotide diversity (π). All measurements were higher in theC. amblystomopsis populations, suggesting that intrapopulational variation inC. nozawae was less than inC. amblystomopsis and reflecting the difference in effective population sizes between them. Cluster analyses were performed using the UPGMA method, based on the data matrices of genetic distance (D) and the net nucleotide difference (δ) between populations. TheC. nozawae andC. amblystomopsis populations from Hokkaido Island composed a large cluster (Hokkaido group), while theC. nozawae populations from the Tohoku District composed a different cluster (Tohoku group). Bootstrap probabilities deduced from 1000 bootstrap replications for presence or absence of restriction sites showed that the mtDNA haplotypes detected within the Tohoku Group occurred in 99.9% of the bootstrap replicates outside the mtDNA haplotypes of the Hokkaido group, while those within the Hokkaido group occurred in 3.5–64.9% of bootstrap replicates. Consequently, the Hokkaido populations of the two species (Hokkaido group) were genetically close to each other, whileC. nozawae from the Tohoku District (Tohoku group) were distant from the Hokkaido group. These results suggest that the ancestral populations of the two species on Hokkaido Island shared the same gene pool, even after becoming geographically isolated from the ancestral population ofC. nozawae in the Tohoku District by the formation of the Tsugaru Straits.     

The historical differentiation process inHemerocallis middendorfii (Liliaceae) of Japan based on restriction site variations of chlorplast DNA

Chloroplast DNA restriction site variation inHemerocallis middendorfii Trautv. & Meyer was investigated to deduce the historical differentiation process that had taken place in populations among three districts Hokkaido, Honshu and the Island of Tobishima in Japan as distinct from the morphological data. The populations selected were eight in total, consisting of two populations from Honshu, one each from the Islands of Sado and Tobishima and four from Hokkaido. Twelve endonuclease restriction enzymes were used. Six restriction site mutations were found among the populations investigated. A single, most parsimonious phylogenetic tree is generated, and revealed that the four populations of Hokkaido and two populations of the Islands of Sado and Tobishima are monophyly, respectively.     

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.     

Second-order feedback and climatic effects determine the dynamics of a small rodent population in a temperate forest of South America

 The multiannual cyclic fluctuations exhibited by arvicoline rodents in the Northern Hemisphere have attracted the attention of population ecologists. However, despite the abundant information on small rodent dynamics in South America, there are no studies reporting cyclic population dynamics. Here, we report evidence of cyclic population dynamics in a South American small rodent, the longhaired field mouse (Abrothrix longipilis) from southern temperate forests in Chile. The time-series analyses showed that longhaired field mice dynamics are better represented by a second-order autoregressive model characterized by 3-year cyclic dynamics. The 3-year cycles are clearly shown in the autocorrelation factor (ACF) pattern and in the dominant frequency of the spectral analysis. In addition, we determined nonlinear effects of the Antarctic Oscillation Index (AAOI). The results shown here pointed out that we need the integration of studies about cyclic small rodent populations from the different continents and beyond the Northern Hemisphere to resolve the enigma underlying the cyclic population dynamics exhibited by many small rodent species. Received: September 19, 2002 / Accepted: February 4, 2003     

Mapping of QTLs conferring extremely early heading in rice (Oryza sativa L.)

Two genes related to extremely early heading were identified in populations derived from crosses between Hoshinoyume, a variety adapted to the northernmost limit of rice cultivation (Hokkaido), and Nipponbare, a variety adapted to the temperate region of Japan. The segregations for heading date clearly revealed that a two-gene model determined the extremely early heading in the F₂ and BC₁F₁ populations under natural field conditions in Hokkaido. Using molecular markers corresponding to ten known quantitative trait loci (QTLs) for heading date, we carried out QTL analysis in the BC₁F₁ population and detected two QTLs, qDTH-7-1 and qDTH-7-2, both on chromosome 7, and observed epistatic interaction between them. We conclude that the recessive alleles of these two genes contribute to extremely early heading for the adaptation to Hokkaido environment and to stable rice production in Hokkaido. The relationships between the two QTLs identified in this study and known QTLs are discussed.     

Geographical variation in the cranial and external characters of the little tube-nosed bat,Murina silvatica in the Japanese archipelago

The distribution ofMurina silvatica (Yoshiyuki, 1983) in the Japanese archipelago extends over about 2000 km from north to south. Specimens were obtained from populations in Hokkaido and Yakushima, which are at the northern and southern ends of the range, and from two intermediate locations in Honshu. Measurements of cranial and external morphology were examined for evidence of geographical variation. The results of both multivariate analysis of variance and cluster analysis showed that there was no distinct cline in skull morphology among the Hokkaido, Tohoku and Chubu populations. However, the results of multivariate analysis of variance showed that all measures were significantly greater for the Yakushima population than for the others. Similarly, in a dendrogram of cluster analysis, the Yakushima population formed a cluster that was distinct from the other populations. However, as the difference between the Yakushima population and the other populations was less than the variation found within the Hokkaido, Tohoku and Chubu populations, morphological divergence of the Yakushima population was attributable to intraspecific variation. The island of Yakushima is the most isolated of the four locations and the morphological divergence of this population may be associated with its relative geographic isolation.     

Population dynamics of two rodent species in agro-ecosystems of central Argentina: intra-specific competition,land-use,and climate effects

Understanding the role of feedback structure (endogenous processes) and exogenous (climatic and environmental) factors in shaping the dynamics of natural populations is a central challenge within the field of population ecology. We attempted to explain the numerical fluctuations of two sympatric rodent species in agro-ecosystems of central Argentina using Royama’s theoretical framework for analyzing the dynamics of populations influenced by exogenous climatic forces. We found that both rodent species show a first-order negative feedback structure, suggesting that these populations are regulated by intra-specific competition (limited by food, space, or enemy-free space). In Akodon azarae endogenous structure seems to be very strongly influenced by human land-use represented by annual minimum normalized difference vegetation index (NDVI), with spring and summer rainfall having little influence upon carrying capacity. Calomys venustus’ population dynamics, on the other hand, seem to be more affected by local climate, also with spring and summer rainfall influencing the carrying capacity of the environment, but combined with spring mean temperature. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Different population responses of three sympatric rodent species to acorn masting—the role of tannin tolerance

Rodent population dynamics are predicted to respond positively to the masting of acorns, but diverging results have been published. This study tested the hypothesis that population responses to acorn masting vary depending on differences in the tolerance to tannins of different rodent species. The effects of acorn abundance on the rodent population densities were analyzed using a dataset obtained in Hokkaido, Japan. Specifically, population fluctuations of three rodent species (Apodemus speciosus, A. argenteus, and Myodes rufocanus) and the abundance of Quercus crispula acorns have been monitored since 1992. Acorn production in previous years had a positive effect on the annual population growth rates of A. speciosus; however, this trend was not clear in the other two species. Tannin tolerance, assessed by body weight changes in an acorn feeding experiment, exhibited clear differences among the rodent species; namely, the body weight of A. speciosus increased, whereas that of the other two species decreased. The observed responses to acorn masting of populations of the three sympatric rodent species reflected tannin tolerance. It suggests that only populations of species with high tannin tolerance positively respond to acorn masting. Previous studies tend to overlook species-specific abilities of coping with tannins in acorns. Our results emphasize the necessity of evaluating the tannin tolerance of rodents and the tannin content of acorns to understand how rodent population dynamics and acorn production are related.     

Genetically diversified populations in the loach Misgurnus anguillicaudatus inferred from newly developed microsatellite markers

The loach Misgurnus anguillicaudatus is a freshwater fish which include natural polyploids and clones besides most bisexually reproducing diploids. Recent genetic studies using allozymes differentiated the populations in northern region of Hokkaido from other populations in Japan. Here, we developed 23 new sets of polymerase chain reaction primers to detect polymorphic microsatellites loci and tested them in 20 individuals from Memanbetsu town (northern Hokkaido) and Kita village (southern Hokkaido). These markers can be potentially diagnostic for identification of two populations.     

Variation of sterility and fertility in Utricularia australis f. australis in Hokkaido, northern Japan

Seed-production ability was studied in Utricularia australis R. Br. f. australis Komiya and Shibata through field observation, pollination experiment, pollen culture, and isozyme analysis for populations in various regions of Hokkaido, northern Japan. Utricularia australis f. australis has previously been postulated to be sterile in Japan, however, in the present study, fertile populations were found in eastern Hokkaido. Bisexual sterility and male sterility were suspected to be present in populations in the western part of Hokkaido. There was also a strain that seemed to produce no seed because of intra-clonal inbreeding depression or self-incompatibility. Isozyme analysis of three enzyme systems indicated a uniformity of multienzymatic phenotype (MEP) in each population or region. The MEP grouping of populations corresponded to the type of sterility and fertility revealed by pollination and pollen culture experiments. These experiments suggested that each regional strain had its own sterility or fertility type.     

Characterization of six microsatellite markers in Trillium camschatcense using a dual‐suppression‐polymerase chain reaction technique

Trillium camschatcense is a herbaceous perennial plant distributed in Hokkaido and northern Honshu, Japan. Geographical variations in the breeding system (partial selfing or obligate outcrossing) are reported in the populations of Hokkaido. We isolated six polymorphic microsatellite loci from this species. The number of allele per locus ranged from four to 12, whereas the expected heterozygosities ranged from 0.69 to 0.83. These markers may allow further investigations to reveal the evolutionary and ecological processes of mating system in T. camschatcense.     

Phenetic diversity in the <Emphasis Type="Italic">Fritillaria camschatcensis</Emphasis> population grown on the Sapporo campus of Hokkaido University

Triploid Fritillaria camschatcensis (L.) Ker-Gawler (2n = 3x = 36) is a wild species growing in the low-lying areas of Hokkaido Island, Japan, including the Sapporo campus of Hokkaido University. Many F. camschatcensis plants grew on the campus about a century ago, but we seldom find the plants nowadays and so a project to restore this species is being planned. Because preservation of genetic diversity and composition in populations has become a major target of conservation, this study compared variation in the F. camschatcensis population on the Sapporo campus with that in two other populations in Hokkaido. Phenetic variation assessed by 57 randomly amplified polymorphic DNA markers showed that the three populations were significantly distinct from each other; analysis of molecular variance showed 64.3% of variation (P < 0.001) existed among the three populations. Comparison of phenetic diversity on the Sapporo campus population with that in the two other populations showed that the Sapporo campus population contained large genetic variation despite reduced plant numbers. These results indicate that multiplying F. camschatcensis individuals on the Sapporo campus is adequate to restore the Sapporo campus population because this population contains enough genetic diversity, and that transplanting from other populations should be avoided so as not to introduce different genotypes into the campus. These results will be used to design the restoration strategy.