Frontiers in Population Ecology of Microtine Rodents: a Pluralistic Approach to the Study of Population Ecology
Nils Chr. STENSETH*,1), Takashi SAITOH*,2) and Nigel G. YOCCOZ*,3)
* Centre for Advanced Study, Norwegian Academy of Science and Letters, Drammensveien 78, N-0271 Oslo, Norway
1)Division of Zoology, Department of Biology, University of Oslo, P.O. Box 1050 Blindern, N-0316 Oslo, Norway. E-mail: n.c.stenseth@bio.uio.no
2)Hokkaido Research Center, Forestry and Forest Products Research Institute, Sapporo 062-8516, Japan. E-mail: bedford@ffpri-hkd.affrc.go.jp
3) Department of Arctic Ecology, Norwegian Institute for Nature Research, Storgata 25, N-9005 Troms(I?(J, Norway. E-mail: nigel.yoccoz@ninatos.ninaniku.no
Abstract. Current challenges for the study of population ecology of microtine rodents are reviewed. Comparisons with other taxonomic groups (insects, birds, large mammals) are given throughout. A major challenge is to link patterns and processes (i.e. mechanisms) better than is the case today. Other major challenges include the furthering of our understanding of the interaction between deterministic and stochastic processes, and as part thereof, the interaction between density-dependent and density-independent processes. The applicability of comparative studies on populations exhibiting different temporal patterns is, in this connection, emphasized. Understanding spatio-temporal dynamical patterns is another major challenge, not the least from a methodological point of view. Long-term and large-scale ecological data on population dynamics (in space and time) are critical for this. Looking for consistency between hypothesized mechanisms and observed patterns is emphasized as a good platform for further empirical and theoretical work. The feedback process between different approaches to the study of microtine population ecology (observational studies, experimental manipulative studies, statistical modeling and mathematical modeling) are discussed. We recommend a pluralistic approach (involving both observational and experimental as well as theoretical studies) to the study of small rodent ecology.
Key words: Clethrionomys rufocanus, experimental manipulation and testing, mathematical modeling, patterns and processes, statistical modeling.
Yukibumi KANEKO1), Keisuke NAKATA2), Takashi SAITOH3), Nils Chr. STENSETH4)
and Ottar N. BJ(I?(JRNSTAD4)
1) Biological Laboratory, Faculty of Education, Kagawa University, Takamatsu 760-0016 Japan. E-mail: kaneko@laplace.ed.kagawa-u.ac.jp
2) Hokkaido Forestry Research Institute, Bibai 079-0198, Japan. E-mail: nakata@hfri.bibai.hokkaido.jp
3) Hokkaido Research Center, Forestry and Forest Products Research Institute, Sapporo 062-8516, Japan. To whom correspondence should be addressed. E-mail: bedford@ffpri-hkd.affrc.go.jp
4) Division of Zoology, Department of Biology, University of Oslo, P.O. Box 1050 Blindern, N-0316 Oslo, Norway. E-mail: n.c.stenseth@bio.uio.no; o.n.bjornstad@bio.uio.no
Abstract. The biology of the grey-sided vole Clethrionomys rufocanus in Hokkaido, concerning taxonomy, morphology, phylogeny, distribution, and natural history, is reviewed. Applied issues in forest management (damage, control and census) are also historically mentioned. Although Clethrionomys rufocanus of Hokkaido was originally identified as a distinct species, Evotomys (= now Clethrionomys) bedfordiae Thomas, 1905, current literature generally refers to the grey-sided vole of Hokkaido as Clethrionomys rufocanus or as C. rufocanus bedfordiae (in vernacular name, the Bedford(IU(Js red-backed vole). The grey-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 grey-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. The vole C. 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 takes this vole. Damage by voles(IU(J barking used to be sever on forest plantations in Hokkaido. Censuses of small rodents have been carried out for management purpose since 1954.
Key words: biogeography, forest damage, life history, monitoring, taxonomy.
Social Organization of the Vole Clethrionomys rufocanus and its Demographic and Genetic Consequences: a Review
Yasuyuki ISHIBASHI1), Takashi SAITOH2) and Masakado KAWATA3)
1) Chromosome Research Unit, Faculty of Science, Hokkaido University, North 10, West 8, Kita-ku, Sapporo 060-0810, Japan. E-mail: stone@ees.hokudai.ac.jp
2) Hokkaido Research Center, Forestry and Forest Products Research Institute, Sapporo 062-8516, Japan. E-mail: bedford@ffpri-hkd.affrc.go.jp
3) Biological Institute, Graduate School of Science, Tohoku University, Aoba, Sendai, 980-8578, Japan. E-mail: kawata@mail.cc.tohoku.ac.jp
Abstract. Recent findings on the relationship between social interaction and demographic process in the grey-sided vole Clethrionomys 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 character 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.
Key words: dispersal behavior, kin cluster, philopatry, spatial genetic structure, territoriality, the grey-sided vole.
Kin-related Social Organization in a Winter Population of the Vole Clethrionomys rufocanus
Yasuyuki ISHIBASHI*,1), Takashi SAITOH2), Syuiti ABE* and Michihiro C. YOSHIDA*
* Chromosome Research Unit, Faculty of Science, Hokkaido University, North 10, West 8, Sapporo 060-0810, Japan. 1) E-mail: stone@ees.hokudai.ac.jp
2) Hokkaido Research Center, Forestry and Forest Products Research Institute, Sapporo 062-8516, Japan. E-mail: bedford@ffpri-hkd.affrc.go.jp
Abstract. Kinship among gray-sided voles, Clethrionomys 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 (September-November). These philopatric individuals aggregated and formed an maternal family in the winter. Several females which failed to reproduce were solitary in 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 quickly after the onset of spring reproduction. Most females established a territory near the wintering site and made a kin-cluster, 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.
Key words: communal nesting, kinship, microsatellite DNA, parentage.
The Population Dynamics of the Vole Clethrionomys rufocanus in Hokkaido, Japan
Takashi SAITOH*,1), Nils Chr. STENSETH*,2), and Ottar N. BJ(I?(JRNSTAD2)
1)Hokkaido Research Center, Forestry and Forest Products Research Institute, Sapporo 062-8516, Japan. E-mail: bedford@ffpri-hkd.affrc.go.jp
2) Division of Zoology, Department of Biology, University of Oslo, P.O. Box 1050 Blindern, N-0316 Oslo, Norway. E-mail: n.c.stenseth@bio.uio.no; o.n.bjornstad@bio.uio.no
* Centre for Advanced Study, Norwegian Academy of Science and Letters, Drammensveien 78, N-0271 Oslo, Norway
Abstract. 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 topographical 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. The other 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 northwest.
Key words: cycle, density-dependence, geographical gradient, population variability, spatial scale, regional synchrony.
Mapping the Regional Transition to Cyclicity in Clethrionomys rufocanus: Spectral Densities and Functional Data Analysis
Ottar N. BJ(I?(JRNSTAD*, Nils Chr. STENSETH*, Takashi SAITOH and Ole Chr. LINGJ(I>(JRDE*
* Division of Zoology, Department of Biology, University of Oslo, P.O. Box 1050 Blindern, N-0316 Oslo, Norway. E-mail: o.n.bjornstad@bio.uio.no; n.c.stenseth@bio.uio.no; ole@ifi.uio.no
Hokkaido Research Center, Forestry and Forest Products Research Institute, Sapporo 062-8516, Japan. E-mail: bedford@ffpri-hkd.affrc.go.jp
Abstract. 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 seasonal-forcing on the trophic interactions in which the gray-sided voles are involved.
Key words: biogeography, microtine cycle, population fluctuation, scale of regulation, seasonality.
Seasonal Forcing on the Dynamics of Clethrionomys rufocanus: Modeling Geographic Gradients in Population Dynamics
Nils Chr. STENSETH*, , Ottar N. BJ(I?(JRNSTAD* and Takashi SAITOH ,$B_ë(J
* Division of Zoology, Department of Biology, University of Oslo, P.O. Box 1050 Blindern, N-0316 Oslo, Norway. E-mail: n.c.stenseth@bio.uio.no; o.n.bjornstad@bio.uio.no
Center of Advanced Studies, Drammensvein 78, N-0271, Oslo, Norway
$B_(JHokkaido Research Center, Forestry and Forest Products Research Institute, Sapporo 062-8516, Japan. E-mail: bedford@ffpri-hkd.affrc.go.jp
Abstract. We interpret the gradient in population dynamics from the southwestern part of the island of Hokkaido to its northeastern part within the framework of a phenomenological model. In Hokkaido, as in other northern regions, both spring and fall is considered as short transition periods between the two main seasons (IP(J 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.
Key words: density-dependence, length of summer and winter, phenomenological model, seasonal and annual dynamics, the grey-sided vole.
The Role of Vole Populations in Prevalence of the Parasite (Echinococcus multilocularis) in Foxes
Takashi SAITOH1) and Kenichi TAKAHASHI2)
1) Hokkaido Research Center, Forestry and Forest Products Research Institute, Sapporo 062-8516, Japan. E-mail: bedford@ffpri-hkd.affrc.go.jp
2) Hokkaido Institute of Public Health, Kita 19, Nishi 12, Sapporo 060-0819, Japan. E-mail: takaken@iph.pref.hokkaido.jp
Abstract. Effects of population fluctuation of the gray-sided vole (Clethrionomys rufocanus) on the prevalence (infection rates) of the parasite Echinococcus 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.
Key words: Clethrionomys rufocanus, density-dependence, functional response, numerical response, Vulpes vulpes.
The Demography of Clethrionomys rufocanus: from Mathematical and Statistical Models to Further Field Studies
Nigel G. YOCCOZ*,1), Keisuke NAKATA*,2), Nils Chr. STENSETH*,3) and Takashi SAITOH*,4)
* Centre for Advanced Study, Norwegian Academy of Science and Letters, Drammensveien 78, N-0271 Oslo, Norway
1) Department of Arctic Ecology, Norwegian Institute for Nature Research, Storgata 25, N-9005 Troms(I?(J, Norway. E-mail: nigel.yoccoz@ninatos.ninaniku.no
2) Hokkaido Forestry Research Institute, Bibai, Hokkaido 079-0198, Japan. E mail: nakata@hfri.bibai.hokkaido.jp
3) Division of Zoology, Department of Biology, University of Oslo, POB 1050 Blindern, N-0316 Oslo, Norway. E-mail: n.c.stenseth@bio.uio.no
4) Hokkaido Research Centre, Forestry and Forest Products Research Institute, Sapporo 062-8516, Japan. E-mail: bedford@ffpri-hkd.affrc.go.jp
Abstract. Until recently, most studies of 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 one hand and in capture-recapture statistical modeling on the other hand, now allow for improved analyses. We reviewed 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 grey-sided vole Clethrionomys 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, including C. rufocanus. Investigating the relative importance of the different demographic parameters (e.g. survival, maturation, dispersal) will require studies done on larger scale than is usual today, with more effort devoted to the low density phase. Special emphasis is given to study-design, and to experimental designs tailored for the study of specific demographic mechanisms.
Key words: age-structured models, seasonality, survival, capture-recapture, elasticity.
The Population Biology of Coevolution
John N. Thompson
Departments of Botany and Zoology, Washington State University, Pullman, WA 99164 U.S.A. E-mail: jnt@wsu.edu (or jnt@nceas.ucsb.edu); National Center for Ecological Analysis and Synthesis University of California , Santa Barbara 735 State Street, Suite 300 Santa Barbara, CA 93101-3351 U.S.A.
Abstract. New populational approaches to the study of coevolution among species are confronting two major problems: the geographic scale at which coevolution proceeds, and the long-standing issue of how species may coevolve with more than one other species. By incorporating the ecological structure of life histories and populations into analyses of the coevolutionary process, these studies are indicating that coevolutionary change is much more ecologically dynamic than indicated by earlier work. Rather than simply a slow, stately process shaping species over long periods of time, parts of the coevolutionary process may proceed rapidly (sometimes observable in less than a decade) , continually molding and remolding populations and communities locally and over broad geographic scales.
Key words: coevolution, gene-for-gene interaction, geographic structure, local adaptation, rapid evolution.
Receptivity of Female Remating and Sperm Number in the Sperm Storage Organ in the Bean Bug, Riptortus clavatus (Heteroptera: Alydidae)
Tamito SAKURAI
Laboratory of Applied Entomology, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya 464-8601, Japan; Present address: Laboratory of Biological Communication, Research Institute for Bioresources, Okayama University, Kurashiki 710, Japan. E-mail: sakurai@rib. okayama-u.ac.jp
Abstract. This study examines the relationship between the number of sperm in the seminal receptacle (spermatheca) and the receptivity of female remating in the bean bug Riptortus clavatus Thunberg. On the 21st day after the first mating when receptivity to remating was > 70 %, females receptive to remating had significantly fewer sperm (< 40 on average) in the spermathecae than females reluctant to do (about 150 on average). However, averages of the number of eggs laid by receptive and reluctant females within 21 days were almost same. The proportion of fertilized eggs for receptive females at 15-21 days after copulation was significantly lower than that for reluctant females. Spermatozoa transferred from a male to a female's spermatheca were detected 5 min after copulation and then increased continuously to about 500 with the first hour. When copulation durations were manipulated artificially, the shorter the copulation period ( = females had less sperm in their spermathecae) the higher the remating rate became. Females may perceive the number of sperm in their seminal receptacles and then determine whether they copulate or not. These results support the hypothesis that females mate multiply in order to replenish inadequate sperm supplies to fertilize all eggs produced.
Key words: female remating, sperm number, spermatheca, fertilization, Riptortus clavatus