小型啮齿动物种群系统调节复合因子理论的野外实验研究：食物可利用性和捕食对根田鼠种群空间行为的作用模式及其对种群调节的探讨

本项研究在野外围栏条件下,采用析因实验设计,测定食物可利用性和捕食对根田鼠（Ｍｉｃｒｏｔｕｓｏｅｃｏｎｏｍｕｓ）种群空间行为的作用模式。检验的特定假设为,高质量食物较大的可利用性能降低田鼠的攻击行为和活动;捕食能减少田鼠的活动。研究结果表明,食物可利用性能间接地和直接地影响根田鼠的空间行为。附加食物种群具有较高的密度和较小的巢区,且在诱捕期间具有较少的长距离活动和较低的攻击水平。捕食者的存在不直接影响攻击行为,但能影响诱捕期间的长距离活动,此为根田鼠对捕食者存在作出的直接反应。在阐明田鼠种群动态时,应仔细考虑上述因子相互作用的效应。     

捕食和食物交互作用条件下根田鼠季节性波动种群攻击水平及其行为多态性分析

在捕食和附加食物交互作用条件下,以恐吓、进攻、追逐、争斗及回避5类行为为变量,以恐吓、进攻、追逐计数之和的平均值作为攻击水平,测定根田鼠种群不同波动时期成体的攻击水平.发现根田鼠的攻击性与种群波动时期之间,存在明显的关联.统计分析结果表明,在种群3个波动时期,4种处理种群两性攻击型个体比例差异显著.除预防捕食者无附加食物（-P,-F）种群的雌体外,其它处理种群增长期和高峰期雌性和雄性攻击型个体的比例高于其衰减期.其中,预防捕食者附加食物（-P,＋F）种群、-P,-F种群及未预防捕食者附加食物（＋P,＋F）种群,雄性攻击型个体的比例均为增长期＞高峰期＞衰减期;在未预防捕食者无附加食物（＋P,-F）种群,雄性攻击型个体比例为高峰期＞增长期＞衰减期.各处理种群雌性攻击型个体比例的格局与雄体的不同.其中,-P,＋F种群及＋P,＋F种群为增长期＞高峰期＞衰减期,＋P,-F种群为高峰期＞增长期＞衰减期,而-P,-F种群攻击型个体比例为高峰期＞衰减期＞增长期.虽不同处理种群雌体及雄体的5类行为变量与种群密度的相关性不一致,而具有明显攻击性的恐吓、进攻及争斗3类行为则分别与种群密度呈显著或极显著的线性正相关关系,其结果与Chitty多态行为假设预测的一致;验证了所提出的特定假设：种群外部因子捕食和食物交互效应介导的攻击行为选择,是引起田鼠类种群季节性波动的主要内部因子.     

Does risk of predation by mammalian predators affect the spacing behaviour of rodents? Two large-scale experiments

Predator-prey interactions between small mammals and their avian and mammalian predators have attracted much attention. However, large-scale field experiments examining small-mammal antipredatory responses under the risk of predation by mammals are rare. As recently pointed out, the scale of experiments may cause misleading results in studies of decision-making under predation risk. We studied the effect of small mustelid predators on the spacing behaviour of the gray-tailed vole (Microtus canicaudus) and the bank vole (Clethrionomys glareolus) in two separate field enclosure experiments. The experiments were conducted during the breeding season in North America and northern Europe, where small mustelids have been suggested to be important mammalian predators of voles. As in most of the earlier laboratory studies, predation risk was simulated using fresh mustelid faeces and urine. This made it possible to compare the results from experiments at different spatial scales. We did not find any effect of increased predation risk on spacing behaviour (mean and/or maximum distance moved and home range size) or trappability in either vole species. Simulated predation risk did not affect the breeding of females in gray-tailed voles, as has previously been shown in bank voles. The results disagree with most of the studies conducted in laboratory conditions with small mammals. We discuss whether this discrepancy could be caused by differences in the scale of the experiments. Received: 12 April 1999 / Accepted: 7 October 1999     

Competition, predation and interspecific synchrony in cyclic small mammal communities

Although competition and predation are considered to be among the most important biotic processes influencing the distribution and abundance of species in space and time, the relative and interactive roles of these processes in communities comprised of cyclically fluctuating populations of small mammals are not well known. We examined these processes in and among populations of field voles, sibling voles, bank voles and common shrews in western Finland, using spatially replicated trapping data collected four times a year during two vole cycles (1987–1990 and 1997–1999). Populations of the four species exhibited relatively strong interspecific temporal synchrony in their multiannual fluctuations. During peak phases, we observed slight deviations from close temporal synchrony: field vole densities peaked at least two months earlier than those of either sibling voles or bank voles, while densities of common shrews peaked even earlier. The growth rates of all four coexisting small mammal species were best explained by their own current densities. The growth rate of bank vole populations was negatively related to increasing densities of field voles in the increase phase of the vole cycle. Apart from this, no negative effects of interspecific density, direct or delayed, were observed among the vole species. The growth rates of common shrew populations were negatively related to increasing total rodent (including water voles and harvest mice) densities in the peak phase of the vole cycle. Sibling voles appeared not to be competitively superior to field voles on a population level, as neither of these Microtus voles increased disproportionately in abundance as total rodent density increased. We suggest that interspecific competition among the vole species may occur, but only briefly, during the autumn of peak years, when the total available amount of rodent habitat becomes markedly reduced following agricultural practices. Our results nonetheless indicate that interspecific competition is not a strong determinant of the structure of communities comprised of species exhibiting cyclic dynamics. We suggest that external factors, namely predation and shortage of food, limit densities of vole populations below levels where interspecific competition occurs. Common shrews, however, appear to suffer from asymmetric space competition with rodents at peak densities of voles; this may be viewed as a synchronizing effect.     

Large manipulative experiments reveal complex effects of food supplementation on population dynamics of Brandt's voles

Although food supplementation is well known to increase population density,there is still debate on the causative effects of food supplementation on reproduction,survival,and immigration.Large manipulative experiments,which exclude any confounding effects of dispersal and predation,are essential for clarifying the debate.In this study,we investigated the effects of food supplementation on Brandt's vole population dynamics and plant community in eight large enclosures(0.48 ha each) from2010 to 2014.Food supplementation showed significant positive effects on population density due to increases in recruitment;however,it showed a complex effect on survival of voles:positive in non-breeding seasons,but negative in breeding seasons.In addition,food supplementation increased the quality of plants(as reflected by increased crude protein content),but decreased the quantity of less preferred plants in experimental enclosures.Thus,food seems to have direct positive effects on small rodents through improvement of food supply and indirect negative effects through food-induced density-dependent effects,and may have long-term effects on rodents through altering plant community composition and abundance.     

Voles on small islands: effects of food limitation and alien predation

Ecosystems of three trophic levels may be bottom-up (by food-plant availability) and/or top-down (by predators) limited. Top-down control might be of greater consequence when the predation impact comes from an alien predator. We conducted a replicated two-factor experiment with field voles (Microtus agrestis) during 2004-2005 on small islands of the outer archipelago of the Baltic Sea, south-west Finland, manipulating both predation impact by introduced American mink (Mustela vison) and winter food supply. In autumn 2004, we live-trapped voles on five islands from which mink had been consistently removed, and on four islands where mink were present, and provided half of these islands with 1.8 kg oats per vole. Body mass of female voles increased as a response to supplementary food, whereas both food supplementation and mink removal increased the body mass of male voles in subsequent spring. During winter, there was a positive effect of supplementary food, but in the subsequent summer, possible positive long-term impacts of food supplementation on field voles were not detected. Mink removal appeared not to affect density estimates of field voles during the winter and summer immediately after food addition. Trapping data from 2004 to 2005 and 2007 suggested, however, that in two out of three summers densities of voles were significantly higher in the absence than in the presence of mink. We conclude that vole populations on small islands in the archipelago of the Baltic Sea are mainly bottom-up limited during winter (outside the growing season of food plants), when food availability is low, and limited by mink predation during summer which slows population growth during the reproductive season of voles.     

小型啮齿动物种群系统调节复合因子理论的野外实验研究：食物可利用性和捕食对根田鼠种群动态作用的分析

本研究在野外围栏条件下采用析因实验设计,测定营养、捕食及空间行为对根田鼠（Ｍｉ－ｃｒｏｔｕｓｏｅｃｏｎｏｍｕｓ）种群统计特征的影响。本文旨在检验下述特定假设：高质量食物可利用性和捕食对限制小型啮齿动物种群密度具有独立的和累加的效应。３年期间,４种野外实验处理６个重复的研究结果表明,附加食物并预防捕食者处理的种群具有最高密度;未附加食物及不预防捕食者处理（对照）的种群密度最低;而单一处理的种群,其密度居中。不同处理条件下,新生个体在种群的补充模式以及种群瞬时增长率的变化均与种群密度的变动相应一致。双因素ＡＮＯＶＡ的结果证明,附加高质量食物能明显地提高根田鼠的种群密度,而对种群补充量的作用则较弱,仅接近显著水平;预防捕食者不仅能显著地作用于种群密度,更能强烈地影响种群补充量。高质量食物和捕食者的作用具有累加的性质,两者的交互作用对种群密度和补充量均无显著影响。     

To breed, or not to breed? Predation risk induces breeding suppression in common voles

Breeding suppression hypothesis (BSH) predicts that, in several vole species, females will suppress breeding in response to high risk of mustelid predation; compared to breeding females, suppressing females would gain higher chances of survival. Seminal evidence for BSH was obtained in the laboratory, but attempts to replicate breeding suppression under field conditions were less conclusive. We tested whether breeding suppression occurs in common voles (Microtus arvalis), and how population density and predation risk combined affect voles’ reproductive activity. We found that, in contrast to males, female common voles suppress reproductive activity when faced with high predation risk. Population size was not reduced despite breeding suppression. A model of the interaction between predation risk and population density revealed that predator-induced breeding suppression depends on the density of conspecifics. We concluded that breeding suppression is a viable adaptation only at low vole densities, when per capita predation risk is high. Finally, we identified the key issues of experimental design required for the consistency of future studies on breeding suppression.     

食物、捕食和种间竞争对东方田鼠种群动态的作用

采用2×2×2析因实验设计,在野外围栏条件下,测定食物、捕食和竞争物种黑线姬鼠(Apodemus agrarius)对东方田鼠(Microtus fortis)种群动态作用的格局.食物可利用性、捕食及种间竞争的独立作用对种群最小存活数均具有极显著的效应,除捕食与种间竞争的交互作用接近显著水平外,食物与种间竞争、食物与捕食者以及三者间的交互作用均不显著;三类外部因子对种群补充量的独立作用效应均达到极显著水平,且对种群补充量的作用具有累加效应;食物可利用性、捕食及种间竞争对种群繁殖成体的比例具有极显著的作用;三类外部因子对种群幼体与成体的比例具有极显著的作用.对种群年龄结构而言,与捕食者及种间竞争比较,食物可利用性是相对较弱的影响因子,在任何捕食与种间竞争交互作用条件下,食物的作用均不显著;三类外部因子均能显著地影响东方田鼠的体重增长率,但三者的交互作用对其影响不显著;MANOVA结果表明,捕食对成体存活率的作用最强烈,其次,为食物可利用性,种间竞争的作用最弱,但三者的交互作用效应不显著.对幼体的存活时间,除捕食的作用接近显著水平外,食物可利用性及种间竞争的作用均不显著.结果提供了食物可利用性、捕食和种间竞争对东方田鼠种群动态作用的充分证据,验证了食物、捕食和种间竞争对田鼠类种群动态具有独立或累加效应的总假设.     

Reproductive investment under fluctuating predation risk: Microtine rodents and small mustelids

Summary We studied the reproductive investment of microtine rodents (bank vole (Clethrionomys glareolus),Microtus epiroticus andMicrotus agrestis) in western Finland under predation risk from small mustelids. During 1984–1992, the yearly mean litter size of overwintered bank voles was smaller at high least weasel and stoat densities than at low densities (close to 3 versus 4–5). In addition, the annual mean litter size of young bank voles was negatively correlated to the least weasel density. In youngM. agrestis voles, the yearly late summer litter size was negatively associated with the autumn density of small mustelids. In the crash phase of the vole cycle (1989 and 1992), we removed small mustelids (mainly least weasels) from four unfenced areas in late April to late May and studied the reproduction of voles in four removal and comparable control areas (each 2–4 km²). Reduction of small mustelids significantly increased the proportion of pregnant bank vole females, but not that of pregnantMicrotus vole females. We conclude that predation risk apparently reduced reproductive investment of free-living bank vole females; these voles appear to trade their current parental investment against future survival and reproductive prospects. Accordingly, the presence of small mustelids (or their scent) may slow down the reproductive rate of voles. As antipredatory behaviours occurred on a large scale, our results add evidence to the hypothesis that crashes in multiannual vole cycles are driven by small mustelid predators.     

Population‐level manipulations of field vole densities induce subsequent changes in plant quality but no impacts on vole demography

Grazing‐induced changes in plant quality have been suggested to drive the negative delayed density dependence exhibited by many herbivore species, but little field evidence exists to support this hypothesis. We tested a key premise of the hypothesis that reciprocal feedback between vole grazing pressure and the induction of anti‐herbivore silicon defenses in grasses drives observed population cycles in a large‐scale field experiment in northern England. We repeatedly reduced population densities of field voles (Microtus agrestis) on replicated 1‐ha grassland plots at Kielder Forest, northern England, over a period of 1 year. Subsequently, we tested for the impact of past density on vole life history traits in spring, and whether these effects were driven by induced silicon defenses in the voles’ major over‐winter food, the grass Deschampsia caespitosa. After several months of density manipulation, leaf silicon concentrations diverged and averaged 22% lower on sites where vole density had been reduced, but this difference did not persist beyond the period of the density manipulations. There were no significant effects of our density manipulations on vole body mass, spring population growth rate, or mean date for the onset of spring reproduction the following year. These findings show that grazing by field voles does induce increased silicon defenses in grasses at a landscape scale. However, at the vole densities encountered, levels of plant damage appear to be below those needed to induce changes in silicon levels large and persistent enough to affect vole performance, confirming the threshold effects we have previously observed in laboratory‐based studies. Our findings do not support the plant quality hypothesis for observed vole population cycles in northern England, at least over the range of vole densities that now prevail here.     

The stoat Mustela erminea population decline in northern Belarus and its consequences for weasels Mustela nivalis

Abstract

In northern Belarus, we have documented a decline in the local stoat Mustela erminea population following the naturalisation of the American mink Mustela vison. The most likely cause is the reduction in the density and distribution of the main prey of stoats, the riparian voles (the water vole Arvicola terrestris and the root vole Microtus oeconomus), due to excessive predation by mink. Since the stoat population has declined, the number of weasels Mustela nivalis in marshlands has increased and their mean body mass has increased, correlated with the higher number and mean weights of rodents available for weasels in marshland compared with forest habitats.     

Predator-induced changes in population structure and individual quality of Microtus voles: a large-scale field experiment

In small mammal populations with multiannual oscillations in density, observational data have revealed cyclic changes in population structure, reproduction, and individual quality, but mechanisms inducing these changes have remained an open question. We analysed data collected during a 3-year predator reduction experiment to find out the effects of predators on population structure, reproductive parameters, and individual quality of Microtus voles (the field vole M. agrestis and the sibling vole M. rossiaemeridionalis ) in western Finland. Voles were collected by snap trapping in April, June, August, and October during 1997–1999. The yearly reduction of predators from April to October had a clear positive effect on the abundance of sibling voles but did not significantly affect the densities of field voles. Predator reduction apparently also affected the age ratio and mean body size in late summer, as well as pancreatic weights of voles. However, all observed differences between predator reduction and control areas, except those in abundance, were small and may mainly reflect a generally higher survival leading to higher densities of voles in predator reduction areas. Our results also indicated a relative lack of high quality food at population peaks but not because of reduced foraging activity in the presence of predators. We conclude that the indirect effects of vole-eating predators on the population growth of main prey are small compared to the detrimental direct effects on prey survival. In the case of less preferred prey, indirect effects of predation through reduced interspecific competition may play a role at high densities.     

Breeding state and season affect interspecific interaction types: indirect resource competition and direct interference

Indirect resource competition and interference are widely occurring mechanisms of interspecific interactions. We have studied the seasonal expression of these two interaction types within a two-species, boreal small mammal system. Seasons differ by resource availability, individual breeding state and intraspecific social system. Live-trapping methods were used to monitor space use and reproduction in 14 experimental populations of bank voles Myodes glareolus in large outdoor enclosures with and without a dominant competitor, the field vole Microtus agrestis. We further compared vole behaviour using staged dyadic encounters in neutral arenas in both seasons. Survival of the non-breeding overwintering bank voles was not affected by competition. In the spring, the numbers of male bank voles, but not of females, were reduced significantly in the competition populations. Bank vole home ranges expanded with vole density in the presence of competitors, indicating food limitation. A comparison of behaviour between seasons based on an analysis of similarity revealed an avoidance of costly aggression against opponents, independent of species. Interactions were more aggressive during the summer than during the winter, and heterospecific encounters were more aggressive than conspecific encounters. Based on these results, we suggest that interaction types and their respective mechanisms are not either-or categories and may change over the seasons. During the winter, energy constraints and thermoregulatory needs decrease direct aggression, but food constraints increase indirect resource competition. Direct interference appears in the summer, probably triggered by each individual's reproductive and hormonal state and the defence of offspring against conspecific and heterospecific intruders. Both interaction forms overlap in the spring, possibly contributing to spring declines in the numbers of subordinate species.     

Fox predation on cyclic field vole populations in Britain

The diet of the red fox Vulpes vulpes L. was studied during three winter periods in spruce pklantations in Britain, during which time the cyclic field vole Microtus agrestis L. populations varied in abundance. Field voles and roe deer Capreolus capreolus L. were the two main prey species in the diet of the red fox. The contribution of lagomorphs to fox diet never exceeded 35% and species of small mammal other than field voles were of minor importance. The contribution of field voles was dependent on vole density. The non-linear density dependent relationship with a rather abrupt increase of field voles in fox did when vole density exceeded ca 100 voles ha⁻¹ was consistent with a prey-switching response. The contribution of field voles to fox diet during the low phase of population cycles was lower in Kielder Forest than in other ecosystems with cyclic vole populations. The number of foxes killed annually by forestry rangers was consistent with the evidence from other studies that foxes preying on cyclic small rodents might show a delayed numerical response to changes in vole abundance. Estimates of the maximum predation rate of the fox alone (200–290 voles ha⁻¹ of vole habitat year⁻¹) was well above a previously predicted value for the whole generalist predator community in Kielder Forest. Our data on the functional response of red foxes and estimates of their predation rates suggest that foxes should have a strong stabilising impact on vole populations, yet voles show characteristic 3-4 yr cycles.     

The predation risks of interspecific eavesdropping: weasel–vole interactions

Competing species benefit from eavesdropping on each other's signals by learning about shared resources or predators. But conspicuous signals are also open to exploitation by eavesdropping predators and should also pose a threat to other sympatric prey species. In western Finland, sibling voles Microtus rossiameridionalis and field voles M. agrestis compete for food and space, and both species rely upon scent marks for intraspecific communication. Both vole species are prey to a range of terrestrial scent hunting predators such as least weasels, however, the competitively superior sibling voles are taken preferentially. We tested in large out‐door enclosures whether field voles eavesdrop on the signals of its competitor, and whether they behave as though this eavesdropping carries a risk of predation. We presented field voles with scent marks from unknown conspecifics and sibling voles and measured their visitation, activity and scent marking behaviours at these scents under high (weasel present) and low (weasel absent) predation risk. Field voles readily visited both field and sibling vole scents under both high and low predation risk; however their activity at sibling vole scent marks declined significantly under increased predation risk. In contrast, predation risk did not affect field voles’ activity at conspecific scents. Thus, field voles were compelled to maintain eavesdropping on heterospecific scents under an increased risk of predation, however they compensated for this additional risk by reducing their activity at these risky scents. Scent marking rates declined significantly under high predation risk. Our results therefore reveal a hidden complexity in the use of social signals within multi‐species assemblages that is clearly sensitive to the potential for increased predation risk. The predation risks of interspecific eavesdropping demonstrated here represents a significant generalisation of the concept of associational susceptibility.     

局部环境增温对根田鼠冬季种群的影响

通过建立开顶式增温小室模拟全球变暖的实验, 对海北高寒草甸地区实验增温样地及其对照样地内根田鼠的冬季种群进行调查, 旨在研究局部增温对根田鼠冬季种群的可能影响。结果表明, 在冬季, 实验增温草甸样地和灌丛样地内根田鼠的种群密度均显著高于其对照( P < 0.05) ; 实验增温灌丛样地与对照间性比的差异不显著( P > 0.05) ; 增温样地和对照之间、不同植被类型的增温样地之间、对照样地之间, 根田鼠留存率、平均体重及年龄结构的差异均不显著( P > 0.05) ; 有从对照样地向增温样地单方向迁移的记录。总之, 局部环境增温导致实验样地内根田鼠的冬季种群密度明显上升, 而其性比、存活率、种群平均体重以及年龄结构无明显变化; 在冬季, 根田鼠有从对照样地向增温样地扩散或迁移的趋势。     

Experimental tests of predation and food hypotheses for population cycles of voles

Pronounced population cycles are characteristic of many herbivorous small mammals in northern latitudes. Although delayed density-dependent effects of predation and food shortage are often proposed as factors driving population cycles, firm evidence for causality is rare because sufficiently replicated, large-scale field experiments are lacking. We conducted two experiments on Microtus voles in four large predator-proof enclosures and four unfenced control areas in western Finland. Predator exclusion induced rapid population growth and increased the peak abundance of voles over 20-fold until the enclosed populations crashed during the second winter due to food shortage. Thereafter, voles introduced to enclosures which had suffered heavy grazing increased to higher densities than voles in previously ungrazed control areas which were exposed to predators. We concluded that predation inhibits an increase in vole populations until predation pressure declines, thus maintaining the low phase of the cycle, but also that population cycles in voles are not primarily driven by plant-herbivore interactions.     

Determinants of reproductive success in voles: space use in relation to food and litter size manipulation

Spacing behaviour of female mammals is suggested to depend on the distribution and abundance of food. In addition, food limitation has been found to constrain the reproductive success of females. However, whether females maximize their reproductive success by adjusting space use in relation to current food availability and reproductive effort (e.g. litter size) has not been experimentally studied. We examined these questions by manipulating simultaneously food resources (control vs. food supplementation) and litter sizes (control vs. plus two pups) of territorial female bank voles (Clethrionomys glareolus) in large outdoor enclosures. Females with supplementary food had smaller home ranges (foraging area) and home range overlaps than control females, whereas litter size manipulation had no effect on space use. In contrast, the size of territory (exclusive area) was not affected by food supplementation or litter size manipulation. As we have previously shown elsewhere, extra food increases the reproductive success of bank vole females in terms of size and proportion of weaned offspring. According to the present data, greater overlap of female home ranges had a negative effect on reproductive success of females, particularly on survival of offspring. We conclude that higher food availability increases the reproductive success of bank vole females, and this effect may be mediated through lower vulnerability of offspring to direct killing and/or detrimental effects from other females in the population. Moreover, it seems that when density of conspecifics is controlled for, home range sizes of females, but not territoriality, is related to food resources in Clethrionomys voles.     

Predator–vole interactions in northern Europe: the role of small mustelids revised

The cyclic population dynamics of vole and predator communities is a key phenomenon in northern ecosystems, and it appears to be influenced by climate change. Reports of collapsing rodent cycles have attributed the changes to warmer winters, which weaken the interaction between voles and their specialist subnivean predators. Using population data collected throughout Finland during 1986–2011, we analyse the spatio-temporal variation in the interactions between populations of voles and specialist, generalist and avian predators, and investigate by simulations the roles of the different predators in the vole cycle. We test the hypothesis that vole population cyclicity is dependent on predator–prey interactions during winter. Our results support the importance of the small mustelids for the vole cycle. However, weakening specialist predation during winters, or an increase in generalist predation, was not associated with the loss of cyclicity. Strengthening of delayed density dependence coincided with strengthening small mustelid influence on the summer population growth rates of voles. In conclusion, a strong impact of small mustelids during summers appears highly influential to vole population dynamics, and deteriorating winter conditions are not a viable explanation for collapsing small mammal population cycles.