Changes in population structure and reproduction during a 3-yr population cycle of voles

Cyclic changes in population growth rate are caused by changes in survival and/or reproductive rate. To find out whether cyclic changes in reproduction are an important part of the mechanism causing cyclic fluctuations in small mammal populations, we studied changes in the population structure and reproduction of field voles ( Microtus agrestis ), sibling voles ( M. rossiaemeridionalis ), bank voles ( Clethrionomys glareolus ), and common shrews ( Sorex araneus ) in western Finland during 1984–1992, in an area with 3-yr vole cycles. We also modelled the population growth of voles using parameter values from this study. The animals studied were collected by snap trapping in April, May, June, August, September, and, during 1986–1990, also in October. We found several phase-related differences in the population structure (age structure, sex ratio, proportion of mature individuals) and reproduction (litter size, length of the breeding season) of voles. In non-cyclic common shrews, the only significant phase-related difference was a lower proportion of overwintered individuals in the increase phase. According to the analyses and the vole model, phase-related changes in litter size had only a minor impact on population growth rate. The same was true for winter breeding in the increase phase. The length and intensity of the summer breeding season had an effect on yearly population growth but this impact was relatively weak compared to the effect of cyclic changes in survival. The population increase rates of Microtus were delayed dependent on density (8–12-month time lag). Our results indicate that cyclic changes in reproduction are not an important part of the mechanism driving cyclic fluctuations in vole populations. Low survival of young individuals appeared to play an important role in the shift from the peak to the decline phase in late summer and early autumn.     

Survival of cohorts in a fluctuating population of the vole Microtus townsendii

Survival patterns of cohorts are described during a population cycle of the vole Microtus townsendii near Vancouver, British Columbia, Canada. A two–year live–trapping study on both enclosed and unfenced populations showed that cohorts during the increase phase of growth lived longest and had the best survival. Smaller voles in the peak density spring cohort had poor survival, but survival increased during the peak density summer. Survival of cohorts in the decline phase breeding season was very poor. The suggestions are made that changes in spacing behaviour may cause changes in cohort survival and that the causes of rapid changes in survival need to be determined.     

Effects of competition and season on survival and maturation of young bank vole females

In territorial microtines intra-specific density dependent processes can limit the maturation of individuals during the summer of their birth. This may have demographic consequences by affecting the number and the age distribution of breeding individuals in the population. Little is known about this process on a community level, though populations of many northern microtine species fluctuate in synchrony and are known to interfere socially with each other. We experimentally studied the influence of the field vole Microtus agrestis on maturation, breeding, space use and survival of weanling bank voles, Clethrionomys glareolus. Two additive competition experiments on bank vole populations were conducted in large outdoor enclosures, half of them additionally housing a field vole population. In a mid-summer experiment low population density and absence of older breeding females minimised intra-specific competition. Survival was not affected by the presence of field voles. Season had a significant effect on both the probability of maturation and breeding of the weanlings. Competition with field voles significantly delayed breeding, and coupled with seasonal effects decreased the probability of breeding. In a late-summer experiment breeding and survival of bank vole weanlings were studied for three weeks as part of a high density breeding bank vole population. Weanlings did not mature at all nor were their space use and survival affected by the presence of field voles. Our results show that competition with other species can also have an impact on breeding of immatures. In an extreme seasonal environment, even a short delay of breeding may decrease survival chances of offspring. Seasonal and competition effects together may thus limit the contribution of year born females to reproductive output of the population. Other studies have shown that adult breeding bank voles suffer lower survival in the presence of field voles, but this study showed no survival effects on the weanlings. Thus it might be beneficial for weanlings to stay immature especially in the end of the breeding season and postpone reproduction to the next breeding season if densities of competing species are high.     

Phase dependence in winter physiological condition of cyclic voles

Lack of food resources has been suggested as a factor which limits the growth of cyclic vole populations. During peak phases of the cycle, vole population growth typically ceases during late autumn or early winter, and is followed by a decrease in density over the winter. To investigate whether this decrease is due to increased mortality induced by a depletion of food resources, we studied overwinter food consumption and physiological condition of field voles ( Microtus agrestis ) in western Finland in both an increase and a decrease phase of a three-year population cycle. The growth rate of vole populations was negatively related both to prevailing vole densities and to densities six months earlier. The condition index of voles, as well as their blood levels of haematocrit, proteins, free fatty acids and immunoglobulin G, were positively related to population growth rate when populations were declining. When populations were increasing, these parameters tended to be negatively related to population growth rate. The overall physiological condition of voles was lower in the winter of the decrease phase as compared to the increase phase. The return rate of voles, a proxy of survival, was also lower in the decrease than in the increase phase of the cycle and positively related to haematocrit levels. Almost 90% of all green vegetation shoots were consumed by voles during the winter of the decrease phase while only two thirds were eaten in the increase phase. Our results suggest that the winter decrease phase of cyclic vole populations is associated with both a deterioration in the physiological condition of voles and a significant depletion of winter food resources. This implies that malnutrition induces poor physiological condition in voles, which in turn may increase mortality either directly through starvation or indirectly through increased susceptibility to predators and pathogens.     

Rate of population change in voles from different phases of the population cycle

Factors involved in causing cyclic vole populations to decline, and in preventing populations from recovering during the subsequent low density phase have long remained unidentified. The traditional view of self-regulation assumes that an increase in population density is prevented by a change in the quality of individuals within the population itself, but this is still inadequately tested in the field. We compared the population growth of wild field voles ( Microtus agrestis ) from the low phase (conducted in 1998) with that of voles from the increase phase (conducted in 1999) in predator-proof enclosures (each 0.5 ha) in western Finland. Within a few months, enclosed vole populations increased to high density, and the realised per capita rate of change over the breeding season did not differ between the populations from different cycle phases. This implies that the recovery of populations from the low phase was not hindered by an impoverishment in quality of individual voles. Accordingly, we suggest that population intrinsic factors (irrespective of the mechanisms they are based on) are unlikely to play a significant role in the generation of cyclic density fluctuations of voles. Instead, we discovered direct density-dependent regulation in the vole populations. Accurate estimates of population growth and the observed density dependence provide important information for empirically based models on population dynamics of rodents.     

Breeding suppression in the bank vole as antipredatory adaptation in a predictable environment

Summary In northern Fennoscandia, microtine rodent populations fluctuate cyclically. The environment of an individual vole can be considered to be predictable when the risks of predation and intra- and interspecific competition change with the cycle, such that both are high during the population highs of voles. The risk of predation is also high during the vole crash. After the crash, the vole population is characterized by low intra- and interspecific competition and low predation pressure. The main predators affecting voles during the crash are the small mustelids, least weasel and stoat. The density of these specialist predators declines drastically during the winter after the vole crash. We studied experimentally the impact of the perceived presence of stoats on the breeding and mating behaviour of voles. In a series of breeding experiments with bank voles,Clethrionomys glareolus, both old and young females suppressed breeding when exposed to the odour of stoats,Mustela erminea. The weights of females decreased in both experimental and control groups, but more among the voles under odour exposition. It seems that females actively avoided copulations under high predation risk and that breeding suppression is mediated by a change in female mating behaviour. There was no change in male behaviour or physical condition between the experimental and control treatments. An alternative mechanism for the observed breeding suppression could be the one caused by decreased feeding in females mediated with low energy intake which does not allow breeding. Regardless of its mechanism, delay of breeding should increase the probability of non-breeding females to survive to the next breeding season. The females surviving the crash should gain a strong selective advantage in a predator-free environment of the subsequent breeding season, which could explain the adaptive function of this antipredatory strategy.     

Reproduction of the bank vole, Clethrionomys glareolus, in northern and southern Sweden during several seasons and in different phases of the vole population cycle

The breeding biology of the bank vole was studied in northern and southern populations in Sweden in the years 1973–76. Trapped specimens supplied organ weights and histological data, which were utilized to describe the breeding season, number and size of litters, reproductive losses, spermatogenesis, and sexual maturation. In the north the populations are cyclic. During the increase phase of the cycle the breeding season was long, litter sizes and gonad weights were large, and there was maturation of yearlings in the summer. During the peak phase reproduction was impaired in all these respects. In southern Sweden there was no cyclicity, and the reproductive events varied less, but in 1976 the litters were larger than usual and the season was much extended.
In the south the voles born during the early part of the season regularly became sexually mature during their first summer. The differences in reproductive biology are related to population dynamics and discussed in terms of different hypotheses concerning vole population cyclicity.     

Fluctuating food supply affects the clutch size of Tengmalm's owl independent of laying date

Summary In western Finland, yearly median laying dates of Tengmalm's owls varied from 14 March to 27 April during 1973–1989 and were negatively correlated with the winter densities of voles. Yearly mean clutch sizes varied from 4.0 to 6.7 and were more closely related to the spring than to the winter densities of voles. The yearly mean clutch size decreased with yearly median laying date. The 3-year vole population cycle is typical of the study area. The start of egg-laying was earliest in the peak phase of the cycle (median laying date 22 March), when vole numbers are high during egg-laying, but decline rapidly to low numbers in the next autumn or winter. In the increase phase (1 April) vole abundances are moderate at the time of laying, but increase to a peak in the next autumn or winter. In the low phase (15 April) voles are scarce in spring and in the preceding winter, starting to increase in late summer. Clutch size and female body mass were independent of laying date in the low phase, decreased slowly but significantly in the increase phase, and declined abruptly in the peak phase. These trends also held when the effects of territory quality, female age and male age were ruled out. When comparing the same laying periods, clutch sizes were significantly larger in the increase than in other phases of the cycle, but there was no difference between the peak and low phases. Supplementary feeding prior to and during egg-laying increased clutch size independent of laying date. These results agreed with the income model (the rate of energy supply during laying determines clutch size). Tengmalm's owls invest most in a clutch in the increase phase, as the reproductive value of eggs is largest because of high survival of yearlings. A high reproductive effort may be adaptive during this phase, because the availability of voles is predictable during the laying period.     

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

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.     

Fading out of vole and predator cycles?

Northern voles and lemmings are famous for their spectacular multiannual population cycles with high amplitudes. Such cyclic vole populations in Scandinavia have shown an unexpected and marked long-term decline in density since the early 1970s, particularly with a marked shift to lower spring densities in the early 1980s. The vole decline, mainly characterized by a strongly decreased rate of change in numbers over winter, is associated with an increased occurrence of mild and wet winters brought about by a recent change in the North Atlantic Oscillation. This has led to a decrease in winter stability and has shortened the period with protective snow cover, the latter considered as an important prerequisite for the occurrence of multiannual, high-amplitude cycles in vole populations. Although the vole decline is predicted to be negative for predators' reproduction and abundance, empirical data showing this are rare. Here we show that the dynamics of a predator-prey system (Tengmalm's owl, Aegolius funereus, and voles), have in recent years gradually changed from 3-4 yr, high-amplitude cycles towards more or less annual fluctuations only.     

Do intrinsic or extrinsic factors limit reproduction in cyclic populations of Clethrionomys glareolus and C. rufocanus?

Changes in reproduction and functional age structure of females in cyclic populations of Clethrionomys glareolus and C. rufocanus were studied by live-trapping individually marked voles during 1980 to 1984 in northern Sweden. A complete population cycle was observed in both species, with a synchronous 'summer-decline' in 1982. In both species, the length of the breeding season became successively shorter towards the peak, and it was extremely short at the decline. When the populations expanding, the density of breeding females increased in a sigmoid way, and thereafter it remained fairly constant throughout the summer. At the decline, the density of breeding females decreased successively from spring to autumn. Year-born females matured and bred in all years except at the decline. Intrinsic factors, such as spacing behaviour of breeding females, are thought to limit the density of breeders in general, but only when the populations are expanding. Other factors such as deteriorating food conditions are more likely to operate at the decline.     

Spatiotemporal dynamics of Puumala hantavirus in suburban reservoir rodent populations

The transmission of pathogens to susceptible hosts is dependent on the vector population dynamics. In Europe, bank voles (Myodes glareolus) carry Puumala hantavirus, which causes nephropathia epidemica (NE) in humans. Fluctuations in bank vole populations and epidemics in humans are correlated but the main factors influencing this relationship remain unclear. In Belgium, more NE cases are reported in spring than in autumn. There is also a higher incidence of human infections during years of large vole populations. This study aimed to better understand the link between virus prevalence in the vector, vole demography, habitat quality, and human infections. Three rodent populations in different habitats bordering Brussels city, Belgium, were studied for two years. The seroprevalence in voles was influenced first by season (higher in spring), then by vole density, vole weight (a proxy for age), and capture site but not by year or sex. Moreover, voles with large maximal distance between two captures had a high probability for Puumala seropositivity. Additionally, the local vole density showed similar temporal variations as the number of NE cases in Belgium. These results showed that, while season was the main factor influencing vole seroprevalence, it was not sufficient to explain human risks. Indeed, vole density and weight, as well as the local habitat, were essential to understanding the interactions in these host‐pathogen dynamics. This can, in turn, be of importance for assessing the human risks.     

Tawny owl prey remains indicate differences in the dynamics of coastal and inland vole populations in southern Finland

Some studies suggest that mild winters decrease overwinter survival of small mammals or coincide with decreased cyclicity in vole numbers, whereas other studies suggest non-significant or positive relationships between mild winter conditions and vole population dynamics. We expect for the number of voles to be higher in the rich and low-lying habitats of the coastal areas than in the less fertile areas inland. We assume that this geographical difference in vole abundances is diminished by mild winters especially in low-lying habitats. We examine these relationships by generalized linear mixed models using prey remains of breeding tawny owls Strix aluco as a proxy for the abundance of voles. The higher number of small voles in the coastal area than in the inland area suggest that vole populations were denser in the coastal area. Vole populations of both areas were affected by winter weather conditions particularly in March, but these relationships differed between areas. The mild ends of winter with frequent fluctuations of the ambient temperature around the freezing point (“frost seesaw”) constrained significantly the coastal vole populations, while deep snow cover, in general after hard winters, was followed by significantly lowered number of voles only in the inland populations. Our results suggest that coastal vole populations are more vulnerable to mild winters than inland ones. We also show that tawny owl prey remains can be used in a meaningful way to study vole population dynamics.     

Population dynamics and spatial behaviour of <Emphasis Type="Italic">Microtus tatricus</Emphasis> (Arvicolinae,Rodentia)

The population dynamics of the Tatra vole Microtus tatricus (Kratochvíl, 1952) (Arvicolinae, Rodentia) was monitored as part of a long-term study (1996–2008) of demography of small mammals conducted in Western Tatra Mountains—Roháče, Slovakia. We observed low abundance and population densities and a balanced sex ratio but slightly more frequent captures of females. Reproductively active Tatra voles were significantly larger and heavier than reproductively inactive voles. Reproduction in both sexes tended to begin in early spring, and females moved less than males. Individuals start to reproduce after overwintering. Spatial characteristics differed between sexes, with home range size, distance travelled, and observed range length being non-significantly greater in males than in females, suggesting greater male mobility. Females remained longer on the site than did males. Mature individuals of both sexes exhibited territoriality during the peak of breeding season in spring. Home range overlap occurred more often within females, and mainly in summer and autumn.     

Redundancy, synergism, and active inhibitory range of non-host volatiles in reducing pheromone attraction in European spruce bark beetle Ips typographus

Brandt's voles ( Microtus brandti ) are small native mammals that inhabit the grasslands of Inner Mongolia, China. The species is considered a pest, particularly during population outbreaks, which have increased in frequency since 1970 from 1 every 7 years to 1 every 3 to 5 years. Using historical records taken between 1948 and 1998, we found that there was significant correlation between years for which the monthly averages of the Southern Oscillation Index (SOI) were consistently high, and years in which outbreaks occurred. Also there was a tendency for outbreaks not to occur in years with precipitation above or below average. For some years at some sites, annual or biannual estimates are available for the density of Brandt's vole populations. We found that the seasonal rate of increase over the non-breeding season from autumn to spring was negatively correlated with the density in autumn. The rate of increase over the breeding season from spring to autumn was independent of the density in spring but instead, reflects the species' preference for habitat with short, sparse grass; populations do not persist in highly degraded grasslands or in tall, dense grassland. The link between outbreaks and climatic indices, and the numerical response of Brandt's voles to particular habitat characteristics, suggest that current grazing intensity tends to maintain grass at low height in years with average precipitation. The substantial increase in livestock numbers over the last 50 years appears to have increased the number of years when the balance of grazing and plant growth favours high rates of increase in Brandt's vole populations, and hence, there has been an increase in the frequency of outbreaks.     

Size and growth characteristics of dispersing voles,Microtus townsendii

Summary In a peak population of Microtus townsendii, adults and subadults dispersed during the spring decline, and subadults and juveniles dispersed during the summer and fall. Voles born in the spring dispersed before the start of the next year's breeding season, whereas fall-born voles dispersed during the next year's breeding season. Voles under 50 g, when they dispersed, had faster growth rates than similar-sized residents, but voles over 59 g, when they dispersed, had slower growth rates than similar-sized residents. Dispersing and resident voles 50–59 g had no consistent trend in growth rates.     

Field Vole Microtus agrestis abundance and Hen Harrier Circus cyaneus diet and breeding in Scotland

In many parts of the global range, voles form an important part of the diet of Hen Harriers Circus cyaneus , and breeding numbers are correlated with the abundance of these small mammals. In Scotland, however, little information is available on harrier diet in the spring and our understanding of causes of variation in harrier breeding density is complicated by human interference. In this paper we explore the relationship between Field Vole Microtus agrestis abundance and harrier spring diet, density and productivity in southern Scotland. Over three years, voles occurred on average in 67% of pellets, and 79% in years of high and intermediate vole abundance. From 1992, the number of breeding harriers increased following protection from illegal persecution. After accounting for this trend, harrier numbers correlated strongly with vole abundance. Harrier clutch size was also correlated with vole abundance. Although fledging success tended to be greater in years of vole increase than in years of vole decline, fledging success was not significantly correlated with the relative abundance of voles, or with the abundance of Meadow Pipits or Red Grouse chicks.     

Unique population dynamics of Japanese field vole: Winter breeding and summer population decline

It is common knowledge that winter temperatures influence the life history of small mammals. Cold temperatures necessitate increased energy requirements for survival, and recent studies indicate that snow cover can have both negative and positive influences. With each new observation, we develop a more comprehensive understanding of the mechanisms that influence small mammal populations. Here we report on our recent study on Japanese field vole Microtus montebelli, which reaches its peak in population during the early spring and its low during the autumn. To understand the population dynamics of these voles, we conducted a capture-mark-recapture survey, then estimated the seasonal abundance, recruit, capture probabilities, and survival probabilities using the Bayesian hierarchical model. We also analyzed the impact of mammalian generalist predator visits on the survival probabilities. Our data indicates that the early spring peak in population is due to intensive winter breeding and the highest survival probabilities during the periods of deep snow cover. When snow cover reaches a certain depth, the circumstances can combine to raise survival probability and favor breeding. During the breeding season in May and June, on the contrary, the survival probability reached its lowest, resulting in a decrease in population despite breeding. The low survival probability between spring and autumn could be attributed to the impact of generalist predators, and low vegetation may have amplified the effect. In summary, the deep snow cover and generalist predators were considered to be the key factors shaping this unique population dynamics in this orchard area.     

Annual cycle in female Three-spined sticklebacks (Gasterosteus aculeatus L.) from an upland and lowland population

The annual cycles in female Three-spined sticklebacks from an upland (275 m) and a lowland (25 m) population were compared. The average length and weight of the lowland females were greater, but in both populations growth was checked in winter and again in the breeding season. Both populations also showed a winter decline in condition followed by a sharp increase in spring associated with the maturation of the ovaries. The hepato-somatic index of the females also increased during the spring, but the dry matter content of the liver declined during the spring and early summer. Lowland females had larger livers than the upland fish. In both populations average gonadosomatic index increased steadily throughout the winter, then abruptly in spring. The lowland population bred from May to early August, but the upland population bred only in May.
The energy content of the carcases of females was lowest in winter and again during the breeding season whereas the ash content showed maxima at these two periods. Lipid and glycogen analyses of the carcase, liver and ovaries also suggested that winter and the breeding season were periods of depletion from the carcase and liver, but not from the ovaries.
The observations indicate that the ovaries are to some extent insulated from fluctuations in resource availability. This supports experimental studies which indicate that egg production in the female stickleback can be subsidised by depletion from the carcase and liver when necessary.     

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.