Population fluctuations of the wood lemming<Emphasis Type="Italic">Myopus schisticolor</Emphasis> in eastern and western Finland

Olavi Eskelinen, Pertti Sulkava and Risto Sulkava From 1982 to 2003 we studied fluctuations in populations of the wood lemmingMyopus schisticolor (Liljeborg, 1844) in the Heinävesi (eastern Finland) and Keuruu regions (western Finland) by counting field signs and dead animals in standardized field surveys. We compared the population fluctuations of lemmings to those of other voles, owls and small mustelids in these regions. The lemming population in Heinävesi fluctuated regularly in 3-year cycles and in synchrony with the field vole population. Populations of owls also fluctuated in synchrony with wood lemming and field vole populations. In the Keuruu region, oscillations in the wood lemming population were irregular, and neither lemming and vole populations nor lemming and owl populations were correlated. Although direct mechanistic evidence is lacking, specialist predators such as weasels and owls probably cause the cyclicity in the field vole and wood lemming populations in the Heinävesi area. On the other hand, scarcity of high-quality habitats, unfavourable winter weather conditions and generalist predators may prevent the development of cyclicity in the wood lemming population of Keuruu.     

Responses of stoats and least weasels to fluctuating food abundances: is the low phase of the vole cycle due to mustelid predation?

Summary We studied responses of stoats and least weasels to fluctuating vole abundances during seven winters in western Finland. Density indices of mustelids were derived from snow-tracking, diet composition from scat samples, and vole abundances from snap-trapping. Predation rate was estimated by the ratio of voles to mustelids and by the vole kill rate by predators (density of predator x percentage of voles in the diet). We tested the following four predictions of the hypothesis that small mustelids cause the low phase of the microtine cycle. (1) The densities of predators should lag well behind the prey abundances, as time lags tend to have destabilizing effects. The densities of stoats fluctuated in accordance with the vole abundances, whereas the spring densities of least weasels tracked the vole abundances with a half-year lag and the autumn densities with a 1-year lag. (2) Predators should not shift to alternative prey with declining vole densities. The yearly proportion of Microtus voles (the staple prey) in the diet of stoats varied widely (range 16–82%) and was positively correlated with the winter abundance of these voles. In contrast, the same proportion in the food of least weasels was independent of the vole abundance. (3) The ratio of voles to small mustelids should be smallest in poor vole years and largest in good ones. This was also observed. (4) Vole densities from autumn to spring should decrease more in those winters when vole kill rates are high than when they are low. The data on least weasels agreed with this prediction. Our results from least weasels were consistent with the predictions of the hypothesis, but stoats behaved like semi-generalist predators. Accordingly, declines and lows in the microtine cycle may be due to least weasel predation, but other extrinsic factors may also contribute to crashes.     

Habitat use of small mustelids in north Fennoscandian tundra: a test of the hypothesis of patchy exploitation ecosystems

The habitat use of small mustelids in a tundra area in Norwegian Lapland was studied chiefly by means of snow-tracking 1986-89 Stoats showed strong peference to a habitat complex immediately beneath the thrust line of the Scandes, with exceptional abundance of luxuriant habitats, whereas weasel activity was more evenly spread over the lowland tundra Mustelid activity on the high tundra above the thrust line was consistently low Within each subarea. stoat activity was concentrated to the most luxuriant habitats Similar preferences were shown by weasels on the lowland but not in the vicinity of the thurst cliff Daily movements of both species varied from local (c 200 m) to extensive (up to 4 km), no consistent interspecific differences in travel distances could be observed
The results largely conform to the hypothesis of patchy exploitation ecosystems (T Oksanen 1990a), according to which predator activity tends to "spill over' from luxuriant habitats, capable of supporting predator populations, to adjacent barren ones, due to despotic behavior within and between species and due to opportunistic predation by transient predators However, predator activity in barren habitats during the crash winter could not be explained by these mechanisms alone A third mechanism - breakdown of habitat preferences of predators during crash phases of a cyclic prey population - was thus introduced     

Dynamics of voles and small mustelids in the taiga landscape of northern Fennoscandia in relation to habitat quality

In the forests of northern Fennoscandia during the I980's, the dynamics of microtine rodents changed from multiannual high amplitude fluctuations (cycles) to, depending on species, fluctuations with a strong seasonal component or fluctuations with smaller amplitude and lower frequency. Microtine and predator data from the Pallasjarvi area, Finnish Lapland, suggest that this transition took place at different rates in different parts of the taiga landscape. Generally, densities in forest habitats have been primarily seasonal since 198S-86. In mesic spruce taiga and in drier forest habitats microtines had a prolonged peak in 1981-83 and a crash in 1984-83. At the timberline, however, microtine populations dropped from peak to low densities already in 1982-83 but the final crash did not occur until spring 1985. The synchronous decrease in microtines densities in all habitat types in 1984-85 coincided with increase in weasel activity. Activity of other carnivores was consistently high in mesic lowland habitats. The data support following three conjectures. 1) Periodic abundance of least weasels is crucial for sustained vole cycles. 2) Predominance of stoats and other generalist predators lead to less regular fluctuations with a strong seasonal component where density declines occur in autumn and early winter. 3) In barren tundra areas, the vegetation cannot sustain high densities of microtines and. consequently, predation is not a necessary condition for population crashes.     

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.     

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.     

Spatial synchrony in vole population fluctuations – a field experiment

Three mechanisms have been proposed to induce spatial synchrony in fluctuations of small mammal populations: climate‐related environmental effects, predation and dispersal. We conducted a field experiment in western Finland to evaluate the relative roles of these mechanisms in inducing spatial synchrony among cyclic populations of field voles Microtus agrestis. The study was conducted during the increase and peak phases of a vole population cycle on four agricultural field sites situated 1.5–7.0 km apart. Each field contained two 0.5‐ha fenced enclosures and one 1‐ha unfenced control area. One enclosure per field allowed access by small mustelid predators and the other by avian predators; all enclosures prevented the dispersal of voles. The unfenced control areas allowed access by all predators as well as dispersal by voles. Enclosed vole populations were in a treatment‐wise asynchronous phase before the predator access treatments were applied. The growth rates of all enclosed populations were tightly synchronized during the course of the experiment. Conversely, synchrony both among the unfenced populations and between the fenced and unfenced populations was practically non‐existent. During winter, in the increase phase of the cycle, vole populations in all treatments declined to low densities due to a seasonal effect of winter food depletion. During summer, in the peak year of the vole cycle, all populations fluctuated in synchrony. At this time, both small mustelids and birds of prey appeared to be abundant enough to induce synchrony. Dispersal was identified as a potential contributor to synchronization, but the magnitude of its effects could not be reliably discerned. Our results indicate that no single mechanism can account for the observed patterns of spatial synchrony among cyclic northern vole populations. Rather, spatial synchronization is induced by different mechanisms, namely seasonality and predation, acting successively during different seasons and phases of the vole cycle.     

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.     

Foraging and diet of the red fox Vulpes vulpes in relation to variable food resources in Biatowieza National Park, Poland

Feeding ecology of red fox Vulpes vulpes was studied by scat analysis and snow-tracking m primeval temperate forest and adjacent meadows during four years (1985/86-1988/89) Winters varied from mild to unusually severe Main food resources for foxes were rodents of open meadows and river valleys (root vole Microtus oeconomus ). forest rodents (bank vole Clethrionomys glareolus and yellow-necked mouse Apodemus flavicollis ), hare Lepus europaetis and carcasses of wild boar Sus scrofa and red deer Cervus elaphus either killed by wolves and lynx or that had died from inanition Composition of fox diet m four cold seasons (autumn-winter) was compared to the abundance of main food resources Prolonged, sharp decline of Microtus was followed by only a twofold decrease of its share in fox diet Foxes continued to prey on declining Microlus The changes in the proportions of forest rodents and hare in fox diet clearly followed the fluctuations in numbers of these two prey Carcasses were alternative, buffer food to foxes and were taken considerably when Microlus and other prey were in low numbers or poorly accessible The depth of snow was the most important factor restricting foxes access to rodents Snow-tracking revealed that foxes dwelling in the forest widely used adjacent open areas In open meadows foxes mainly hunted for rodents, while in the forest the most significant foraging activity was scavenging Seasonal analysis of fox diet revealed that consumption of Microlus by foxes was stable throughout the year (37-47% of biomass consumed) Bank vole significantly contributed to fox diet in autumn, and hare in summer only Scavenging was most pronounced in winter and spring when carcasses made up 30% of biomass taken     

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.     

Population dynamics of microtine rodents: an experimental test of the predation hypothesis

One of the most popular hypotheses to explain the 3–5 year vole cycle in Fennoscandia is the predation hypothesis, which emphasises the role of specialist predators, especially small mustelids, in driving the microtine rodent cycle. I have tested this hypothesis in a field experiment with a focus on the interaction between the least weasel ( Mustela nivalis nivalis L.) and the field vole ( Microtus agrestis L.). The test involved a perturbation of the natural vole-weasel dynamics by increasing the numbers of predators. In natural cyclic dynamics, the numbers of weasels follow the numbers of voles with a time lag; the delay in the numerical response of the predators essentially leads to the cyclic dynamics. In this experiment, I attempted to eliminate the time lag in predators' numerical response by adding weasels into the system at a point when vole numbers are increasing but weasels are still scarce. The experiment was conducted in three experimental islands (each 5–10 km²) using adjacent comparable islands as controls. Results of the experiment did not provide strong evidence either for or against the hypothesis. Two of three experimental areas did not show a treatment effect, while one area showed an effect in both population dynamics and population structure. Unexpectedly, the previously clearly cyclic dynamics were much less regular in the study areas (and elsewhere in southern Finland) during the period of the experiment.     

Population dynamics of the collared lemming and the tundra vole at Pearce Point,Northwest Territories,Canada

From 1987 to 1989 we monitored population changes during summer of the collared lemming (Dicrostonyx groenlandicus) and the tundra vole (Microtus oeconomus) at Pearce Point, Northwest Territories, Canada (69° 48 N, 122° 40 W). Populations on four study areas did not cycle but remained at low density (<3/ha) each year and continued at low numbers for the following 3 years (Reid et al. 1995). Lemming numbers often declined throghout the summer in spite of continous reproduction, and population recovery occurred overwinter. Heavy predation losses of radio-collared lemmings occurred each summer and this lemming population may be trapped in a predator-pit. Collared lemmings breed in winter and only because of winter population growth do these populations persist. Tundra vole numbers increased rapidly in most summers but usually declined overwinter. Tundra voles do not seem able to sustain winter reproduction in this extreme environment and this prevents them from reaching high density because of the short summer. Population growth in both these rodents could be prevented by poor food or by predation losses, and landscape patchiness may also help to prevent population growth. For lemmings we do not think that a shortage of shelter or intrinsic limitations could be restricting population increase at Pearce Point. This is the first detailed study of a non-cyclic collared lemming population.     

Vole cycles and antipredatory behaviour

During recent years the role of predation as a simple mechanism to produce cyclical population fluctuations in microtine rodent populations has gained stronger empirical and theoretical support. Predation by several generalist species produces non-cyclicity, and predation by resident specialists, such as small mustelids, produces a synchronous cyclic pattern of population fluctuations in several vole species. At the same time, behavioural ecological studies have shown that the same group of specialist predators crucial for cyclicity causes the strongest antipredatory responses in vole behaviour. Recently, breeding suppression in cyclic microtines under risk of mustelid predation has been documented both in the laboratory and in the field. This review links the new population ecological studies and modelling of cyclic microtines and their predators with recent findings on antipredatory adaptations of voles.     

Escape from pupal predation as a potential cause of outbreaks of the winter moth, Operophtera brumata

The winter moth, Operophtera brumata , shows varying population dynamics in different host plant habitats. Populations in Sitka spruce, Picea sitchensis, plantations and in Scottish moorlands have a tendency to outbreak that is not shown by winter moth in lowland oak woods. Since pupal predators have previously been identified as being important for the regulation of winter moth in a lowland oak wood it was hypothesized that invertebrate pupal predators were failing to control winter moth in outbreak populations. This hypothesis was tested by comparing the abundance of invertebrate predators and patterns of spatially density dependent pupal predation across habitats. Several results supported this hypothesis. Carabid predators of winter moth were one or two orders of magnitude more abundant in oak woods than in moorland or spruce habitats. Staphylinid predators were also more abundant in high winter moth density oak woods than in any other habitat. Beetle predation of tagged cocoons in the field was inversely density dependent in Highland moors in experiments in 1999 and 2000, and in Sitka spruce in 1999. However, in opposition to our hypothesis, pupal predation was also inversely density dependent in oak woods in 2000, although this result may be explained by the low range of winter moth densities in the field that year. These results are discussed in relation to the role of natural enemies in regulating winter moth populations and the differences in life-history of the beetle predators in different habitats.     

The significance of meandering channel to habitat diversity and fish assemblage: a case study in the Shibetsu River,northern Japan

This study examined the structure and function of habitats for fish, the contribution to fish populations, and the effects of channel modification on habitats and fish populations in the lowland meandering Shibetsu River, northern Japan. Electrofishing and environmental measurements were conducted in bank areas of habitats constituting natural meandering and modified reaches. All types of habitats in a meandering reach highly contributed to the fish population(s). In particular, the contributions of lateral and wood habitats to fish populations were generally high, despite the low spatial extent of these habitats. The modified reach was simplified and had fewer types of habitats with uniform currents, and there was a low abundance of most fish within these habitats. Abundance of each fish group (taxa) was negatively affected by the changes in the habitats and/or channel shortening (i.e., decrease in the absolute abundance of habitat) due to river modification, which was implemented during 1950–1978. This study suggests that the recovery of all the habitat types is important in meander restoration and that the changes in habitat types and abundance should be examined in monitoring meander restoration and channel shortening.     

Is there direct and delayed density dependent variation in population structure in a temperate European cyclic vole population?

Population structure, in terms of the body mass, condition, sex and reproductive status of individuals, has been found to vary in phase with population density in cyclic populations of microtine rodents. Because sustained population cycles involve delayed density dependent changes in the population growth rate, we would expect at least some life history traits also to depend on past densities. Detailed, long-term studies of changes in vole life history traits are however few, and are largely restricted to northern Europe. In view of the uncertainty as to whether the cyclic microtine populations of western Europe represent the same phenomenon as those of northern Europe, we studied temporal variation in the structure of a clearly cyclic population of the common vole Microtus arvalis Pallas, in the cereal plains of mid-western France. Our data set contains seasonal, individual-level data from long-term, large-scale trapping covering four entire population cycles. We found considerable cyclic variation in population structure in spring (April), but less so in summer (June). In spring of post-peak years, animals were of low body weight and body condition (particularly females), litter sizes were smaller and there was a reduction in the proportion of breeders. All of these could be proximal drivers of increased mortality rates, or decreased birth rates, contributing to the population declines. Few life history traits, however, showed direct density dependent variation, and none of the traits studied here showed delayed density dependence. We have shown declines in the fecundity and body condition of voles from a western European population that coincides with, and may be a proximal cause of, cyclic declines in population density. Closer attention to proximal causes, by which ecological processes drive cycles, could clarify the extent to which microtine cycles across Europe represent a single phenomenon.     

Are silica defences in grasses driving vole population cycles?

Understanding the factors that drive species population dynamics is fundamental to biology. Cyclic populations of microtine rodents have been the most intensively studied to date, yet there remains great uncertainty over the mechanisms determining the dynamics of most of these populations. For one such population, we present preliminary evidence for a novel mechanism by which herbivore-induced reductions in plant quality alter herbivore life-history parameters and subsequent population growth. We tested the effect of high silica levels on the population growth and individual performance of voles (Microtus agrestis) reared on their winter food plant (Deschampsia caespitosa). In sites where the vole population density was high, silica levels in D. caespitosa leaves collected several months later were also high and vole populations subsequently declined; in sites where the vole densities were low, levels of silica were low and population density increased. High silica levels in their food reduced vole body mass by 0.5% a day. We argue that silica-based defences in grasses may play a key role in driving vole population cycles.     

The nature of lemming cycles on Wrangel: an island without small mustelids

Lemming cycles are a key process in the functioning of tundra ecosystems. Although it is agreed that trophic interactions are important in causing the cycles, the actual mechanism is disputed. Some researchers attribute a major role to predation by small mustelids such as stoats and least weasels. Here we present a 40-year time series of lemming dynamics from Wrangel Island and show statistically that lemmings do exhibit population cycles in the absence of small mustelids. The observed density fluctuations differed, however, from those observed elsewhere, with long cycles and possibly higher densities of lemmings during the low phase. These differences in the shape of the population cycles may be related to the unique species assemblage of Wrangel Island, where arctic foxes are the only year-round resident lemming predator, and to the high diversity of landscapes, microclimatic conditions, and plants on the island. Both spectral analysis and wavelet analysis show a change in period length from five?years in the 1970s to nearly eight?years in the 1990s and 2000s. This change in dynamics coincides with reports of dampening or fading out of lemming cycles that have been observed in several regions of the Arctic in recent decades. As in the other cases, the changed lemming dynamics on Wrangel Island may be related to ground icing in winter, which could delay peak years.     

Dynamics and trophic interactions of small rodents: landscape or regional effects on spatial variation?

Geographically varying rodent dynamics may be due to specific landscape effects or to regional variation. Two common vole species (Clethrionomys glareolus and Microtus agrestis), their main predators and their impact on some important food items were monitored in Sweden on forest clearcuts in two different landscape types, situated in two different regions with different climatic conditions. Censuses, with 10-16 clearcuts in each landscape and both landscapes in the two regions, were designed to permit analyses of variance of the effects of landscape composition and region on dynamics and species interactions. Region had a far greater influence than landscape on vole numbers, on the proportions of generalist and specialist predators and on the winter browsing of bark of indigenous and experimental woody plants as well on seed consumption in experimental supplies. The findings indicated an influence of the depth and quality of the snow cover on the predation rates by generalist and specialist predators. However, there were also clear signs of food limitation in the snow-rich areas. Such areas had fewer generalist predators, which probably meant less directly density-dependent predation. Thus, lack of high-quality food may put a brake on population growth in climatically harsh regions, permitting increasing populations of specialist predators such as small mustelids to subsequently over-utilise their main prey and potentially cause prolonged low densities. Snow conditions may affect numbers and interactions both within habitats, landscapes and regions. Thus, to more fully understand rodent dynamics, small-scale movements and interactions of individuals in relation to the main large-scale factor(s) of various regions need to be examined.     

Partial recovery and a new population estimate of rhesus monkey populations in India

The purpose of this field study has been to assess major changes in rhesus monkey populations of north central India over a period of 28 yrs from 1959 to 1986. Population censuses have been done in Aligarh District three times per year, and extensive regional surveys were done in 1959–1960, 1964–1965, 1977–1978, and 1985–1986. Throughout the 1960s and 1970s, rhesus populations in India declined more than 90%, from an estimated 2 million animals in 1960 to approximately 180,000 by 1980. These declines were attributed to increasing agricultural pressures in India, loss of primate habitats, less protection for monkeys, and high levels of trapping. In the 1970s, as India's agricultural production rose and stronger wildlife conservation programs developed, local populations of rhesus began to increase. These increases became more prominent after 1978, when India imposed a ban on export of monkeys. By 1985 a population in Aligarh District had returned to its 1960 level in total population size, although the number of groups remained low. Other local populations showed even more striking growth and greatly exceeded former levels. Some areas of India, however, have shown no improvement in rhesus populations. Overall, extensive field surveys of rural habitats in 1985–1986 showed a 53% recovery in the number of rhesus groups, and a 129% recovery in total rhesus from their low points in 1977–1978. We estimate the rhesus population of India in 1985 in the vicinity of 410,000–460,000 individuals.