Population cycles and outbreaks of small rodents: ten essential questions we still need to solve.

Most small rodent populations in the world have fascinating population dynamics. In the northern hemisphere, voles and lemmings tend to show population cycles with regular fluctuations in numbers. In the southern hemisphere, small rodents tend to have large amplitude outbreaks with less regular intervals. In the light of vast research and debate over almost a century, we here discuss the driving forces of these different rodent population dynamics. We highlight ten questions directly related to the various characteristics of relevant populations and ecosystems that still need to be answered. This overview is not intended as a complete list of questions but rather focuses on the most important issues that are essential for understanding the generality of small rodent population dynamics.

Scavenger community structure along an environmental gradient from boreal forest to alpine tundra in Scandinavia.

Scavengers can have strong impacts on food webs, and awareness of their role in ecosystems has increased during the last decades. In our study, we used baited camera traps to quantify the structure of the winter scavenger community in central Scandinavia across a forest-alpine continuum and assess how climatic conditions affected spatial patterns of species occurrences at baits. Canonical correspondence analysis revealed that the main habitat type (forest or alpine tundra) and snow depth was main determinants of the community structure. According to a joint species distribution model within the HMSC framework, species richness tended to be higher in forest than in alpine tundra habitat, but was only weakly associated with temperature and snow depth. However, we observed stronger and more diverse impacts of these covariates on individual species. Occurrence at baits by habitat generalists (red fox, golden eagle, and common raven) typically increased at low temperatures and high snow depth, probably due to increased energetic demands and lower abundance of natural prey in harsh winter conditions. On the contrary, occurrence at baits by forest specialists (e.g., Eurasian jay) tended to decrease in deep snow, which is possibly a consequence of reduced bait detectability and accessibility. In general, the influence of environmental covariates on species richness and occurrence at baits was lower in alpine tundra than in forests, and habitat generalists dominated the scavenger communities in both forest and alpine tundra. Following forecasted climate change, altered environmental conditions are likely to cause range expansion of boreal species and range contraction of typical alpine species such as the arctic fox. Our results suggest that altered snow conditions will possibly be a main driver of changes in species community structure.

Phase- and season-dependent changes in social behaviour in cyclic vole populations.

BACKGROUND: Social behaviour has been linked to hypotheses explaining multiannual population cycles of small rodents. In this paper we aimed to test empirically that the degree of space sharing among adult breeding female voles is higher during the increase phase than in the crash phase, and that the degree of sociality is positively related to population growth rate as suggested by Lambin and Krebs (Oikos 61:126-132, 1991) and Andreassen et al. (Oikos 122:507-515, 2013). We followed 24 natural bank vole Myodes glareolus populations over an area of 113 km2 by monthly live trapping throughout a complete population cycle of three summers and two winters. RESULTS: Using spatially explicit capture-recapture models, we modelled the overlap in adult female home ranges and total population growth rate per season. We identified an increase phase before and during the peak density observation and a crash phase following the peak. Female home range overlap were seasonal- and phase-dependent, while population growth rate was associated with season and female home range overlap. High female home range overlap in the increase phase corresponded to a high population growth rate. CONCLUSIONS: We suggest that intrinsic social behaviour plays a key role in the increase phase of vole population cycles, as social behaviour leads to an increased growth rate, whereas extrinsic factors (predation and/or food) initiate the crash phase. Our results are consistent with those of other studies in a variety of small rodent species.

Surviving winter: Food, but not habitat structure, prevents crashes in cyclic vole populations.

Vole population cycles are a major force driving boreal ecosystem dynamics in northwestern Eurasia. However, our understanding of the impact of winter on these cycles is increasingly uncertain, especially because climate change is affecting snow predictability, quality, and abundance. We examined the role of winter weather and snow conditions, the lack of suitable habitat structure during freeze-thaw periods, and the lack of sufficient food as potential causes for winter population crashes. We live-trapped bank voles Myodes glareolus on 26 plots (0.36 ha each) at two different elevations (representing different winter conditions) in southeast Norway in the winters 2013/2014 and 2014/2015. We carried out two manipulations: supplementing six plots with food to eliminate food limitation and six plots with straw to improve habitat structure and limit the effect of icing in the subnivean space. In the first winter, all bank voles survived well on all plots, whereas in the second winter voles on almost all plots went extinct except for those receiving supplemental food. Survival was highest on the feeding treatment in both winters, whereas improving habitat structure had no effect. We conclude that food limitation was a key factor in causing winter population crashes.

From individuals to population cycles: the role of extrinsic and intrinsic factors in rodent populations.

Rodent population cycles have fascinated scientists for a long time. Among various hypotheses, an interaction of an extrinsic factor (predation) with intrinsic factors (e.g., sociality and dispersal) was suggested to lead to the generation of population cycles. Here, we tested this hypothesis with an individual-based model fully parameterized with an exceptionally rich empirical database on vole life histories. We employed a full factorial design that included models with the following factors: predation only, predation and sociality, predation and dispersal, and predation and both sociality and dispersal. A comprehensive set of metrics was used to compare results of these four models with the long-term population dynamics of natural vole populations. Only the full model, which included both intrinsic factors and predation, yielded cycle periods, amplitudes, and autumn population sizes closest to those observed in nature. Our approach allows to model, as emergent properties of individual life histories, the sort of nonlinear density- and phase-dependence that is expected to destabilize population dynamics. We suggest that the individual-based approach is useful for addressing the effects of other mechanisms on rodent populations that operate at finer temporal and spatial scales than have been explored with models so far.

Why Do the Boreal Forest Ecosystems of Northwestern Europe Differ from Those of Western North America?

The boreal forest is one of the largest terrestrial biomes on Earth. Conifers normally dominate the tree layer across the biome, but other aspects of ecosystem structure and dynamics vary geographically. The cause of the conspicuous differences in the understory vegetation and the herbivore-predator cycles between northwestern Europe and western North America presents an enigma. Ericaceous dwarf shrubs and 3- to 4-year vole-mustelid cycles characterize the European boreal forests, whereas tall deciduous shrubs and 10-year snowshoe hare-lynx cycles characterize the North American ones. We discuss plausible explanations for this difference and conclude that it is bottom-up: Winter climate is the key determinant of the dominant understory vegetation that then determines the herbivore-predator food-web interactions. The crucial unknown for the twenty-first century is how climate change and increasing instability will affect these forests, both with respect to the dynamics of individual plant and animal species and to their community interactions.

Bears are simply voles writ large: social structure determines the mechanisms of intrinsic population regulation in mammals.

The literature reveals opposing views regarding the importance of intrinsic population regulation in mammals. Different models have been proposed; adding importance to contrasting life histories, body sizes and social interactions. Here we evaluate current theory based on results from two Scandinavian projects studying two ecologically different mammal species with contrasting body sizes and life history traits: the root vole Microtus oeconomus and the brown bear Ursus arctos. We emphasize four inter-linked behavioral aspects-territoriality, dispersal, social inhibition of breeding, and infanticide-that together form a density-dependent syndrome with potentially regulatory effects on population growth. We show that the two species are similar in all four behaviors and thus the overall regulatory syndrome. Females form matrilineal assemblages, female natal dispersal is negatively density dependent and breeding is suppressed in philopatric young females. In both species, male turnover due to extrinsic mortality agents cause infanticide with negative effects on population growth. The sex-biased and density-dependent dispersal patterns promote the formation of matrilineal clusters which, in turn, leads to reproductive suppression with potentially regulatory effects. Hence, we show that intrinsic population regulation interacting with extrinsic mortality agents may occur irrespective of taxon, life history and body size. Our review stresses the significance of a mechanistic approach to understanding population ecology. We also show that experimental model populations are useful to elucidate natural populations of other species with similar social systems. In particular, such experiments should be combined with methodical innovations that may unravel the effects of cryptic intrinsic mechanisms such as infanticide.

Concurrent effects of age class and food distribution on immigration success and population dynamics in a small mammal.

During the settlement stage of dispersal, the outcome of conflicts between residents and immigrants should depend on the social organization of resident populations as well as on individual traits of immigrants, such as their age class, body mass and/or behaviour. We have previously shown that spatial distribution of food influences the social organization of female bank voles (Myodes glareolus). Here, we aimed to determine the relative impact of food distribution and immigrant age class on the success and demographic consequences of female bank vole immigration. We manipulated the spatial distribution of food within populations having either clumped or dispersed food. After a pre-experimental period, we released either adult immigrants or juvenile immigrants, for which we scored sociability and aggressiveness prior to introduction. We found that immigrant females survived less well and moved more between populations than resident females, which suggest settlement costs. However, settled juvenile immigrants had a higher probability to reproduce than field-born juveniles. Food distribution had little effects on the settlement success of immigrant females. Survival and settlement probabilities of immigrants were influenced by adult female density in opposite ways for adult and juvenile immigrants, suggesting a strong adult-adult competition. Moreover, females of higher body mass at release had a lower probability to survive, and the breeding probability of settled immigrants increased with their aggressiveness and decreased with their sociability. Prior to the introduction of immigrants, resident females were more aggregated in the clumped food treatment than in the dispersed food treatment, but immigration reversed this relationship. In addition, differences in growth trajectories were seen during the breeding season, with populations reaching higher densities when adult immigrants were introduced in a plot with dispersed food, or when juvenile immigrants were introduced in a plot with clumped food. These results indicate the relative importance of intrinsic and extrinsic factors on immigration success and demographic consequences of dispersal and are of relevance to conservation actions, such as reinforcement of small populations.

Geo-spatial aspects of acceptance of illegal hunting of large carnivores in Scandinavia.

Human-carnivore conflicts are complex and are influenced by: the spatial distribution of the conflict species; the organisation and intensity of management measures such as zoning; historical experience with wildlife; land use patterns; and local cultural traditions. We have used a geographically stratified sampling of social values and attitudes to provide a novel perspective to the human - wildlife conflict. We have focused on acceptance by and disagreements between residents (measured as Potential Conflict Index; PCI) towards illegal hunting of four species of large carnivores (bear, lynx, wolf, wolverine). The study is based on surveys of residents in every municipality in Sweden and Norway who were asked their opinion on illegal hunting. Our results show how certain social values are associated with acceptance of poaching, and how these values differ geographically independent of carnivore abundance. Our approach differs from traditional survey designs, which are often biased towards urban areas. Although these traditional designs intend to be representative of a region (i.e. a random sample from a country), they tend to receive relatively few respondents from rural areas that experience the majority of conflict with carnivores. Acceptance of poaching differed significantly between Norway (12.7-15.7% of respondents) and Sweden (3.3-4.1% of respondents). We found the highest acceptance of illegal hunting in rural areas with free-ranging sheep and strong hunting traditions. Disagreements between residents (as measured by PCI) were highest in areas with intermediate population density. There was no correlation between carnivore density and either acceptance of illegal hunting or PCI. A strong positive correlation between acceptance of illegal hunting and PCI showed that areas with high acceptance of illegal hunting are areas with high potential conflict between people. Our results show that spatially-stratified surveys are required to reveal the large scale patterns in social dynamics of human-wildlife conflicts.

Local and regional determinants of colonisation-extinction dynamics of a riparian mainland-island root vole metapopulation.

The role of local habitat geometry (habitat area and isolation) in predicting species distribution has become an increasingly more important issue, because habitat loss and fragmentation cause species range contraction and extinction. However, it has also become clear that other factors, in particular regional factors (environmental stochasticity and regional population dynamics), should be taken into account when predicting colonisation and extinction. In a live trapping study of a mainland-island metapopulation of the root vole (Microtus oeconomus) we found extensive occupancy dynamics across 15 riparian islands, but yet an overall balance between colonisation and extinction over 4 years. The 54 live trapping surveys conducted over 13 seasons revealed imperfect detection and proxies of population density had to be included in robust design, multi-season occupancy models to achieve unbiased rate estimates. Island colonisation probability was parsimoniously predicted by the multi-annual density fluctuations of the regional mainland population and local island habitat quality, while extinction probability was predicted by island population density and the level of the recent flooding events (the latter being the main regionalized disturbance regime in the study system). Island size and isolation had no additional predictive power and thus such local geometric habitat characteristics may be overrated as predictors of vole habitat occupancy relative to measures of local habitat quality. Our results suggest also that dynamic features of the larger region and/or the metapopulation as a whole, owing to spatially correlated environmental stochasticity and/or biotic interactions, may rule the colonisation-extinction dynamics of boreal vole metapopulations. Due to high capacities for dispersal and habitat tracking voles originating from large source populations can rapidly colonise remote and small high quality habitat patches and re-establish populations that have gone extinct due to demographic (small population size) and environmental stochasticity (e.g. extreme climate events).

The role of colonization in the dynamics of patchy populations of a cyclic vole species.

The crash phase of vole populations with cyclic dynamics regularly leads to vast areas of uninhabited habitats. Yet although the capacity for cyclic voles to re-colonize such empty space is likely to be large and predicted to have become evolved as a distinct life history trait, the processes of colonization and its effect on the spatio-temporal dynamics have been little studied. Here we report from an experiment with root voles (Microtus oeconomus) specifically targeted at quantifying the process of colonization of empty patches from distant source patches and its resultant effect on local vole deme size variation in a patchy landscape. Three experimental factors: habitat quality, predation risk and inter-patch distance were employed among 24 habitat patches in a 100 × 300-m experimental area. The first-born cohort in the spring efficiently colonized almost all empty patches irrespective of the degree of patch isolation and predation risk, but this was dependent on habitat quality. Just after the initial colonization wave the deme sizes in patches of the same quality were underdispersed relative to Poisson variance, indicating regulated (density-dependent) settlement. Towards the end of the breeding season local demographic processes acted to smooth out the initial post-colonization differences among source and colonization patches, and among patches of initially different quality. However, at this time demographic stochasticity had also given rise to a large (overdispersed) variation in deme sizes that may have contributed to an overshadowing of the effect of other factors. The results of this experiment confirmed our expectation that the space-filling capacity of voles is large. The costs associated with transience appeared to be so low, at least at the spatial scale considered in this experiment, that such costs are not likely to substantially constrain habitat selection and colonization in the increase phase of cyclic patchy populations.

Vole preference of bilberry along gradients of simulated moose density and site productivity.

Browsing by large herbivores might either increase or decrease preference for the plant by other herbivores, depending on the plant response. Using a cafeteria test, we studied the preference by root voles (Microtus oeconomus [Pallas, 1776]) for bilberry (Vaccinium myrtillus L.) previously subjected to 4 levels of simulated moose (Alces alces [Linnaeus, 1758]) density. The different levels of moose density were simulated at population densities relevant for Fennoscandian conditions, in exclosures situated along a site productivity gradient. We expected: (i) voles to prefer bilberry from high productivity sites over low productivity sites; (ii) voles to prefer browsed bilberry, if plants allocate resources to compensatory growth or to avoid browsed bilberry if plants allocate resources to defense; (iii) these effects to increase with increasing simulated moose density; and (iv) the concentration of plant chemicals and the plant morphology to explain vole preference. Specifically, we predicted that voles would prefer: (i) plants with high nitrogen content; (ii) plants with low content of defensive substances; and (iii) tall plants with long shoots. Voles preferred bilberry from the high productivity sites compared to the low productivity sites. We also found an interaction between site productivity and simulated moose density, where voles preferred unbrowsed plants at low productivity sites and intermediate levels of browsing at high productivity sites. There was no effect of plant chemistry or morphology on vole preference. We conclude that moose browsing impacts the food preference of voles. With the current high densities of moose in Fennoscandia, this could potentially influence vole food selection and population dynamics over large geographical areas.

Effects of individual condition and habitat quality on natal dispersal behaviour in a small rodent.

1. Individuals should benefit from settling in high-quality habitats, but dispersers born under favourable conditions have a better physical condition and should therefore be more successful at settling in high-quality habitats. 2. We tested these predictions with root voles (Microtus oeconomus) by a manipulation of individual condition through litter-size enlargement and reduction during lactation combined with a manipulation of habitat quality through degradation of the vegetation cover. We accurately monitored movements of 149 juveniles during a settlement and breeding period of 3 months. 3. The litter size treatment had long-lasting effects on body size, life-history traits and home range size, but did not influence dispersal behaviour. 4. Different stages of dispersal were influenced by habitat quality. In low-quality patches, females dispersed earlier, spent more time prospecting their environment before settling, and settlers had a smaller adult body size than in high-quality patches. Preference and competition for high-quality patches is likely adaptive as it increased fitness both in terms of survival and reproduction. 5. We found no interactive effect of individual condition and habitat quality on natal dispersal and habitat selection. 6. These findings suggest that immediate conditions are more important determinants of dispersal decisions than conditions experienced early in life.

Demographic side effects of selective hunting in ungulates and carnivores.

Selective harvesting regimes are often implemented because age and sex classes contribute differently to population dynamics and hunters show preferences associated with body size and trophy value. We reviewed the literature on how such cropping regimes affect the demography of the remaining population (here termed demographic side effects). First, we examined the implications of removing a large proportion of a specific age or sex class. Such harvesting strategies often bias the population sex ratio toward females and reduce the mean age of males, which may consequently delay birth dates, reduce birth synchrony, delay body mass development, and alter offspring sex ratios. Second, we reviewed the side effects associated with the selective removal of relatively few specific individuals, often large trophy males. Such selective harvesting can destabilize social structures and the dominance hierarchy and may cause loss of social knowledge, sexually selected infanticide, habitat changes among reproductive females, and changes in offspring sex ratio. A common feature of many of the reported mechanisms is that they ultimately depress recruitment and in some extreme cases even cause total reproductive collapse. These effects could act additively and destabilize the dynamics of populations, thus having a stronger effect on population growth rate than first anticipated. Although more experimental than observational studies reported demographic side effects, we argue that this may reflect the quite subtle mechanisms involved, which are unlikely to be detected in observational studies without rigorous monitoring regimes. We call for more detailed studies of hunted populations with marked individuals that address how the expression of these effects varies across mating systems, habitats, and with population density. Theoretical models investigating how strongly these effects influence population growth rates are also required.

Male turnover reduces population growth: an enclosure experiment on voles.

Turnover of individuals is assumed to cause disruptions of social organization, followed by reduced reproduction and survival. We tested how male turnover (removal of resident males and their replacement by unfamiliar males) affected population performance in experimental root vole (Microtus oeconomus) populations. The treatment simulated predation of adult males, with the subsequent replacement by immigrants, and provided insight into the interaction between extrinsic (i.e., predation) and intrinsic (i.e., social organization) factors. We showed that recruitment and female survival dramatically declined and that reproduction commenced slightly later in treatment populations compared with control populations. The treatment nearly halved the population growth rate. We suspect that recruitment failed due to infanticidal immigrating males. Reduced female survival was particularly apparent in treatment populations in which females exhibited a high degree of spatial overlap. Our experimental results show how males may significantly shape population dynamics and suggest how predation and social factors interact mechanistically.

Density-dependent dispersal and spatial population dynamics.

The synchronization of the dynamics of spatially subdivided populations is of both fundamental and applied interest in population biology. Based on theoretical studies, dispersal movements have been inferred to be one of the most general causes of population synchrony, yet no empirical study has mapped distance-dependent estimates of movement rates on the actual pattern of synchrony in species that are known to exhibit population synchrony. Northern vole and lemming species are particularly well-known for their spatially synchronized population dynamics. Here, we use results from an experimental study to demonstrate that tundra vole dispersal movements did not act to synchronize population dynamics in fragmented habitats. In contrast to the constant dispersal rate assumed in earlier theoretical studies, the tundra vole, and many other species, exhibit negative density-dependent dispersal. Simulations of a simple mathematical model, parametrized on the basis of our experimental data, verify the empirical results, namely that the observed negative density-dependent dispersal did not have a significant synchronizing effect.

The return of the giants: ecological effects of an increasing elephant population.

Northern Botswana and adjacent areas, have the world's largest population of African elephant (Loxodonta africana). However, a 100 years ago elephants were rare following excessive hunting. Simultaneously, ungulate populations were severely reduced by decease. The ecological effects of the reduction in large herbivores must have been substantial, but are little known. Today, however, ecosystem changes following the increase in elephant numbers cause considerable concern in Botswana. This was the background for the "BONIC" project, investigating the interactions between the increasing elephant population and other ecosystem components and processes. Results confirm that the ecosystem is changing following the increase in elephant and ungulate populations, and, presumably, developing towards a situation resembling that before the reduction of large herbivores. We see no ecological reasons to artificially change elephant numbers. There are, however, economic and social reasons to control elephants, and their range in northern Botswana may have to be artificially restricted.

Foraging behaviour of the root vole Microtus oeconomus in fragmented habitats.

The effect of habitat fragmentation on spatial foraging behaviour in the root vole Microtus oeconomus was investigated in seven experimental populations. Four of the populations were established in large, continuous blocks (30 × 95 m) of meadow habitat (treatment plots), whereas the three remaining populations had six small rectangular habitat fragments (30 × 7.5 m) with variable inter-fragment distances (control plots). Both the small habitat fragments and the large continuous habitat were embedded in a non-habitat matrix area which was regularly mowed. Half-way through the study period, the continuous habitat in treatment plots was destroyed by mowing to give a configuration identical to the control plots. Dyed bait placed at the edges and in the interior of habitat fragments as well as in the matrix area was used to reveal differential use of these areas for foraging. Animals in the small-fragment plots fed more than expected along the edges, while edges were used according to availability in the large blocks of continuous habitat. In the fragmented plots, the frequency of foraging in the matrix decreased with increasing distance to the fragment border and with increasing inter-fragment distances. Furthermore, the frequency of use of more than one habitat fragment in individual foraging ranges decreased with increasing inter-fragment distances. Reproductively inactive animals of both sexes fed more often along habitat edges than reproductively active animals. Reproductively active females fed exclusively in one habitat fragment, whereas inactive animals and especially reproductively active males frequently included more than one fragment in their foraging ranges. The only effect of habitat destruction was less foraging in the matrix habitat in the post-destruction treatment plots compared to the permanently fragmented control plots. This was probably an effect of different matrix quality. Root voles in these experimental populations forage in edge and matrix habitat with great risk of becoming victims to predation, and the results are interpreted in this context.