Rodent Population Cycles Research Articles

Macroecological patterns of rodent population dynamics shaped by bioclimatic gradients

Long‐term studies of cyclic rodent populations have contributed fundamentally to the development of population ecology. Pioneering rodent studies have shown macroecological patterns of population dynamics in relation to latitude and have inspired similar studies in several other taxa. Nevertheless, such studies have not been able to disentangle the role of different environmental variables in shaping the macroecological patterns. We collected rodent time‐series from 26 locations spanning 10 latitudinal degrees in the tundra biome of Fennoscandia and assessed how population dynamics characteristics of the most prevalent species varied with latitude and environmental variables. While we found no relationship between latitude and population cycle peak interval, other characteristics of population dynamics showed latitudinal patterns. The environmental predictor variables provided insight into causes of these patterns, as 1) increased proportion of optimal habitat in the landscape led to higher density amplitudes in all species and 2) mid‐winter climate variability lowered the amplitude in Norwegian lemmings and grey‐sided voles. These results indicate that biome‐scale climate and landscape change can be expected to have profound impacts on rodent population cycles and that the macro‐ecology of such functionally important tundra ecosystem characteristics is likely to be subjected to transient dynamics.

Host in reserve: The role of common shrews (Sorex araneus) as a supplementary source of tick hosts in small mammal communities influenced by rodent population cycles.

Rodents often act as important hosts for ticks and as pathogen reservoirs. At northern latitudes, rodents often undergo multi‐annual population cycles, and the periodic absence of certain hosts may inhibit the survival and recruitment of ticks. We investigated the potential role of common shrews (Sorex araneus) to serve as a supplementary host source to immature life stages (larvae and nymphs) of a generalist tick Ixodes ricinus and a small mammal specialist tick I. trianguliceps, during decreasing abundances of bank voles (Myodes glareolus). We used generalized mixed models to test whether ticks would have a propensity to parasitize a certain host species dependent on host population size and host population composition across two high‐latitude gradients in southern Norway, by comparing tick burdens on trapped animals. Host population size was defined as the total number of captured animals and host population composition as the proportion of voles to shrews. We found that a larger proportion of voles in the host population favored the parasitism of voles by I. ricinus larvae (estimate = −1.923, p = .039) but not by nymphs (estimate = −0.307, p = .772). I. trianguliceps larvae did not show a lower propensity to parasitize voles, regardless of host population composition (estimate = 0.875, p = .180), while nymphs parasitized shrews significantly more as vole abundance increased (estimate = 2.106, p = .002). These results indicate that common shrews may have the potential to act as a replacement host during periods of low rodent availability, but long‐term observations encompassing complete rodent cycles may determine whether shrews are able to maintain tick range expansion despite low rodent availability.

A nomadic avian predator displays flexibility in prey choice during episodic outbreaks of rodents in arid Australia.

In environments driven by unpredictable resource pulses, populations of many consumer species experience dramatic fluctuations in abundance and spatial extent. Predator-prey relationships in these acyclic systems are poorly understood in particular with respect to the level of prey specialisation shown by nomadic predators. To understand the dynamics of such a system I examined the response to rodent outbreaks by the letter-winged kite (Elanus scriptus) in the Simpson Desert, Australia; a region that experiences major pulses in primary productivity, driven by unpredictable rainfall events. The kite feeds on small mammals and is the only night-hunting species in the Accipitridae. Letter-winged kites irrupted in the area on only three occasions during 20years of sampling (1999-2019) and remained for a maximum of 20months. Each period of kite occupation occurred only during the increase and/or peak phase of rodent population cycles (which occurred three times during the study). During each period kite diet was dominated by small (10-50g body mass) quadrupedal rodents (Pseudomys australis, P. hermannsburgensis, Mus musculus). Abundance of these species varied across the three outbreaks and kites typically captured them in proportion to availability. The large body mass (134g) long-haired rat (Rattus villosissimus) was abundant during one outbreak but was infrequently consumed. The bipedal spinifex hopping-mouse (Notomys alexis) was within the kites' favoured prey size range (35g) but was consistently avoided. The flexibility in prey selection by letter-winged kites appears to be an important adaptation for survival and reproduction by species exploiting acyclic rodent outbreaks.

Spatiotemporal patterns of red fox scavenging in forest and tundra: the influence of prey fluctuations and winter conditions

Concern has been raised regarding red fox (Vulpes Vulpes) population increase and range expansion into alpine tundra, directly and indirectly enhanced by human activities, including carrion supply, and its negative impact on native fauna. In this study, we used cameras on bait stations and hunting remains to investigate how spatiotemporal patterns of red fox scavenging were influenced by abundance and accessibility of live prey, i.e., small rodent population cycles, snow depth, and primary productivity. We found contrasting patterns of scavenging between habitats during winter. In alpine areas, use of baits was highest post rodent peaks and when snow depth was low. This probably reflected relatively higher red fox abundance due to increased reproduction or migration of individuals from neighboring areas, possibly also enhanced by a diet shift. Contrastingly, red fox use of baits in the forest was highest during rodent low phase, and when snow was deep, indicating a higher dependency of carrion under these conditions. Scavenging patterns by red fox on the pulsed but predictable food resource from hunting remains in the autumn revealed no patterns throughout the rodent cycle. In this study, we showed that small rodent dynamics influenced red fox scavenging, at least in winter, but with contrasting patterns depending on environmental conditions. In marginal alpine areas, a numerical response to higher availability of rodents possible lead to the increase in bait visitation the proceeding winter, while in more productive forest areas, low availability of rodents induced a functional diet shift towards scavenging.

Host-microbiota interaction helps to explain the bottom-up effects of climate change on a small rodent species

The population cycles of small rodents have puzzled biologists for centuries. There is a growing recognition of the cascading effects of climate change on the population dynamics of rodents. However, the ultimate cause for the bottom-up effects of precipitation is poorly understood, from a microbial perspective. Here, we conducted a precipitation manipulation experiment in the field, and three feeding trials with controlled diets in the laboratory. We found precipitation supplementation facilitated the recovery of a perennial rhizomatous grass (Leymus chinensis) species, which altered the diet composition and increase the intake of fructose and fructooligosaccharides for Brandt’s vole. Lab results showed that this nutrient shift was accompanied by the modulation of gut microbiota composition and functional pathways (especially for the degradation or biosynthesis of L-histidine). Particularly, the relative abundance of Eubacterium hallii was consistently increased after feeding voles with more L. chinensis, fructose or fructooligosaccharide. These modulations ultimately increased the production of short chain fatty acids (SCFAs) and boosted the growth of vole. This study provides evidence that the precipitation pulses cascades through the plant community to affect rodent gut microbiome. Our results highlight the importance of considering host-microbiota interaction when investigating rodent population responses to climate change.

Nest association between two predators as a behavioral response to the low density of rodents

AbstractMany birds nest in association with aggressive birds of other species to benefit from their protection against predators. We hypothesized that the protective effect also could extend to foraging resources, whereby the resultant resource-enriched habitats near a nest of aggressive raptors could be an alternative cause of associations between nesting bird species with non-overlapping foraging niches. In the Arctic, the Rough-legged Hawk (Buteo lagopus) and the Peregrine Falcon (Falco peregrinus) are 2 raptor species with non-overlapping food resources that have been reported to nest sometimes in close proximity. Since nesting Peregrine Falcons are very aggressive, they may protect the small rodent prey near their nests from predation, and Rough-legged Hawks could use these hot spots as a nesting territory. In 2 regions in low Arctic Russia we found that (1) the nesting territories of Peregrine Falcons were indeed enriched with small rodents as compared to control areas, (2) the probability of nest association between the 2 raptors increased when rodent abundance was generally low in the region where hawks did not use alternative prey, and (3) hawk reproductive success increased when nesting close to Peregrine Falcons. These results suggest that implications of aggressive nest site defense in birds in certain cases may involve more mechanisms than previously explored. A key ecological process in tundra, rodent population cycles, may explain the occurrence and adaptive significance of a specific behavior pattern, the nesting association between 2 raptor species.

Numerical response of a mammalian specialist predator to multiple prey dynamics in Mediterranean farmlands.

The study of rodent population cycles has greatly contributed, both theoretically and empirically, to our understanding of the circumstances under which predator-prey interactions destabilize populations. According to the specialist predator hypothesis, reciprocal interactions between voles and small predators that specialize on voles, such as weasels, can cause multiannual cycles. A fundamental feature of classical weasel-vole models is a long time-lag in the numerical response of the predator to variations in prey abundance: weasel abundance increases with that of voles and peaks approximately 1 yr later. We investigated the numerical response of the common weasel (Mustela nivalis) to fluctuating abundances of common voles (Microtus arvalis) in recently colonized agrosteppes of Castilla-y-Léon, northwestern Spain, at the southern limit of the species' range. Populations of both weasels and voles exhibited multiannual cycles with a 3-yr period. Weasels responded quickly and numerically to changes in common-vole abundance, with a time lag between prey and weasel abundance that did not exceed 4months and occurred during the breeding season, reflecting the quick conversion of prey into predator offspring and/or immigration to sites with high vole populations. We found no evidence of a sustained, high weasel abundance following vole abundance peaks. Weasel population growth rates showed spatial synchrony across study sites approximately 60km apart. Weasel dynamics were more synchronized with that of common voles than with other prey species (mice or shrews). However, asynchrony within, as well as among sites, in the abundance of voles and alternative prey suggests that weasel mobility could allow them to avoid starvation during low-vole phases, precluding the emergence of prolonged time lag in the numerical response to voles. Our observations are inconsistent with the specialist predator hypothesis as currently formulated, and suggest that weasels might follow rather than cause the vole cycles in northwestern Spain. The reliance of a specialized predator on a functional group of prey such as small rodents does not necessarily lead to a long delay in the numericalresponse by the predator, depending on the spatial and interspecific synchrony in prey dynamics.

Population cycles in voles and lemmings: state of the science and future directions

AbstractDespite nearly a century of research, the causes of population cycles in Arvicoline rodents (voles and lemmings) in northern latitudes are not yet fully understood. Theory tells us that delayed density‐dependent feedback mechanisms are essential for rodent population cycles, suggesting vegetation–rodent, rodent–parasite or rodent–predator interactions as the most likely drivers of population cycles.However, food provisioning, carried out either indirectly through fertilisation treatments of the habitat or directly through food supplementation, has failed to alter population cycles substantially, suggesting that variation in food supply by itself is not necessary or sufficient to cause cyclic fluctuations in abundance.Predator exclusion experiments conducted in Fennoscandia have succeeded in slowing population crashes and increasing autumn densities, implicating predation as the most likely cause of rodent cycles in this region. However, experimental removal of specialist predators in northern England had no discernible effect on a cyclic vole population, casting doubt on the notion that predation is a necessary explanation of rodent population cycles.Population cycle research has contributed substantially to our current understanding of the dynamics, regulation and persistence of biological populations, but we do not yet know with certainty what factors or processes cause multiannual population fluctuations or if population cycles are driven by the same mechanisms everywhere. Recent theoretical and empirical studies suggest that extrinsic factors (primarily food supply and predator abundance) may interact with population intrinsic processes (e.g. dispersal, social behaviour, stress response) to cause multiannual population fluctuations and to explain biological attributes of rodent population cycles.Solving the enigma of population cycles may necessitate identifying factors and processes that cause phase‐specific demographic changes and performing conclusive experiments to ascertain the mechanisms that generate multiannual density fluctuations.

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

BackgroundSocial 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.ResultsUsing 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.ConclusionsWe 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.

Voles and climate in Norway: Is the abundance of herbivorous species inversely related to summer temperature?

For several mammalian species, both population levels and distribution ranges are predicted to change due to changing habitat conditions caused by climate change. A general decrease in the amplitude of small rodent population cycles in northern Europe since the late 1980s has commonly been attributed to a lack of permanent snow cover during winter, or to unfavourable snow conditions. An alternative explanation is that increasing summer temperatures and an extended growing season are unfavourable for herbivorous rodents, by reducing the forage quality. If so, the negative effect should be stronger for the strictly herbivorous Microtus voles than for the herbivorous-granivorous Myodes voles. In a previous study small rodents were snap trapped in 22 regions in Norway during 1971–1979. We found that the trapping index of Microtus voles, but not Myodes voles, in this study was negatively related to summer temperatures. Both in this study and in a snap trapping study from 1994 to 2015, conducted in 13 study areas in Norway, the proportion of Microtus voles among voles captured was negatively related to summer temperatures. Summer temperature was a better predictor than snow depth, but both variables contributed significantly in multiple regression models. We conclude that summer temperature is likely to be a more important factor than snow cover for the population dynamics of herbivorous voles in northern Europe.

Transferability of biotic interactions: Temporal consistency of arctic plant-rodent relationships is poor.

Variability in biotic interaction strength is an integral part of food web functioning. However, the consequences of the spatial and temporal variability of biotic interactions are poorly known, in particular for predicting species abundance and distribution. The amplitude of rodent population cycles (i.e., peak‐phase abundances) has been hypothesized to be determined by vegetation properties in tundra ecosystems. We assessed the spatial and temporal predictability of food and shelter plants effects on peak‐phase small rodent abundance during two consecutive rodent population peaks. Rodent abundance was related to both food and shelter biomass during the first peak, and spatial transferability was mostly good. Yet, the temporal transferability of our models to the next population peak was poorer. Plant–rodent interactions are thus temporally variable and likely more complex than simple one‐directional (bottom‐up) relationships or variably overruled by other biotic interactions and abiotic factors. We propose that parametrizing a more complete set of functional links within food webs across abiotic and biotic contexts would improve transferability of biotic interaction models. Such attempts are currently constrained by the lack of data with replicated estimates of key players in food webs. Enhanced collaboration between researchers whose main research interests lay in different parts of the food web could ameliorate this.

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.

Indirect food web interactions affect predation of Tengmalm's Owls Aegolius funereus nests by Pine Martens Martes martes according to the alternative prey hypothesis

Although population cycles of rodents are geographically widespread and occur in a number of rodent species, higher‐order food web interactions mediated by predator–rodent dynamics have primarily been described from boreal and arctic biomes. During periods of low rodent abundance, predators may switch to alternative prey, which may affect other predators directly or indirectly. Using a long‐term dataset, we assessed the frequency of Pine Marten Martes martes predation on the nests of Tengmalm's Owl Aegolius funereus during periods of fluctuating rodent abundance in Central Europe. The number of nests predated by Pine Martens was positively correlated with the annual number of nests available. The probability of predation by Pine Martens on Tengmalm's Owl nests decreased with increasing spring abundance index of Apodemus mice, but was not related to the abundance index of Myodes and Microtus voles, pooled rodent abundance or age of the nestbox. Additionally, we found no relationship between the breeding frequency (i.e. the number of nesting attempts per nestboxes available) and an abundance index of Microtus and Myodes voles, Apodemus mice or overall rodent abundance. Our results demonstrate, for the first time in a temperate area, that during periods of low Apodemus mouse abundance, the switching response of an opportunistic mammalian predator can lead to indirect food web interactions through an increase in nest predation on a sympatric avian predator.

Plant–herbivore interactions: silicon concentration in tussock sedges and population dynamics of root voles

Summary It has been hypothesized that the induction of silicon (Si)‐based plant defence in response to herbivore damage may engender rodent population cycles. Many studies have also considered accumulation of Si as a process controlled by geo‐hydrological factors. To test these ideas, we investigated the relationship between concentration of Si in fibrous tussock sedge (Carex appropinquata) and the population density of a major sedge consumer, the root vole (Microtus oeconomus), in field enclosures in natural habitat under a variety of natural water regimes and weather conditions. We found that a high density of voles at the end of summer resulted in the immediate accumulation of Si by rhizomes, followed by accumulation of Si in leaves with a 1‐year lag time. The level of river flooding in the same year had an additional impact on Si concentration in rhizomes but did not affect silicification of leaves. Overwinter changes in concentration of Si in sedges were influenced by fluctuations in ambient temperature and the depth of snow cover (multiple freeze–thaw cycles), thus affecting the quality of winter food available for voles. Smaller voles had lower mortality during early winter than large voles, which seemed to be connected with changes in the quality of the autumn rather than the winter food base. Winter survival of voles was not associated with Si concentration in their faeces, however. Our results suggest that changes in Si concentration in fibrous tussock sedge can be induced by changes in vole population density and are also additionally affected by the amount of flooding and weather conditions.

Effect of the abrasive properties of sedges on the intestinal absorptive surface and resting metabolic rate of root voles.

Recent studies on grasses and sedges suggest that the induction of a mechanism reducing digestibility of plant tissues in response to herbivore damage may drive rodent population cycles. This defence mechanism seems to rely on the abrasive properties of ingested plants. However, the underlying mechanism has not been demonstrated in small wild herbivores. Therefore, we carried out an experiment in which we determined the joint effect of abrasive sedge components on the histological structure of small intestine as well as resting metabolic rate (RMR) of the root vole (Microtus oeconomus). Histological examination revealed that voles fed with a sedge-dominated diet had shorter villi composed from narrower enterocytes in duodenum, jejunum and ileum. Reduction in the height of villi decreased along the small intestine. Activity of the mucus secretion increased along the small intestine and was significantly higher in the ileum. The intestinal abrasion exceeded the compensatory capabilities of voles, which responded to a sedge-dominated diet by a reduction of body mass and a concomitant decrease in whole body RMR. These results explain the inverse association between body mass and the probability of winter survival observed in voles inhabiting homogenous sedge wetlands.

Indirect food web interactions mediated by predator–rodent dynamics: relative roles of lemmings and voles

Production cycles in birds are proposed as prime cases of indirect interactions in food webs. They are thought to be driven by predators switching from rodents to bird nests in the crash phase of rodent population cycles. Although rodent cycles are geographically widespread and found in different rodent taxa, bird production cycles appear to be most profound in the high Arctic where lemmings dominate. We hypothesized that this may be due to arctic lemmings inducing stronger predator responses than boreal voles. We tested this hypothesis by estimating predation rates in dummy bird nests during a rodent cycle in low-Arctic tundra. Here, the rodent community consists of a spatially variable mix of one lemming (Lemmus lemmus) and two vole species (Myodes rufocanus and Microtus oeconomus) with similar abundances. In consistence with our hypothesis, lemming peak abundances predicted well crash-phase nest predation rates, whereas the vole abundances had no predictive ability. Corvids were found to be the most important nest predators. Lemmings appear to be accessible to the whole predator community which makes them particularly powerful drivers of food web dynamics.

Mast Pulses Shape Trophic Interactions between Fluctuating Rodent Populations in a Primeval Forest

How different functional responses of consumers exploiting pulsed resources affect community dynamics is an ongoing question in ecology. Tree masting is a common resource pulse in terrestrial ecosystems that can drive rodent population cycles. Using stable isotope (δ13C, δ15N) analyses, we investigated the dietary response of two fluctuating rodent species, the yellow-necked mouse Apodemus flavicollis and the bank vole Myodes glareolus, to mast events in Białowieża Forest (NE Poland). Rodent hair samples were obtained non-invasively from faeces of their predators for an 11-year period that encompassed two mast events. Spectacular seed crops of deciduous trees, namely oak Quercus robur and hornbeam Carpinus betulus, occur after several intermediate years of moderate seed production, with a post-mast year characterised by a nil crop. While a Bayesian isotopic (SIAR) mixing model showed a variety of potential vegetation inputs to rodent diets, the isotopic niche of the yellow-necked mouse was strongly associated with mast of deciduous trees (>80% of diet), showing no variation among years of different seed crop. However, bank voles showed a strong functional response; in mast years the vole shifted its diet from herbs in deciduous forest (∼66% of diet) to mast (∼74%). Only in mast years did the isotopic niche of both rodent species overlap. Previous research showed that bank voles, subordinate and more generalist than mice, showed higher fluctuations in numbers in response to masting. This study provides unique data on the functional response of key pulse consumers in forest food webs, and contributes to our understanding of rodent population fluctuations and the mechanisms governing pulse–consumer interactions.

Linking climate change to lemming cycles

The population cycles of rodents at northern latitudes have puzzled people for centuries, and their impact is manifest throughout the alpine ecosystem. Climate change is known to be able to drive animal population dynamics between stable and cyclic phases, and has been suggested to cause the recent changes in cyclic dynamics of rodents and their predators. But although predator-rodent interactions are commonly argued to be the cause of the Fennoscandian rodent cycles, the role of the environment in the modulation of such dynamics is often poorly understood in natural systems. Hence, quantitative links between climate-driven processes and rodent dynamics have so far been lacking. Here we show that winter weather and snow conditions, together with density dependence in the net population growth rate, account for the observed population dynamics of the rodent community dominated by lemmings (Lemmus lemmus) in an alpine Norwegian core habitat between 1970 and 1997, and predict the observed absence of rodent peak years after 1994. These local rodent dynamics are coherent with alpine bird dynamics both locally and over all of southern Norway, consistent with the influence of large-scale fluctuations in winter conditions. The relationship between commonly available meteorological data and snow conditions indicates that changes in temperature and humidity, and thus conditions in the subnivean space, seem to markedly affect the dynamics of alpine rodents and their linked groups. The pattern of less regular rodent peaks, and corresponding changes in the overall dynamics of the alpine ecosystem, thus seems likely to prevail over a growing area under projected climate change.

Noise with memory as a model of lemming cycles

Population cycles in small rodents of the north are modeled by noise with memory. Multiannual lemming density fluctuations are presented as a pulse sequence. These pulses correspond to the peaks of lemming density. The memory is presented as some delay time after each pulse. During this time the next pulse is forbidden. Parameter of periodicity, average period, correlation function and parameter of synchronization are calculated for different places of North America. Examples of equations modeling population dynamics of lemmings (or their predators) are considered. The model of connected oscillators gives the qualitative explanation of synchronization effects and relation between synchronization and periodicity. These results have implication for the testing of hypotheses regarding lemming cycles.

Predation on native birds in New Zealand beech forests: the role of functional relationships between Stoats Mustela erminea and rodents

In the Holarctic, predation by mustelids on birds is often linked to population cycles of rodents (especially voles and lemmings) because birds may be buffered against mustelid predation at high rodent densities. By contrast, interguild relationships between introduced mustelids and rodents can have very different consequences for native birds in ecosystems where mustelids have been introduced. Here, we consider the interactions between Stoats Mustela erminea, feral House Mice Mus musculus and native birds in New Zealand beech Nothofagus spp. forests. We conclude that buffering to protect birds from Stoat predation normally fails in these systems, because peak populations of mice in these forests are low by Holarctic standards, and mice usually do not become sufficiently abundant to distract increased numbers of Stoats from preying on birds. However, temporary buffering is possible during rare episodes of extreme mouse abundance.