Multiannual Population Fluctuations Research Articles

Population Fluctuations of the Deer Mouse (Peromyscus maniculatus) in Old-Field and Bunchgrass–Sagebrush Habitats: The Role of Agricultural Setting and Optimum Habitat

In semiarid regions, the deer mouse (Peromyscus maniculatus) is a major small mammal species occupying perennial grassland habitats that include old-fields, native bunchgrass–sagebrush, and some agricultural settings. We investigated population changes in deer mouse populations in perennial grasslands, both natural and old-field, from 1982 to 2003 in southern British Columbia, Canada. Hypotheses (H) predicted that P. maniculatus populations will have (H1) multiannual fluctuations in abundance driven by population increases from extended breeding in summer and winter; (H2) relaxed spring reorganization events in some years leading to higher overall recruitment and survival; and (H3) interspecific competition with montane voles that causes deer mice to be lower in density when voles are higher. P. maniculatus populations in old-field and grass–sagebrush sites had clearly defined periods of high “peak” mean numbers (32–52/ha) and other times of low mean numbers (20–22/ha). Based on mean annual peak density in autumn, deer mouse populations exhibited fluctuations of 3–4 years in both habitats, but this pattern was not always present. The greater numbers of P. maniculatus in high than low years was directly related to population increases from extended breeding seasons and an increased number of lactating females, thereby supporting H1. Spring breeding season declines occurred but were similar or less in high than low years of mean abundance and were relaxed in comparison to forest populations of deer mice in other studies. Thus, H2 was supported for recruitment with high numbers of young-of-the-year breeding and total number of juvenile recruits but for survival was equivocal. Total summer survival was consistently higher in high than low population years but juvenile productivity in all years was poor. Mean abundance of P. maniculatus and M. montanus in old-field sites were highly correlated, and hence H3 was not supported. This latter result is the first, to our knowledge, of P. maniculatus coexisting in a similar pattern of population fluctuations with a Microtus species in a mainland grassland habitat. Higher than average precipitation in the year preceding a peak population of deer mice may have enhanced herbaceous vegetation and contributed to population increases in both habitats. We conclude that the old-field habitat associated with this agricultural setting provides optimum habitat for P. maniculatus and facilitates multiannual population fluctuations in this species.

Numerical response of predators to large variations of grassland vole abundance and long-term community changes.

Voles can reach high densities with multiannual population fluctuations of large amplitude, and they are at the base of predator communities in Northern Eurasia and Northern America. This status places them at the heart of management conflicts wherein crop protection and health concerns are often raised against conservation issues. Here, a 20‐year survey describes the effects of large variations in grassland vole populations on the densities and the daily theoretical food intakes (TFI) of vole predators based on roadside counts. Our results show how the predator community responded to prey variations of large amplitude and how it reorganized with the increase in a dominant predator, here the red fox, which likely negatively impacted hare, European wildcat, and domestic cat populations. This population increase did not lead to an increase in the average number of predators present in the study area, suggesting compensations among resident species due to intraguild predation or competition. Large variations in vole predator number could be clearly attributed to the temporary increase in the populations of mobile birds of prey in response to grassland vole outbreaks. Our study provides empirical support for more timely and better focused actions in wildlife management and vole population control, and it supports an evidence‐based and constructive dialogue about management targets and options between all stakeholders of such socio‐ecosystems.

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.

Population recovery of a common vole population (Microtus arvalis) after population collapse.

Population collapses in small mammals occur naturally after natural disasters and during multi-annual population fluctuations as well as after man-made intervention such as rodent management action. Although there has been extensive previous work on patterns and mechanisms of population fluctuations and cyclicity, little is known about population recovery after collapse. In Europe, the common vole (Microtus arvalis) is the major pest species in agriculture, damaging crops, competing with livestock and potentially posing a health risk to people. In this study, we investigated population recovery, recovery mechanism and recovery time of common vole populations after artificially inducing a collapse through rodenticide application. The rodenticide treatment reduced abundance in spring (by about 90%) but not in summer. Demographic data (age, sex-ratio, breeding activity) suggest that it was mostly immigration and not reproduction that led to population recovery after collapse. The findings indicate that rodenticide treatment should be conducted in spring before the main reproductive season starts. The treatment effect was transient and lasted for about 3months before immigration offset the initial reduction in population abundance. This indicates that immigration patterns should be considered by managing vole populations at an appropriate spatial scale and frequency to prevent rapid repopulation. © 2018 Society of Chemical Industry.

Long-tailed vole (Microtus longicaudus) population outbreaks and refugia after clearcutting of coniferous forests: The search for fluctuations and hotspots

AbSTRACT Some species of Microtus voles exhibit multi-annual population fluctuations with peak numbers every 3–5 years, and these periods may be interspersed with annual fluctuations in abundance. Populations of long-tailed voles (M. longicaudus Merriam) increase during the first 3–4 years after clearcutting of coniferous forests, and it is during this population outbreak that voles may feed on newly planted tree seedlings. It is unclear if M. longicaudus has multi-annual population fluctuations similar to other Microtus species, and we do not know the location of refuge habitats during low years of abundance. We describe changes in abundance of M. longicaudus during the first 5–10 years after clearcut harvesting near Golden, British Columbia, Canada, and evaluated four hypotheses (H) that long-tailed voles will (H1) have peak populations at 3–4 years post-harvest, decline to low numbers, with outbreak populations appearing again on newly clearcut sites; (H2) occur at very low ( Long-tailed vole populations increased in abundance on newly clearcut sites and reached independent peak numbers (62, 96, and 134/ha) at 3–4 years post-harvest in three different areas and time periods, thus supporting H1. Long-tailed voles were consistently at very low numbers in uncut forest, and hence this habitat did not provide a refuge or source area for voles, thereby supporting H2. We had some evidence to support H3 that long-tailed voles seemed to persist at low numbers (

Population fluctuations of moths and small rodents in relation to plant reproduction indices in southern Norway

Trophic interaction hypotheses for multiannual population fluctuations of herbivores include the predation hypothesis, the induction hypothesis and the plant stress hypothesis. Spatial synchrony is best explained by plant stress, such as high reproduction, because weather may synchronize resource allocation in plants over large areas. We used a 29‐yr time series on moth light trapping (6 selected species) and small rodent snap trapping (2 selected species) from southern Norway to test whether herbivore population fluctuations can be related to sexual reproduction of their host plants. The fluctuation pattern of the moths Parashwammerdamia lutarea and Yponomeuta padella, feeding on leaves of rowan (Sorbus aucuparia), could be explained by fluctuations in an annual index of rowanberry production, whereas the fluctuation pattern of Yponomeuta evonymella, feeding on leaves of bird cherry (Prunus padus), could not. The moth Eulithis populata, feeding on bilberry (Vaccinium myrtillus) leaves, fluctuated in synchrony with the bank vole (Myodes clethrionomys), which feeds on bilberry twigs in winter. E. populata and the bank vole also fluctuated in synchrony with a shorter index on bilberry seed crops. Finally, two moths feeding on mosses, Eudonia truncicolella and Catoptria falsella, fluctuated in synchrony with the moss‐feeding wood lemming (Myopus schisticolor). The observed patterns could be caused by a positive effect of the supply of highly nutritious reproductive plant tissue, but the one‐year delayed response by the rodents, which to a large extent feed on the plant species in question during winter, suggests that feeding deterrents are involved.

Strength of asymmetric competition between predators in food webs ruled by fluctuating prey: the case of foxes in tundra

In food webs heavily influenced by multi-annual population fluctuations of key herbivores, predator species may differ in their functional and numerical responses as well as their competitive ability. Focusing on red and arctic fox in tundra with cyclic populations of rodents as key prey, we develop a model to predict how population dynamics of a dominant and versatile predator (red fox) impacted long-term growth rate of a subdominant and less versatile predator (arctic fox). We compare three realistic scenarios of red fox performance: (1) a numerical response scenario where red fox acted as a resident rodent specialist exhibiting population cycles lagging one year after the rodent cycle, (2) an aggregative response scenario where red fox shifted between tundra and a nearby ecosystem (i.e. boreal forest) so as to track rodent peaks in tundra without delay, and (3) a constant subsidy scenario in which the red fox population was stabilized at the same mean density as in the other two scenarios. For all three scenarios it is assumed that the arctic fox responded numerically as a rodent specialist and that the mechanisms of competition is of a interference type for space, in which the arctic fox is excluded from the most resource rich patches in tundra. Arctic fox is impacted most by the constant subsidy scenario and least by the numerical response scenario. The differential effects of the scenarios stemmed from cyclic phase-dependent sensitivity to competition mediated by changes in temporal mean and variance of available prey to the subdominant predator. A general implication from our result is that external resource subsidies (prey or habitats), monopolized by the dominant competitor, can significantly reduce the likelihood for co-existence within the predator guild. In terms of conservation of vulnerable arctic fox populations this means that the likelihood of extinction increases with increasing amount of subsidies (e.g. carcasses of large herbivores or marine resources) in tundra and nearby forest areas, since it will act to both increase and stabilize populations of red fox.

Is the prevalence of Taenia taeniaeformis in Microtus arvalis dependent on population density?

Populations of common voles Microtus arvalis were studied as hosts of the tapeworm Taenia taeniaeformis during a 14-yr survey. They were monitored in spring, summer, and autumn in a pastoral ecosystem in eastern France. A total of 7,574 voles were sampled during 2 multiannual population fluctuations. A third fluctuation was sampled during the increase phase only. Overall prevalence was lowest in summer (0.6%), increased by 3 times in autumn (1.5%) and a further 5 times in spring (7.8%). Analysis of prevalence, based on 7,384 voles, by multiple logistic regression revealed that extrinsic factors such as season and intrinsic factors such as host age and host density have a combined effect. In the longer term, host age and host density were positively associated with prevalence in summer. Host density was strongly associated with autumn prevalence. There was no association between the fluctuation phase and prevalence. The study shows that a long timescale (here a multiannual survey) is necessary to demonstrate the positive effect of host density on the prevalence of this indirectly transmitted parasite. The demonstration of this relationship depends on the rodents being intermediate rather than definitive hosts.

Population Cycles in Voles and Lemmings: Density Dependence and Phase Dependence in a Stochastic World

I review the regular multiannual population fluctuations in voles and lemmings of northern latitudes. Periodically fluctuating small rodent populations all exhibit a clear two-dimensional density-dependent structure. This implies both a direct and a delayed annual density dependence, and suggests that either a predator-prey type of interaction or a specialised plant-herbivore type of interaction (but not both) may be the underlying cause of these multiannual density cycles. Clear-cut experimental testing relating to these propositions is, however, lacking. A two-dimensional annual density-dependent structure is typically non-linear in a way which may be modelled as a threshold type of non-linearity and interpreted as a phase dependence in the density-dependent structure (implying that the density-dependent structure is different in the increase and the decrease phase). Two clear geographic gradients in the annual density-dependent structure are reviewed: the Fennoscandian gradient and the Hokkaidian gradient. The seasonal nature of the annual density-dependent structure is furthermore reviewed: for voles in both Fennoscandia and Hokkaido the direct annual density dependence during the winter (measured per time unit) is concluded to be the strongest. I close with a survey of the main challenges within the field of small rodent cycles' - the greatest of which is suggested to be the integration of demography and population dynamics. I recommend to look at other populations for potentially applicable model systems. I conclude that multiannual population cycles seen in voles and lemmings will continue to be a strong source of conceptual and methodological developments within the field of population ecology.

Optimization of reproductive effort and foraging time in mammals: The influence of resource level and predation risk

The trade-off between fitness benefits from foraging and associated costs in terms of predation risk is analysed by a simple model which takes into account the differential predation risk for reproducing and non-reproducing individuals. The currency that animals are assumed to maximize is their expected absolute fitness (probability of survival plus half of the expected litter size) after a potential reproductive period. Depending on resource levels and predation risk, this maximization can be achieved by (1) opting for individual survival and behaving as a strict time minimizer, (2) by reproducing at the maximal rate and behaving as a strict energy maximizer or (3) by submaximal reproductive effort and a behaviour intermediate between time minimization and energy maximization. Small changes in the availability of food or cover or in the density of predators can shift the optimum from one strategy to another. The shift is particularly abrupt, if predation pressure increases and the availability of resources remains high. This could explain the spatial and temporal variation in the reproductive effort and body weight observed in boreal small mammals with sustained, multiannual population fluctuations.

A 14-Year Study of Blarina brevicauda Populations in East-Central Illinois

Short-tailed shrew, Blarina brevicauda , populations in east-central Illinois displayed annual population cycles within bluegrass ( Poa pratensis ), tallgrass, and alfalfa ( Medicago sativa ) habitats. There was no indication of multiannual population fluctuations in any habitat. Amplitudes of annual fluctuation were relatively consistent within each habitat type. Population density was significantly higher in bluegrass than in the other two habitats, and higher in alfalfa than in tallgrass from February to July. The annual peak in tallgrass occurred 3 months later (October) than in the other two habitats (July). Males were reproductively active January–July and females, March–September. Survival was highest in bluegrass, intermediate in tallgrass, and lowest in alfalfa. January–August precipitation >24% below the mean was followed by lower peaks in B. brevicauda populations in bluegrass and alfalfa; ≥9% above-normal precipitation was followed by higher populations in alfalfa and bluegrass. There was no correlation between precipitation and population density in tallgrass. There was no correlation between summer temperatures and numbers of B. brevicauda .

Concluding Remarks: Trophic Exploitation and Community Structure

All the empirical contributions in this issue seem to agree about the generally exploitative nature of trophic interactions. This, indeed is an explicit premise of Holt's (1987), Hansson's (1987) and Fretwell's (1987) theories and also implicitly assumed in the contribution of Pimm and Kitching (1987). (Pimm's (1982) theory on stability problems of long food chains and food chains with much omnivory is based on exploitation models.) Moreover, exploitative trophic interactions seem to be essential for generating sustained multiannual population fluctuations (Stenseth and Oksanen 1987). Herbivores are indeed selective foragers (Danell et al. 1987, Ericson and Oksanen 1987) but plants seem nevertheless to be vulnerable to their consumers if not protected by predators, and phenol-based inducible defense does not seem to work reliably (Jonasson et al. 1986, Laine and Henttonen 1987, Oksanen et al. 1987). The idea of Pimm (e.g., 1982, see also Pimm and Kitching 1987) that primary productivity is practically always high enough to support three trophic levels is not contradicted by any contribution. Even barren Fennoscandian highlands and genuinely arctic tundras are invaded by predators during lemming peaks (especially by snowy owls and jaegers; see Andersson 1976, Cernjavskij and Tkacev 1982, Pitelka 1973), and one resident and a chiefly terrestrial predator the arctic fox is practically restricted to relatively barren tundra areas. On the other hand, there seems to be profound between-habitat differences in the intensity of predation (Hanski 1987, Henttonen et al. 1987) and herbivory (Oksanen and Ericson 1987). These differences might even explain a large part of the vegetational characteristics of different habitats (Ericson and Oksanen 1987).