Vole population cycles in northern and southern Europe: is there a need for different explanations for single pattern?

1. Students of population cycles in small rodents in Fennoscandia have accumulated support for the predation hypothesis, which states that the gradient in cycle length and amplitude running from southern to northern Fennoscandia reflects the relative influence of specialist and generalist predators on vole dynamics, itself modulated by the presence of snow cover. The hypothesized role of snow cover is to isolate linked specialist predators, primarily the least weasel, Mustela n. nivalis L. and their prey, primarily field voles Microtus agrestis L., from the stabilizing influence of generalist predators. 2. The predation hypothesis does not readily account for the high amplitude and regular 3-year cycles of common voles documented in agricultural areas of western, central and eastern Europe. Such cycles are rarely mentioned in the literature pertaining to Fennoscandian cycles. 3. We consider new data on population cycles and demographic patterns of common voles Microtus arvalis Pallas in south-west France. We show that the patterns are wholly consistent with five of six patterns that characterize rodent cycles in Fennoscandia and that are satisfactorily explained by the predation hypothesis. They include the: (a) existence of cycle; (b) the occurrence of long-term changes in relative abundance and type of dynamics; (c) geographical synchrony over large areas; (d) interspecific synchrony; and (e) voles are large in the increase and peak phase and small in decline and low phase, namely. There is a striking similarity between the patterns shown by common vole populations in south-west France and those from Fennoscandian cyclic rodent populations, although the former are not consistent with a geographical extension of the latitudinal gradient south of Fennoscandia. 4. It is possible that the dominant interaction leading to multiannual rodent oscillations is different in different regions. We argue, however, that advocates of the predation hypothesis should embrace the challenge of developing a widely applicable explanation to population cycles, including justifying any limits to its applicability on ecological and not geographical grounds.     

Gradients in density variations of small rodents: the importance of latitude and snow cover

Summary Microtine rodents are known to show extreme population variations (cycles) but non-cyclic populations have also been recognized during recent years. The cyclic populations have been widely thought to be regulated by intrinsic mechanisms. However, such predictions for cyclic populations are usually not applicable to non-cyclic ones and extrinsic factors may have to be included in any explanation.A hypothesis that the degree of fluctuations in small rodent numbers is related to the sustainable number of generalist predators was tested on mainly literature data by computing indices of cyclicity for local populations. These indices were related to latitude and snow cover (two measures) as these variables will affect the amount of alternative prey available for these generalists. Within Fennoscandia such indices for Clethrionomys glareolus and Microtus agrestis were clearly positively related to latitude and snow cover. The fraction of populations with summer declines in numbers, characterizing highly cyclic populations, increased in the same way. Cyclicity indices in Great Britain were similar to those in southern Fennoscandia, both areas being poor in snow, but were higher at the same latitudes in eastern Europe with more snow. Indices of density variations were generally low in North American Clethrionomys species and very variable in Microtus species.The gradients observed and differences between continents are interpreted as due to microtine-vegetation interactions in northern European areas poor in generalist predators but with important small mustelid predation, and to similar snowshoe hare-vegetation interactions in mainly Canada-Alaska, where small rodents may serve as alternative prey for numerically fluctuating hare predators, at least in the forests. Western European microtine populations, and probably many others, seem to be regulated by generalist predators.     

Dynamic effects of predators on cyclic voles: field experimentation and model extrapolation

Mechanisms generating the well-known 3-5 year cyclic fluctuations in densities of northern small rodents (voles and lemmings) have remained an ecological puzzle for decades. The hypothesis that these fluctuations are caused by delayed density-dependent impacts of predators was tested by replicated field experimentation in western Finland. We reduced densities of all main mammalian and avian predators through a 3 year vole cycle and compared vole abundances between four reduction and four control areas (each 2.5-3 km(2)). The reduction of predator densities increased the autumn density of voles fourfold in the low phase, accelerated the increase twofold, increased the autumn density of voles twofold in the peak phase, and retarded the initiation of decline of the vole cycle. Extrapolating these experimental results to their expected long-term dynamic effects through a demographic model produces changes from regular multiannual cycles to annual fluctuations with declining densities of specialist predators. This supports the findings of the field experiment and is in agreement with the predation hypothesis. We conclude that predators may indeed generate the cyclic population fluctuations of voles observed in northern Europe.     

Specialist and generalist natural enemies as an explanation for geographical gradients in population cycles of northern herbivores

Within Fennoscandia, two well-studied groups of herbivores exhibit clear geographical gradients in their population dynamics. Populations of a forest lepidopteran ( Epirrita autumnata , the autumnal moth) and voles of the genera Microtus and Clethrionomys show pronounced multi-annual cycles in the north but become more stable towards the south. Here we review empirical and theoretical studies on these species, mainly regarding the biological mechanisms that are assumed to generate the pattern of population dynamics in both systems. We conclude that the specialist/generalist predation hypothesis offers a common explanation for the population cycles and their geographical gradients irrespective of whether a herbivorous insect or small mammals are concerned. According to this hypothesis, originally developed for the Fennoscandian voles, but now applied also to E. autumnata , population cycles are generated by specialist natural enemies (predators for the voles and parasitoids for E. autumnata ). Furthermore, the dynamic shift from cycles to stability is assumed to be caused by an increase in the density and diversity of generalist natural enemies from north to south in Fennoscandia.     

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

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Numerical and dietary responses of a predator community in a temperate zone of Europe

The generalist predation hypothesis predicts that the functional responses of generalist predator species should be quicker than those of specialist predators and have a regulating effect on vole populations. New interpretations of their role in temperate ecosystems have, however, reactivated a debate suggesting generalist predators may have a destabilizing effect under certain conditions (e.g. landscape homogeneity, low prey diversity, temporary dominance of 1 prey species associated with a high degree of dietary specialization). We studied a rich predator community dominated by generalist carnivores ( Martes spp., Vulpes vulpes, Felis catus ) over a 6 yr period in farmland and woodland in France. The most frequent prey were small rodents (mostly Microtus arvalis , a grassland species, and Apodemus spp., a woodland species). Alternative prey were diverse and dominated by lagomorphs ( Oryctolagus cuniculus, Lepus europeus ). We detected a numerical response among specialist carnivores but not among generalist predators. The dietary responses of generalist predators were fairly complex and most often dependent on variation in density of at least 1 prey species. These results support the generalist predation hypothesis. We document a switch to alternative prey, an increase of diet diversity, and a decrease of diet overlap between small and medium-sized generalists during the low density phase of M. arvalis . In this ecosystem, the high density phases of small mammal species are synchronous and cause a temporary specializing of several generalist predator species. This rapid functional response may indicate the predominant role of generalists in low amplitude population cycles of voles observed in some temperate areas.     

Contrasting alternative hypotheses about rodent cycles by translating them into parameterized models

Ecologists working on population cycles of arvicoline (microtine) rodents consider three ecological mechanisms as the most likely explanations of this long-standing puzzle in population ecology: maternal effects, interaction with specialist predators, and interaction with the food supply. Each of these hypotheses has now been translated into parameterized models, and has been shown to be capable of generating second-order oscillations (that is, population cycles driven by delayed density dependence). This development places us in a unique situation for population ecology. We can now practice "strong inference" by explicitly and quantitatively comparing the predictions of the three rival hypotheses with data. In this review, we contrast the ability of each hypothesis to explain various empirically observed features of rodent cycles, with a particular emphasis on the well-studied case of Microtus agrestis and other small rodents in Fennoscandia (Finland, Sweden and Norway). Our conclusion is that the current evidence best supports the predation hypothesis.     

Gradients in population fluctuations of Tengmalm's owl Aegolius funereus in Europe

Summary I studied the importance of geographical location, snow cover and food to the fluctuations in 30 breeding populations of Tengmalm's owl (Aegolius funereu) in Europe. Cyclicity indices were positively related both to latitude and longitude, but within Fennoscandia they were better correlated with snow cover. Population fluctuations increased northward, while food niche breadth and degree of site tenacity decreased northwards.Microtine fluctuations become more pronounced northwards and are more synchronized, while number of alternative prey increases southwards. These factors promote instability in North European and stability in central European owl populations. Furthermore, snow conditions were more important within Fennoscandia, since this small owl cannot hunt voles protected by deep snow. Environmental predictability and diversity of available food for Tengmalm's owl increase southwards in Europe. Thus, the owl is a resident generalist predator of small mammals and birds in central Europe and adopts a partial migration strategy (males being resident and females nomadic) in South and West Finland, changing its habits to nomadic microtine specialist in areas with pronounced vole cycles (in northern Fennoscandia). These changes fit well with the recent suggestion that gradients in density variations of small rodents are related to sustainable numbers of generalist predators.     

An ecological paradox: More woodland predators and less artificial nest predation in landscapes colonized by noisy miners

Many passerine bird populations, particularly those that have open‐cup nests, are in decline in agricultural landscapes. Current theory suggests that an increase in habitat generalist predators in response to landscape change is partially responsible for these declines. However, empirical tests have failed to reach a consensus on how and through what mechanisms landscape change affects nest predation. We tested one hypothesis, the Additive Predation Model, with an artificial nest experiment in fragmented landscapes in southern Queensland, Australia. We employed structural equation modelling of the influence of the relative density of woodland and habitat generalist predators and landscape features at the nest, site, patch and landscape scales on the probability of nest predation. We found little support for the Additive Predation Model, with no significant influence of the density of woodland predators on the probability of nest predation, although landscape features at different spatial scales were important. Within woodlands fragmented by agriculture in eastern Australia, the presence of noisy miner colonies appears to influence ecological processes important for nest predation such that the Additive Predation Model does not hold. In the absence of colonies of the aggressive native bird, the noisy miner, the influence of woodland predators on the risk of artificial nest predation was low compared with that of habitat generalist predators. Outside noisy miner colonies, we found significant edge effects with greater predation rates for artificial nests within woodland patches located closer to the agricultural matrix. Furthermore, the density of habitat generalist predators increased with the extent of irrigated land‐use, suggesting that in the absence of noisy miner colonies, nest predation increases with land‐use intensity at the landscape scale.     

A simple model for the interplay of predators, rodents and food

This paper presents a simple mathematical model for multiannual population cycles, in particular the periods, for the triple of small rodents and their predators and food. The parameters used are average birth rates of rodents and predators. The period lengths fit observations of lemmings and voles rather well and the model explains why the observed periods cluster around 4 years and around 10 years.     

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.     

Bistability and limit cycles in generalist predator–prey dynamics

Since generalist predators feed on a variety of prey species they tend to persist in an ecosystem even if one particular prey species is absent. Predation by generalist predators is typically characterized by a sigmoidal functional response, so that predation pressure for a given prey species is small when the density of that prey is low. Many mathematical models have included a sigmoidal functional response into predator–prey equations and found the dynamics to be more stable than for a Holling type II functional response. However, almost none of these models considers alternative food sources for the generalist predator. In particular, in these models, the generalist predator goes extinct in the absence of the one focal prey. We model the dynamics of a generalist predator with a sigmoidal functional response on one dynamic prey and fixed alternative food source. We find that the system can exhibit up to six steady states, bistability, limit cycles and several global bifurcations.     

Post-dispersal seed predation: consequences for plant demography and evolution

Post-dispersal seed predation is only one of many factors underlying plant demography and evolution. Nevertheless, the generalist feeding habits of many post-dispersal seed predators and the limited ability of plants either to compensate for or to respond to post-dispersal seed losses directly suggest that post-dispersal seed predation may have a considerable impact on plant populations. Seed predators probably have little direct influence on the demography of plants that regenerate exclusively by vegetative means or are buffered by a large active seed bank, but such species are only a minority in most plant communities.In general, ants are significant post-dispersal seed predators in arid and semi-arid ecosystems while they act mainly as seed dispersers rather than as predators in temperate ecosystems. Although studies have probably underestimated the importance of invertebrates and birds as seed predators, rodents appear to have greater potential to influence seed dynamics, and are particularly important in temperate ecosystems. For example, production of mast seed crops is more effective at satiating specialist invertebrate seed predators than generalist vertebrates, and recruitment may be limited by post-dispersal seed predation even during mast years.Both spatial variation in post-dispersal seed predation and differences in predation between species are important elements which facilitate the coexistence of different plant species. Where microsites are limiting, selective post-dispersal seed predators can influence pre-emptive competition for these microsites. Seed size determines the extent of density-dependent predation and the exploitation of buried seed. This suggests that post-dispersal seed predators may also play a role in the evolution of seed characteristics. However, conclusions regarding the ecological and evolutionary impact of post-dispersal seed predators will remain speculative without a more substantial empirical base.     

Influence of extraguild prey density on intraguild predation by heteropteran predators: A review of the evidence and a case study

Heteropteran predators constitute an important component of predatory guilds in terrestrial and aquatic ecosystems. Most heteropteran species have generalist diets, and intraguild predation has been documented in most heteropteran families. Zoophytophagous species also frequently engage in intraguild interactions. An increase in extraguild prey density is often predicted to reduce intraguild predation between guild members by providing abundant alternate prey. However, an increase of extraguild prey density may also be associated with an increase in the density of intraguild predators, which could instead strengthen intraguild predation. Evaluating the combined effect of these potentially opposing influences on intraguild predation is difficult. Most studies have been carried out in the laboratory, using artificially simplified communities of predators and prey and employing spatial and temporal scales that may not reflect field conditions. We review experimental studies examining how extraguild prey density influences the intensity of intraguild predation and then report an observational case study examining the influence of extraguild prey density on the intensity of intraguild predation at larger spatial and temporal scales in unmanipulated cotton fields. Fields with more abundant extraguild prey (aphids, mites) were not associated with elevated densities of intraguild predators, and were strongly associated with increased survival of intraguild prey (lacewing larvae). In this system, the ability of extraguild prey to relax the intensity of intraguild predation, as previously documented in small-scale field experiments, also extends to the larger spatial and temporal scales of commercial agriculture.     

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.     

Delayed numerical response of goshawks to population fluctuations of forest grouse

Delayed density-dependent mortality induced by delayed numerical response of predators can drive prey populations to fluctuate in high-amplitude cycles. We studied numerical response of goshawks Accipiter gentilis to varying densities of their main prey (forest grouse) in western Finland during 1979–1996. Occupancy rate of goshawk territories tracked grouse numbers with a two year lag. Occupancy rate of goshawk territories and pooled number of adult and young goshawks correlated negatively with a 1–2 year lag to the chick production of grouse. Goshawk to grouse ratio was negatively related to grouse density. This suggests that goshawk predation on grouse is inversely dependent on grouse density. We conclude that in northern Europe with few alternative preys, goshawk predation might contribute to the generation of multiannual cycles of forest grouse. This should be tested experimentally.     

Size-Related Differential Seed Predation in a Heavily Defaunated Neotropical Rain Forest

Hunting and habitat loss represent an increasingly common anthropogenic impact. Available evidence suggests that defaunation is typically differential: medium/large mammals are most affected while small rodents are less affected, or even favored. In heavily impacted areas, such as Los Tuxtlas, the residual mammalian fauna is dominated by small rodents. We tested the expectation that if small rodents will preferentially attack small-seeded species, large-seeded species may escape predation in the absence of medium/large seed predators and that this may affect germination and, possibly, recruitment. Experiments with caged rodents ( Heteromys desmarestianus ) under laboratory conditions showed a preference for smaller seeds. A field experiment involving seeds of contrasting size showed that small, unprotected seeds experienced a predation risk 30-times larger than protected seeds, while the effect of protection was not significant for large seeds. These patterns of predation led to significant differences in germination: protected small-seeded species had a fourfold greater germination than unprotected small-seeded species, while germination was not significantly different between exposed and protected large seeds. The observed contrasts in germination suggest that under heavy defaunation, small-seeded species are likely to be penalized by the overabundance of small rodents, while large-seeded species escape predation. Our results are consistent with the observation of dense seedling carpets dominated by large-seeded species in the understory of Los Tuxtlas. We speculate that the patterns we uncovered may explain, at least partly, the impoverished diversity of the understory vegetation that characterizes heavily defaunated understories and that this has the potential to affect forest regeneration.     

Is prey predation risk influenced more by increasing predator density or predator species richness in stream enclosures?

The direct lethal impacts and the indirect effects predators have on prey characteristics, such as behavior, have fitness consequences for the prey. Whether the level of predation risk that prey face in the presence of multiple predator species can be predicted from a null model that sums the risk from each predator species in isolation is unclear. In field enclosures, we tested whether the predation risk experienced by Stenonema mayfly larvae from a dragonfly larva (Boyeria vinosa) and a hellgrammite (Corydalus cornutus) together matched the predictions of the multiplicative risk model. We then compared whether any deviations from the models predictions were larger in the presence of two predator species than in the presence of an equivalent density of individuals from either predator species alone, to determine if unique effects arise for the prey in the presence of multiple predator species. We also determined if prey moved preferentially into predator-free refuge spaces or decreased their movement in the presence of predators. Stenonemas risk of predation was reduced compared to the models prediction, but no unique multiple predator species effects were present because this risk reduction was comparable in magnitude to the level exhibited in the presence of each predator species alone. The prey did not move into predator-free refuge spaces in the presence of predators in the field enclosures. Thus, these predators appear to interfere interspecifically and intraspecifically, which may facilitate the coexistence of the predators and the prey.     

The effects of predation on seasonally migrating populations

Interspecific interactions may occur for just a brief period each year before the populations involved become spatially separated. For instance, the range of a migrating population may overlap with that of a population of predators for a single season. In this work, we outline a framework for examining how this kind of ‘transient’ predation influences the dynamics of the prey population. A time-dependent switching system is used to partition the annual cycle into distinct segments. We then consider the effect of a single predatory interaction during a particular season, with the associated predators characterised as either generalists or specialists. We show that generalist predation potentially can allow multiple stable limit cycles to exist. Predation by specialists may cause prey abundance to oscillate over long time periods. This is shown to be a consequence of over-exploitation of newborn prey individuals. The habitat-based formulation extends naturally to the study of interannual variation in environmental conditions. We illustrate how such changes may cause migrant populations to undergo sudden changes in numbers that are not readily reversible.     

Parasitism-mediated prey selectivity in laboratory conditions and implications for biological control

In agroecosystems, parasitoids and predators may exert top-down regulation and predators for different reasons may avoid or give preference to parasitised prey, i.e., become an intraguild predator. The success of pest suppression with multiple natural enemies depends essentially on predator–prey dynamics and how this is affected by the interplay between predation and parasitism. We conducted a simple laboratory experiment to test whether predators distinguished parasitised prey from non-parasitised prey and to study how parasitism influenced predation. We used a host-parasitoid system, Spodoptera frugiperda and one of its generalist parasitoids, Campoletis flavicincta, and included two predators, the stinkbug Podisus nigrispinus and the earwig Euborellia annulipes. In the experiment, predators were offered a choice between non-parasitised and parasitised larvae. We observed how long it took for the predator to attack a larva, which prey was attacked first, and whether predators opted to consume the other prey after their initial attack. Our results suggest that, in general, female predators are less selective than males and predators are more likely to consume non-parasitised prey with this likelihood being directly proportional to the time taken until the first prey attack. We used statistical models to show that males opted to consume the other prey with a significantly higher probability if they attacked a parasitised larva first, while females did so with the same probability irrespective of which one they attacked first. These results highlight the importance of studies on predator–parasitoid interactions, as well as on coexistence mechanisms in agroecosystems. When parasitism mediates predator choice so that intraguild predation is avoided, natural enemy populations may be larger, thus increasing the probability of more successful biological control.