Spatial synchrony in vole population fluctuations – a field experiment

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

Spatial dynamics of Microtus vole populations in continuous and fragmented agricultural landscapes

Small mammal populations often exhibit large-scale spatial synchrony, which is purportedly caused by stochastic weather-related environmental perturbations, predation or dispersal. To elucidate the relative synchronizing effects of environmental perturbations from those of dispersal movements of small mammalian prey or their predators, we investigated the spatial dynamics of Microtus vole populations in two differently structured landscapes which experience similar patterns of weather and climatic conditions. Vole and predator abundances were monitored for three years on 28 agricultural field sites arranged into two 120-km-long transect lines in western Finland. Sites on one transect were interconnected by continuous agricultural farmland (continuous landscape), while sites on the other were isolated from one another to a varying degree by mainly forests (fragmented landscape). Vole populations exhibited large-scale (>120 km) spatial synchrony in fluctuations, which did not differ in degree between the landscapes or decline with increasing distance between trapping sites. However, spatial variation in vole population growth rates was higher in the fragmented than in the continuous landscape. Although vole-eating predators were more numerous in the continuous agricultural landscape than in the fragmented, our results suggest that predators do not exert a great influence on the degree of spatial synchrony of vole population fluctuations, but they may contribute to bringing out-of-phase prey patches towards a regional density level. The spatial dynamics of vole populations were similar in both fragmented and continuous landscapes despite inter-landscape differences in both predator abundance and possibilities of vole dispersal. This implies that the primary source of synchronization lies in a common weather-related environment.     

Landscape effects on temporal and spatial properties of vole population fluctuations

Populations of northern small rodents have previously been observed to fluctuate in spatial synchrony over distances ranging from tens to hundreds of kilometers between sites. It has been suggested that this phenomenon is caused by common environmental perturbations, mobile predators or dispersal movements. However, very little focus has been given to how the physical properties of the geographic area over which synchrony occurs, such as landscape composition and climate, affect spatial population dynamics. This study reports on the spatial and temporal properties of vole population fluctuations in two areas of western Finland: one composed of large interconnected areas of agricultural farmland interspersed by forests and the other highly dominated by forest areas, containing more isolated patches of agricultural land. Furthermore, the more agricultural area exhibits somewhat milder winters with less snow than the forested area. We found the amplitude of vole cycles to be essentially the same in the two areas, suggesting that the relative amount of predation on small rodents by generalist versus specialist predators is similar in both areas. No seasonal differences in the timing of synchronization were observable for Microtus voles, whereas bank vole populations in field habitats appeared to become synchronized primarily during winter. Microtus populations in field habitats exhibited smaller spatial variation and a higher degree of synchrony in the more continuous agricultural landscape than in the forest-dominated landscape. We suggest that this inter-areal difference is due to differences in the degree of inter-patch connectivity, with predators and dispersal acting as the primary synchronizing agents. Bank vole populations in field habitats were more synchronized within the forest-dominated landscape, most likely reflecting the suitability of the inter-patch matrix and the possibility of dispersal. Our study clearly indicates that landscape composition needs to be taken into account when describing the spatial properties of small rodent population dynamics.     

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.     

Geographical and temporal patterns of lemming population dynamics in Fennoscandia

There is a long-lasting debate in ecology on cyclicity. synchrony and time lags of lemming population fluetuations. We have analysed 137 yr of previously published population data on the Norwegian lemming Lemmus lemmus in ten geographic regions of Fennoscandia. The dominating pattern was synchronous 4-yr cycles. There was no support for the hypothesis of a north-south gradient in cycle length. However, we found periods of prolonged interruptions in the cyclicity, which were more eommon in northern areas. We found a high degree of synchrony between regions, with only a weak relationship to distance. The observed pattern in lemming population dynamics was more consistent with effects from extrinsic factors, such as climate, than intrinsic factors, such as dispersal.     

Are goose nesting success and lemming cycles linked? Interplay between nest density and predators

The suggested link between lemming cycles and reproductive success of arctic birds is caused by potential effects of varying predation pressure (the Alternative Prey Hypothesis, APH) and protective association with birds of prey (the Nesting Association Hypothesis, NAH). We used data collected over two complete lemming cycles to investigate how fluctuations in lemming density were associated with nesting success of greater snow geese ( Anser caerulescens atlanticus ) in the Canadian High Arctic. We tested predictions of the APH and NAH for geese breeding at low and high densities. Goose nesting success varied from 22% to 91% between years and the main egg predator was the arctic fox ( Alopex lagopus ). Nesting associations with snowy owls ( Nyctea scandiaca ) were observed but only during peak lemming years for geese nesting at low density. Goose nesting success declined as distance from owls increased and reached a plateau at 550 m. Artificial nest experiments indicated that owls can exclude predators from the vicinity of their nests and thus reduce goose egg predation rate. Annual nest failure rate was negatively associated with rodent abundance and was generally highest in low lemming years. This relationship was present even after excluding goose nests under the protective influence of owls. However, nest failure was inversely density-dependent at high breeding density. Thus, annual variations in nest density influenced the synchrony between lemming cycles and oscillations in nesting success. Our results suggest that APH is the main mechanism linking lemming cycles and goose nesting success and that nesting associations during peak lemming years (NAH) can enhance this positive link at the local level. The study also shows that breeding strategies used by birds (the alternative prey) could affect the synchrony between oscillations in avian reproductive success and rodent cycles.     

Owl winter irruptions as an indicator of small mammal population cycles in the boreal forest of eastern North America

Contrary to what is observed in Fennoscandia, it seems to be widely accepted that small mammals do not exhibit multi-annual population cycles in the boreal forest of North America. However, in the last thirty years, irruptions of vole predators such as owls have been reported by ornithologists south of the North American boreal forest. While such southerly irruptions have been associated in Fennoscandia with periods of low abundance of small mammals within their usual distribution range, their possible cyclic nature and their relationships to fluctuations in vole densities at northern latitudes has not yet been demonstrated in North America. With information collected from existing data-bases, we examined the presence of cycles in small mammals and their main avian predators by using temporal autocorrelation analyses. Winter invasions of boreal owls ( Aegolius funereus ) were periodic, with a 4-yr cycle in Québec. Populations of one species of small mammal, the red-backed vole ( Clethrionomys gapperi ), fluctuated periodically in boreal forests of Québec (north to 48°N). Boreal owls show invasion cycles which correspond to years of low density of red-backed voles, the main food item for this owl species. In addition, winter observations of northern hawk owls ( Surnia ulula ) and great gray owls ( Strix nebulosa ) south of their usual range increased in years of low density of red-backed voles. Our results suggest that a 4-yr population cycle exists in the eastern boreal forest of North America for voles and owls, which is very similar to the one observed in Fennoscandia.     

Patterns in grouse and Woodcock Scolopax rusticola hunting yields from central Norway 1901–24 do not support the alternative prey hypothesis for grouse cycles

According to the alternative prey hypothesis, autumn populations of ground-nesting game birds fluctuate in synchrony with vole numbers because generalist predators that mainly eat voles switch to alternative prey, such as eggs and chicks, when vole numbers decline. In hunting statistics from Nord-Trøndelag, central Norway, 1901–24, annual fluctuations in the number of Willow Grouse Lagopus lagopus and Western Capercaillie Tetrao urogallus , but not of Woodcock Scolopax rusticola , were positively related to vole numbers in the current year. Both Woodcock and grouse indices were related to hunting indices of Goshawk Accipiter gentilis and to weather variables assumed to influence the birds' survival or reproduction, suggesting that the indices actually reflected local population levels. Synchronous vole and grouse fluctuations are consistent with the alternative prey hypothesis (although predator densities were low in the early 1900s), but the asynchronous Woodcock fluctuations refute the hypothesis. Rather, because the Woodcock does not feed on plants utilized by voles and grouse, I suggest that food quality is the ultimate factor for the synchrony in vole and grouse numbers in Norway.     

An estimate of the impact of predators on the British Field Vole Microtus agrestis population

The productivity of the British Field Vole population is estimated to be between 677 000 and 982 000 voles per year, depending on the precise basis of the calculation. The total consumption of Field Voles by all the major predators, mammalian and avian, is estimated to be around 980 000, if the very uncertain consumption by Feral Cats is included. Two specialist vole predators (Weasel, Kestrel) and two generalist predators (Red Fox, Feral Cat) consume 85% of the total between them, the other 10 species share the rest between them. However important voles might be for owls, owl predation is unimportant to voles. The slight evidence for cyclicity in Field Vole populations in Britain might be explained by the overall take of voles by the predators, and by the rather generalized diet of even the vole specialists.     

Vole cycles and antipredatory behaviour

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

The breeding productivity of dark-bellied brent geese and curlew sandpipers in relation to changes in the numbers of arctic foxes and lemmings on the Taimyr Peninsula, Siberia —

There were about three-year cycles in the populations of arctic foxes, and the breeding productivities of brent geese and curlew sandpipers on the Taimyr Peninsula, Russia, The populations of arctic foxes and lemmings changed in synchrony. The breeding productivities of the birds tended to be good when the arctic foxes were increasing in numbers and poor when the arctic foxes were decreasing. There was a negative relationship between arctic fox numbers (or occupied lairs) and the breeding productivity of brent geese in the following year. Although there was evidence of wide-spread synchrony In the lemming cycle across the Taimyr Peninsula, some localities showed differences, However, such sites would still have been influenced by the general pattern of fox abundance in the typical tundra zone of the Taimyr Peninsula, where most of the arctic foxes breed and from which extensive movements of foxes occur after a decline in lemming numbers. The results support a prey-switching hypothesis (also known as the alternative prey hypothesis) whereby arctic foxes, and other predators, feed largely on lemmings when these are abundant or increasing, but switch to birds when the lemming population is small or declining. The relationships between arctic foxes, lemmings and brent geese may be further influenced by snowny owls which create fox-exclusion zones around their nests, thus providing safe nesting areas for the geese.     

Habitat composition as a determinant of reproductive success of Tengmalm's owls under fluctuating food conditions

The effect of landscape composition on the breeding success of vole-eating Tengmalm's owl ( Aegolius funereus ) was studied in western Finland at five different spatial scales (250–4000 m) around the nests during two consecutive three-year population cycles of voles. Landscape composition had strongest effects on owl breeding in the decrease phase of vole cycles. Significant variation in owl breeding occurred along the productivity gradient from farmland predominated areas to barren hinterland. Owls tended to produce earlier clutches on territories predominated by agricultural areas in increasing vole years. A similar trend was observed in the decreasing phase of the vole cycle; owls breeding on barren hinterland seemed to delay breeding compared to owls breeding near agricultural areas. Surprisingly, nestling survival and fledgling production in the decreasing phase declined steeply with increasing proportion of farmland. Clutch size was not significantly related to landscape composition. The number of fledglings decreased with increases in clear-cut and sapling areas in the decrease phase. During the declining years of vole abundance nestling survival increased from western farmland areas towards the eastern outlying district. These results indicate sudden summer decline of vole populations on farmland predominated habitats. This is probably due to that the number of vole-eating predators, and hence their impact on vole populations is apparently higher in farmland areas than on forested hinterland. This finding gives support for the 'spill-over' hypothesis, which states that predators and their exploitation tends to 'spill over' from luxuriant habitats to the barren habitats.     

Long-term microtine dynamics in north Fennoscandian tundra: the vole cycle and the lemming chaos

Densities of microtine rodents in two habitat complexes in the tundra of Finnmarks-vidda, Norwegian Lapland, were studied during 1977-89 by means of snap trapping (Small Quadrat Method) Predator populations were studied by mapping breeding raptors and by snow-tracking small mustelids During 1977-85, snow-trackmg was conducted only during peak and decline years, whereas during 1986-89, snow-tracking was conducted every winter (November-December) and live-trapping (in August) was used as an additional method
Lowland vole populations had regular density fluctuations with peaks in 1978-79. 1982-84 and 1987-88 Highland vole populations fluctuated less regularly and at lower over-all densities Highland lemming populations had two outbreaks, in 1978 and 1988, ending in abrupt winter crashes In the lowland, outbreak levels were reached only in 1978 All microtine declines in relatively productive lowland habitats were accompanied by intense activity of small mustelids. whereas avian predators were common only in 1983 Lowland declines also showed clear between-habitat asynchrony they started in areas with an exceptional abundance of productive habitats and then spread to more barren areas These lowland data are consistent with the hypothesis of a mustelid-microtine limit cycle, although also several other hypotheses remain unrefuted The highland lemming data suggest a simple exploiter-victim interaction between lemmings and the vegetation     

Numerical response of small mustelids to vole abundance: delayed or not?

One of the most studied problems in population ecology has been to understand the relative roles of top–down and bottom–up forces in regulating animal populations. This has also been a key issue in studies of vole population dyna mics. Vole populations exhibit a wide variation of dynamics, from seasonal fluctuations to multiannual variations or cyclicity. One of the hypotheses to explain cyclic population dynamics is predation by the specialist predators. A common counterargument against the predation hypothesis has been the lack of conclusive observations of the time delay in the predators’ numerical response. We studied the interaction between voles and their specialist small mustelid predators, the stoat Mustela erminea and the least weasel Mustela n. nivalis, by modelling their interaction to data sets that cover large areas of Finland. Vole abundance was monitored with biannual trappings and their predators with snow‐tracking. Results show a high dependence of the predators on the voles, and this connection is generally tighter in weasels than in stoats. Weasel abundance is affected most strongly by the vole abundance in previous spring, 8.5– 10 months earlier, while in stoats the effect of autumn abundance of voles, 2.5–6 months earlier, was the strongest. These results, together with the observation that the weasels’ effects on voles are stronger after a time lag of 6–9.5 than 2–4.5 months, indicate the existence of a time lag in weasels’ numerical response. A time lag in the predators’ numerical response is a necessary condition for the predators to drive population cycles in its prey, and therefore our results support the specialist predation hypothesis.     

Environmental,parental and adaptive variation in egg size of Tengmalm's owls under fluctuating food conditions

We studied egg size variation of Tengmalm's owls in western Finland during 1981–1990. The owls fed on voles whose population fluctuated in a predictable manner: low (1981, 1984, 1987, 1990), increase (1982, 1985, 1988) and peak (1983, 1986, 1986) phases of the cycle occurred every third year. Eggs were largest in the increase phase of the vole cycle, even though that voles were more abundant and egg-laying started earlier in the peak phase than in the increase phase. This suggests that owls invest mostly in egg size when vole abundance increases along with survival chances of offspring. Territory quality and female age had no effects on egg size, but egg size decreased with laying data in the increase phase of the vole cycle. Egg size was significantly positively related to the male age in the increase phase, but the opposite relationship was significant in the peak phase of the vole cycle. The partners of adult males also decreased their egg volume from the increase to the peak phase, whereas the partners of yearling males produced their largest eggs in the peak phase of the vole cycle. This suggests the importance of experience in prevailing food fluctuations. Possibly male Tengmalm's owls can adjust the intensity of courtship feeding not only in relation to the food abundance on their territories at the time of egg laying, but also to the survival prospects of their offspring. Phenotypic plasticity seems to play a substantial role, as the egg size repeatabilities of individual females and partners of individual males were low. Obviously, under cyclic food conditions, predictability and inter-generational trade-offs are important to life history traits.     

Spatio‐temporal covariation in abundance between the cyclic common vole Microtus arvalis and other small mammal prey species

Populations of the common vole Microtus arvalis in mid‐western France show cyclic dynamics with a three‐year period. Studies of cyclic vole populations in Fennoscandia have often found inter‐specific synchrony between the voles and other small mammals which share the voles' predators. Although predators are central to the favoured mechanism to explain Fennoscandian vole cycles and the spatial variation of small mammal populations, their role in vole cycles elsewhere, including France, is less clear. Establishing whether alternative prey species in France cycle in parallel with voles as they do in Fennoscandia is thus an important step towards understanding the generality of predators' influence on cyclic vole populations. We applied spatial and temporal autocorrelation and cross‐correlation methods to French populations of M. arvalis and two sympatric non‐cyclic small mammal species, Apodemus sylvaticus and Crocidura russula. Patterns of time‐lagged cross‐correlation between the abundance of M. arvalis and the other two species suggested synchrony in their dynamics beyond that expected of stochastic environmental variation, and indicated a weak three‐year cycle in A. sylvaticus and C. russula that was in phase with that of M. arvalis. We interpret the synchrony between these species as the effect of shared predators and environmental stochasticity. Abundance within species showed weak spatial autocorrelation in June at scales consistent with dispersal being the mechanism responsible, but a more general lack of spatial structure within and between species was consistent with the strong spatial synchrony at regional scales often found in fluctuations of small mammal abundance.     

Tawny owl prey remains indicate differences in the dynamics of coastal and inland vole populations in southern Finland

Some studies suggest that mild winters decrease overwinter survival of small mammals or coincide with decreased cyclicity in vole numbers, whereas other studies suggest non-significant or positive relationships between mild winter conditions and vole population dynamics. We expect for the number of voles to be higher in the rich and low-lying habitats of the coastal areas than in the less fertile areas inland. We assume that this geographical difference in vole abundances is diminished by mild winters especially in low-lying habitats. We examine these relationships by generalized linear mixed models using prey remains of breeding tawny owls Strix aluco as a proxy for the abundance of voles. The higher number of small voles in the coastal area than in the inland area suggest that vole populations were denser in the coastal area. Vole populations of both areas were affected by winter weather conditions particularly in March, but these relationships differed between areas. The mild ends of winter with frequent fluctuations of the ambient temperature around the freezing point (“frost seesaw”) constrained significantly the coastal vole populations, while deep snow cover, in general after hard winters, was followed by significantly lowered number of voles only in the inland populations. Our results suggest that coastal vole populations are more vulnerable to mild winters than inland ones. We also show that tawny owl prey remains can be used in a meaningful way to study vole population dynamics.     

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.     

Diet variation of common buzzards in Finland supports the alternative prey hypothesis

The regional synchrony of short-term population fluctuations of small rodents and small game has usually been explained by varying impacts of generalist predators subsisting on both voles and small game (the "alternative prey hypothesis" APH). APH says that densities of predators increase as a response to increasing vole densities and then these predators shift their diet from the main prey to the alternative prey when the main prey decline and vice versa. We studied the diet composition of breeding common buzzards Buteo buteo during 1985-92 in western Finland. Microtus voles were the main prey and water voles, shrews, forest grouse, hares and small birds the most important alternative prey. Our data from the between-year variation in the diet composition of buzzards fulfilled the main predictions of APH. The yearly proportion of main prey (Microtus voles) in the diet was higher in years of high than low vole abundance. The proportion of grouse in the diet of buzzards was negatively related to the abundance of Microtus voles in the field and was nearly independent of grouse abundance in the field. In addition, buzzards mainly took grouse chicks and young hares which is consistent with the prediction of APH. Therefore, we conclude that buzzards are able to shift their diet in the way predicted by the APH and that buzzards, together with other generalist predators, may reduce the breeding success of small game in the decline phase of the vole cycle, and thus substantially contribute to the existence of short-term population cycles of small game.     

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.