Ecology, 83(12), 2002, pp.

3449–3456
q 2002 by the Ecological Society of America

INTRINSIC AND CLIMATIC DETERMINANTS OF POPULATION

DEMOGRAPHY: THE WINTER DYNAMICS OF TUNDRA VOLES
JON AARS1,3 AND ROLF A. IMS2
1Department of Zoology, University of Aberdeen, Tillydrone Avenue, Aberdeen AB24 2TZ, Scotland, UK
2 Department of Ecology, Institute of Biology, University of Tromsø, N-9037 Tromsø, Norway

Abstract. The relative impacts of intrinsic factors (e.g., density dependence) and ex-
trinsic factors (e.g., climate) on winter demography may be critical for the generation of
different population dynamic patterns (including cyclicity) in northern vole and lemming
populations. However, little is known about winter demography because studies with tem-
poral and spatial replication at the population level and an adequate sample of individuals
with known fates within each population are rare. In this study, we monitored the winter
demography of 48 local tundra vole populations introduced to experimentally enclosed
plots the preceding spring for four years in Norway.
The rate of population change over the winter (November–May) was density dependent
due to recruitment. However, the large variation in the rate of change between the different
winters was due to a density-independent, and most likely a climatically driven, variation
in survival rate. In particular, mild weather that led to the formation of ice on the ground
seemed to be detrimental for winter survival. We predict that if increased frequency of
such events arose, due to climate change, normal cyclic dynamics of northern small rodent
populations would be disrupted.
We found support for the hypothesis that voles adjusted their body mass toward a certain
mean during the winter so as to maximize winter survival. The survival rate of males was
lower than that of females, possibly due to their larger body mass, and this resulted in
female-biased population sex ratios in the spring. This result suggests a link between sexual
selection (responsible for the sexual size dimorphism) and natural selection (operating
though size-dependent winter survival) with implications for the demographic structure of
the population.
Key words: body mass; density dependence; Microtus oeconomus; Norway; population cycles;
sex ratio; survival rate; tundra vole; winter climate.

INTRODUCTION population fluctuations, often with clear evidence of

The population dynamics of small mammals can be
simultaneously determined by density-dependent and
density-independent factors (Leirs et al. 1997, Karels
and Boonstra 2000). Climatic factors, which normally
underlie the density-independent component of popu-
lation change, are expected to exert their influence most
strongly during certain seasons (e.g., the summer dry
period in the tropics or the winter cold period in the
arctic). Density-dependent processes are more likely to
shape population dynamics year round. However, the
specific mechanism of the density dependence may dif-
fer depending on the season (Ostfeld et al. 1993, Ost-
feld and Canham 1995, Hansen et al. 1999). Knowing
the relative strength of density-dependent and density-
independent processes during all seasons of the year is
necessary to understand the great variety of multi-an-
nual population dynamics found in small mammals
(Turchin and Ostfeld 1997, Stenseth 1999).
Small mammal populations in regions with long and
snowy winters have become famous for their violent
Manuscript received 14 November 2001; revised 18 April
2002; accepted 22 April 2002.
3 E-mail: jon.aars@abdn.ac.uk
3449
cyclic dynamics (Hansson and Henttonen 1988, Hanski
et al. 1993, Stenseth and Ims 1993, Bjørnstad et al.
1995, Turchin and Hanski 1997). Winter has been sus-
pected to play a crucial role in the generation of the
population dynamics pattern in northern regions (Hans-
son and Henttonen 1988, Stenseth 1999, Yoccoz and
Ims 1999). Although recent analyses of time series have
indicated that the rate of population change during the
winter is strongly density dependent (Stenseth et al.
1998, Hansen et al. 1999), the demographic mecha-
nisms underlying the rate of change have not yet been
elucidated. To unravel the demographic mechanisms,
capture–recapture data monitoring the fates of the in-
dividuals over the winter will be required. Unfortu-
nately, demographic studies of northern rodents con-
ducted on a multi-annual time scale are generally scarce
(Yoccoz et al. 1998). In particular, studies covering the
critical winter period are almost nonexistent and thus
badly needed (Stenseth 1999).
Here we analyze winter demography of the tundra
vole (Microtus oeconomus) in grassland habitats based
on data covering four consecutive winters at Evenstad
Research Station, in southeastern Norway. Evenstad
has a continental winter climate (mean temperature in
3450 JON AARS AND ROLF A. IMS
January: 210.78C), with snow normally covering the
ground from November to late April. Our analyses were
facilitated by spatial replication of experimentally en-
closed populations and by a large number of individ-
ually marked animals at the onset of the winter, of
which a sample sufficient to allow statistical analyses
was recaptured in the spring. The experimental setting
was repeated over four winters so that the study in-
cluded among-year variation in winter weather.
We focused on two aspects of winter demography.
First, at the population level, we quantified the effects
of density-dependent and density-independent factors
on the rate of population change during the winter, and
we estimated the contribution of survival and recruit-
ment to these effects. Second, based on the well-es-
tablished fact that most northern small mammals de-
press their body size from summer to winter (Iverson
and Turner 1974, Whitney 1976, Merritt and Merritt
1978, Hansson 1990, 1991, 1992), we tested the hy-
pothesis that mass loss over the winter is an adaptive
adjustment to maximize winter survival (Stenseth
1978, Hansson 1990). Changes in mass in small rodents
have been shown to be induced by photoperiod (Dark
1983), thus indicating that it is an adaptive preparation
for the winter (Iverson and Turner 1974, Malcolm and
Brooks 1993). We also evaluated possible links be-
tween individual-level life history tactics and popu-
lation-level dynamics based on the results of our anal-
ysis.
MATERIALS AND METHODS
The data was obtained from experiments conducted
during the years 1994 to 1998 at Evenstad Research
Station in southern Norway (618129 N, 118069 E). New
experimental populations of tundra voles were estab-
lished in spring/early summer every year by releasing
laboratory-raised tundra voles on six fence-enclosed
experimental plots. The animals in the laboratory were
outbred as new animals from the field were added to
the breeding stock every year. Each plot was 0.5 ha
(50 3 100 m) and contained two 750-m2 (20 3 37.5
m) meadow patches (i.e., habitat) separated by 50 m
of barren ground that was treated with herbicide during
the growing season. As effective dispersal between the
two patches was mostly restricted to the early summer
season (Aars et al. 1999), each enclosure effectively
consisted of two populations both in the autumn and
during the winter. The meadow patches in the experi-
mental plots were fertilized every spring to standardize
habitat quality among the years. This gave rise to a
dense vegetation cover that formed a thick mat of wilt-
ed grass and herbs during the winter period. We chose
to burn this debris every spring as to avoid a gradual
change in the substrate that would increase the envi-
ronmental variability between habitat patches in time
and space. Tundra voles are common in natural and
seminatural meadow patches in the surroundings of the
experimental plots at Evenstad and elsewhere in alpine
Ecology, Vol. 83, No. 12
and boreal meadow and mire habitats in Fennoscandia
(Tast 1966). The population densities in the enclosures
were within the range of what has been observed in
natural populations. Details regarding the maintenance
of the plots and the procedure for establishment of the
experimental populations can be found in Aars and Ims
(1999, 2000), Aars et al. (1999), and Gundersen et al.
(2001).
The populations grew freely over the summer, and
were monitored by 3-d live-trapping sessions (capture–
mark–recapture trapping) every 18 d throughout the
snow-free period. A high trap density in the habitat
patches and 6 trap checks during the 3 d in each trap-
ping session ensured close to 100% trapping rate all
years (see Aars et al. 1999, Aars and Ims 2000, Gun-
dersen et al. 2001). Thus, we could ignore capture prob-
ability when estimating demographic rates. Live trap-
ping was terminated when permanent snow cover was
established in November. Trapping was resumed im-
mediately after the snow had melted in late April or
early May. During this spring trapping session, all an-
imals were removed and the plots were left empty until
new populations were established by the release of new
laboratory-raised animals. The vole-proof fences effi-
ciently prevented dispersal between enclosures also
over the winter, despite drifted snow in some short
periods that reached the fence tops. No marked animal
was ever recorded to have moved between enclosures.
Analyses of the summer demography in the exper-
imental populations are found in Aars et al. (1999),
Aars and Ims (1999, 2000), and Gundersen et al.
(2001). These analyses focus on the effects of dispersal
on demography and population genetics. Here, we use
data from the two trapping sessions at the onset and
termination of the winter, respectively, to highlight de-
mographic processes during winter.
The rate of population change from autumn (Nautumn)
to spring (Nspring) at the patch level was analyzed by
fitting the following statistical model to the data (Le-
breton 1991):
Nspring,i 5 Nautumn,i 3 exp[a j 1 b j 3 Nautumn,i ] 1 « i
where b is the strength of density dependence (i.e., the
slope), a a constant, j is year (i.e., winter), and « is an
error term specific to each population i. The model was
fitted to the data using a logarithmic link, i.e., log
(E[Nspring]), with log(Nautumn) as an offset term, and the
error term was quasi-Poisson distributed due to over-
dispersion (residual deviance/df 5 3.32). The influence
of year was tested (Wald x2) with respect to the a-
(additive year effect) and b-parameters (year 3 Nautumn
interaction effect).
Recruitment was analyzed with Poisson regression,
and survival with logistic regression. These regression
models fitted the data (i.e., no overdispersion), and the
significance of the predictor variables could be eval-
uated with ordinary likelihood ratio tests and Akaike’s
Information Criterion (AIC) values.
December 2002 WINTER DEMOGRAPHY OF VOLES
FIG. 1. Change in population density (number of tundra
voles per habitat patch) from autumn to spring during the
four years of this study at the Evenstad Research Station,
Norway.
RESULTS
Population level parameters
The habitat patches constitute the natural scale for
analyses of density-dependent effects on population pa-
rameters, because the densities frequently differed
markedly between the two patches within enclosures.
There was no tendency for patch-specific population
densities to be similar within enclosures (enclosure ran-
dom effect on log[spring density], F15,18 5 1.00, P 5
0.49).
The rate of decline in patch-specific population den-
sities (number of animals per habitat patch) over the
winter varied strikingly among the four years (Fig. 1).
The declines were most severe during the winters of
1994 and 1997. The fairly low-density autumn popu-
lations in 1997 (on average 17 6 8 individuals per patch
[mean 6 1 SD]) were all extinct by the following spring.
In 1994, four of the 12 patches, which generally had
very high autumn densities (77 6 23 individuals per
patch in November), went extinct, and the eight extant
spring populations were only 6% of their autumn size.
The autumn populations of 1995 and 1996 had very
similar average sizes (1995: 31 6 13 and 1996: 29 6
13 individuals per patch), and all were extant in the
spring, with 36% (1995) and 22% (1996) of their au-
tumn numbers, respectively.
We had to exclude the year 1997 from the analysis
because there were no extant populations left in the
spring. In addition to a significant partial effect of year
(Wald x2 5 10.20, df 5 2, P 5 0.006), there was also
evidence for a negative density-dependent rate of
change over the winter (b 5 20.020 6 0.009 [mean
6 1 SE], Wald x2 5 5.12, df 5 1, P 5 0.024) (Fig. 2).
This model accounted for 64% of the total variation
(i.e., deviance).
On average, 26.5% of the animals in the spring were
unmarked due to recruitment over the winter period
(November–April). A Poisson regression gave evi-
dence for a strong negative effect of population density
in the autumn on the number of recruits in a patch the
3451
following spring (Nrecruits 5 exp[1.65 2 0.03 3 Nautumn],
likelihood ratio test [LRT] x2 5 16.70, df 5 1, P ,
0.0001). Adding year as an extra term in this model
did not improve its fit (year effect: LRT x2 5 2.10, df
5 3, P 5 0.35).
Winter survival rates differed markedly among
years, and a logistic regression model applied to the
patch-specific proportion of individuals present in No-
vember that were recaptured six months later in the
spring gave the following estimates of year-specific
survival probabilities: 1994: 0.02 (95% CI 5 0.01–
0.05), 1995: 0.25 (95% CI 5 0.17–0.34), 1996: 0.15
(95% CI 5 0.09–0.24). There was no evidence for den-
sity-dependence in the survival rate (Wald x2 5 0.52,
df 5 1, P 5 0.48). The yearly estimates of winter
survival rates correlated negatively with the mean win-
ter temperature at Evenstad (Pearson product-moment
correlation r 5 0.97, n 5 4, P 5 0.034). The mildest
winters with the lowest survival rates had many days
with temperatures .08C during the midwinter period
(Fig. 3). This corresponds well with our observations
in the field in the spring, especially in 1995 and 1998,
when vole habitats were extensively covered by ice as
a result of alternating melting and freezing events dur-
ing the winter.
Altogether, these analyses of recruitment and sur-
vival show that the highly variable winter decline rate
had a large among-year component due to a highly
variable winter survival rate, most likely due to vari-
able winter climate. The winter demography also had
a considerable density-dependent within-year compo-
nent due to a sharply declining recruitment rate with
increasing autumn densities.
Individual level parameters
Turning to the relationship between the autumn body
mass of the individuals and their survival probability,
we found that a logistic regression model with autumn
FIG. 2. Rate of population change in tundra voles from
autumn to spring (r 5 log[Nspring/Nautumn]) as a function of
autumn population density for years with extant populations
in the spring.
3452 JON AARS AND ROLF A. IMS Ecology, Vol. 83, No. 12

small and large animals (Fig. 4), but also a change in

body mass from autumn to spring for those animals
that survived the winter (Fig. 6). Large individuals, in
particular large females (.29 g), lost mass from au-
tumn to spring, while small individuals (especially
males) grew (Fig. 6). The small individuals (,20 g) in
the autumn were juveniles that had been recently
weaned, while some of the largest individuals (.35 g)
were still reproducing. There were no signs of repro-
ductive activity in the spring populations.
DISCUSSION
The rate of population change over winter had both
density-dependent and density-independent compo-
nents in this study. In previous studies, the relative

FIG. 3. Yearly winter tundra vole survival rate (with 95%

confidence intervals) plotted against the number of days with
temperatures above 08C during midwinter (December–Feb-
ruary). Mean winter temperature and the year are denoted
above the survival rate estimates.

body mass as a second order polynomial (mass 1

mass2: LRT x2 5 19.55, df 5 2, P , 0.0001) and with
different intercepts for the two sexes (LRT x2 5 11.28,
df 5 1, P 5 0.001) and the three years (LRT x2 5
167.49, df 5 2, P , 0.0001) explained the variation
in survival best in terms of the model selection criterion
AIC (we found no evidence for any interaction between
year and mass: LRT x2 5 1.30, df 5 2, P 5 0.58). The
predicted survival function according to body mass was
modal with a maximum survival probability for ani-
mals weighing 25 g in the autumn in each year (Fig.
4). Females survived generally better than males (odds-
ratio females:males: 1.93, 95% CI 5 1.61–2.32), caus-
ing the sex ratio to change from 55% females in the
autumn to 70% in the spring. A variable denoting
whether an individual had been recorded as reproduc-
tive or not during the summer did not improve the
survival model described above (LRT x2 5 0.35, df 5
1, P 5 0.55). However, reproductive activity and au-
tumn mass were confounded (R2 5 53%, mean autumn
mass reproductive: 43.5 6 8.6 [mean 6 1 SD], non-
reproductive: 24.5 6 7.2), so their relative effects on
winter survival were hard to assess. Nonetheless, au-
tumn body mass appeared more important than repro-
ductive history, since a survival model with reproduc-
tive history substituting the polynomial mass term gave
a less appropriate model (DAIC 5 5). Moreover, within
the group of animals that had reproduced there was a
significant negative effect of body mass (LRT x2 5
5.92, df 5 1, P 5 0.015), while this was not the case
for those animals that had not reproduced over the
course of the summer (LRT x2 5 0.61, df 5 1, P 5 FIG. 4. Winter survival probability predicted from body
0.43). mass in the autumn for males (solid circles) and females (open
circles) in the three years with extant spring populations of
The variance of the body mass distribution shrank tundra voles. Observed survival and deaths (both sexes com-
quite substantially from autumn to spring (Fig. 5). This bined) are shown as small black squares at the top and the
change partly reflects the lower survival rate of very bottom of each panel, respectively.
December 2002 WINTER DEMOGRAPHY OF VOLES 3453

FIG. 5. Female and male tundra vole body mass distributions in autumn and spring.

impacts of environmental stochasticity and density de- Tast 1984), and most often during winters preceding
pendence on the rate of population change over the cyclic peaks in summer population density. However,
winter in vole and lemming populations have mostly it has been an unresolved issue whether population den-
been inferred from time series data of population den- sity or other circumstances are the triggering factors
sity (Reid and Krebs 1996, Stenseth et al. 1998, Hansen (Krebs 1993, Hansson 1984). Although the four winters
et al. 1999, Stenseth 1999). However, the underlying in this study differed much in terms of the rate of
demographic mechanisms have remained elusive due population change and the mortality rate, there was no
to a lack of sufficient capture–recapture data in terms independent effect of year on recruitment rate, thus
of spatial and temporal replication. In this study, we pointing to population density as the most important
had access to an extensive data set comprising indi- determinant of winter breeding.
vidually marked animals distributed on a large number
of population replicates allowing for inferences about
determinants of winter demography, both at the level
of individuals and populations.
We found that the density-dependent component of
population change worked through recruitment, but we
found no evidence for a density-dependent effect on
survival. This result is consistent with previous de-
mographic studies of tundra voles and other Microtus
species in the normal breeding season (spring and sum-
mer), which showed that recruitment is the most strong-
ly density-dependent demographic parameter (Ostfeld
et al. 1993, Ostfeld and Canham 1995, Ims and An-
dreassen 1999). However, studies on winter demog-
raphy are rare, and in particular, winter breeding is a
poorly understood phenomenon in northern popula-
tions of small mammals (Hansson 1984, Krebs 1993).
While responsiveness to photoperiod at the onset of
reproductive activity has been shown to exhibit indi- FIG. 6. Change in body mass from autumn to spring for
vidual variation under laboratory conditions (Spears individual males (solid circles) and females (open circles)
and Clarke 1988, Bronson and Kerbeshian 1995), it is plotted against autumn body mass. Female regression line
(solid line): growth 5 19.6 2 0.68(autumn mass), r2 5 0.76,
unclear how this could produce population-level var- n 5 111, P , 0.001. Male regression line (dashed line):
iation in nature. Recruitment in the winter seems to growth 5 25.3 2 0.62(autumn mass), r2 5 0.53, n 5 52, P
take place only occasionally in voles (Hansson 1984, , 0.001.
3454 JON AARS AND ROLF A. IMS
Although density-dependence influenced the winter
dynamics through recruitment (at least for those pop-
ulation that did not go extinct), population density at
the onset of the winters was a poor predictor of the
fate of a population over the winter when considering
all four winters included in this study. For example,
the most severe population crashes (causing extinc-
tions) took place after the two autumns with maximum
(1994) and minimum (1997) population densities, re-
spectively. Indeed, the demographic parameter most
responsible for the highly variable winter dynamics in
this study, namely winter mortality, showed no evi-
dence of density dependence.
The experimental setting at Evenstad was similar
across the years. Mammalian predators were excluded
with fences and removal trapping, and the conditions
within the enclosures were standardized by introducing
new laboratory-raised founder populations and by
burning and fertilizing the habitat patches every spring.
Thus, potential influences of delayed density-depen-
dent factors can most likely be ruled out. Still, the
population dynamics in the experimental populations
of tundra voles at Evenstad were dominated by large
annual variation, both during the winter and during the
summer, as shown elsewhere (Aars et al. 1999, Ims and
Andreassen 2000). Moreover, just like what is the case
for winter dynamics, it is differential mortality that
drives the between-year variation in summer dynamics
(Ims and Andreassen 2000). Due to detailed monitoring
of radio-tagged individuals during the summer, it has
been demonstrated that the main mortality factor was
predatory birds (Ims and Andreassen 2000). Although
we do not have equivalent information on the fates of
individuals during the winter, the strong correlation
between winter temperature and winter survival rate
suggests that the winter demography to a large extent
was climatically driven. In particular, it seems that win-
ters with mild weather are detrimental because of the
formation of ice on the ground. When inspecting the
meadow patches at Evenstad during snow melt in the
spring, we recorded extensive formation of ice covering
the ground in these two years. Such ice formations will
both reduce thermal insulation and accessibility of food
resources and, moreover, causes flooding during spring
thaw. It is possible that the flat, homogeneous habitats
in our experimental areas exaggerated the influence of
such climatic events. However, for natural populations
inhabiting heterogeneous landscapes, similar critical
weather episodes in winter and early spring have also
been suggested to dramatically reduce winter survival
in small mammals (e.g., Merritt and Merritt 1978,
Boonstra and Rodd 1983). Such episodes introduce a
strong stochastic element in the demography that may
dominate the population dynamics of some northern
small-mammal populations (Yoccoz and Ims 1999).
Predation can be ruled out as an important factor of
winter survival in our study. The species of birds of
prey that influenced summer survival (Ims and An-
Ecology, Vol. 83, No. 12
dreassen 2000) are absent during the winter period.
Mustelides were efficiently kept out by the predator
fence and trapping. No tracks of mammalian predators
were observed on the snow cover, even though the
enclosures were visited several times during the winter
months.
Evenstad belongs to a geographic region (the north-
ern boreal coniferous forest zone), where the previous
population cycle of Microtus voles has vanished during
the last two decades (Lindström and Hörnfeld 1994,
Hanski and Henttonen 1996, Steen et al. 1996). Small
rodent population fluctuations in this region now are
characterized by declines during the winter leading to
low spring population densities (Steen et al. 1996,
Hansson 1999). The changes in dynamics have been
particularly pronounced for Microtus voles in grassland
habitats (Hanski and Henttonen 1996, Steen et al.
1996). Although climate has been suggested as a po-
tential cause that either directly (i.e., due to lack of
snow or presence of ice; Yoccoz and Ims 1999) or
indirectly (i.e., due to predation; Lindström and Hörn-
feld 1994, Hansson 1999) regulates winter survival,
the mechanism of the increased mortality rate during
the winter should be studied in greater detail.
Some clues to the mechanism by which winter cli-
mate influences population demography can be ob-
tained by identifying individual determinants of winter
mortality. It has been hypothesized that body mass is
an important determinant of winter survival (Stenseth
1978, Hansson 1990, 1995). This hypothesis is based
on empirical studies of northern small mammals show-
ing that individuals seem to adjust their body size to
what is presumably a physiological optimum in terms
of winter survival (e.g., Iverson and Turner 1974, Mer-
ritt and Merritt 1978, Hansson 1990, 1991). In this
study, a similar adjustment was seen in terms of chang-
es in mass in animals that survived the winter: large
animals lost mass, while small animals gained mass.
However, to the best of our knowledge this is the first
demonstration of the expected link between body mass
and winter survival. Individuals that were either large
or very small at the onset of the winter paid a cost in
terms of low winter survival probability. Such indi-
viduals may have died because they failed to adjust
their mass, or they may have paid a cost following mass
adjustment that compromised survival.
We suggest that the higher mortality rate in males
than in females was due to the fact that males over-
wintered at a larger size than did females. Tundra voles
are polygynous and sexually dimorphic with respect to
body size, with breeding males ;30% larger than fe-
males (Bondrup-Nielsen and Ims 1990, Ims 1997).
Since the large size of males is due to sexual selection,
we speculate that the cost males pay in terms of low
winter survival is offset by a reproductive advantage
in the winter if winter breeding takes place or in the
early part of the next breeding season (Hansson 1995),
December 2002 WINTER DEMOGRAPHY OF VOLES
or by a survival advantage due to their large size in
the summer (Boonstra and Krebs 1979).
The individual determinants of winter survival may
interact with population processes in several ways.
First, different winter survival rates of males and fe-
males leads to a seasonally changing sex ratio in the
population. In the tundra vole, the higher mortality rate
in males than in females (which we think is related to
the larger body size in males) produced a more female-
biased sex ratio in the spring than in the autumn. In
some other small rodent species, the sexual size di-
morphism is reversed, i.e., breeding females are larger
than males (Bondrup-Nielsen and Ims 1990). There-
fore, given the kind of size-dependent winter mortality
rate demonstrated here, we may expect seasonal sex
ratio changes opposite to what we found in the tundra
vole. Indeed, both in the wood lemming Myopus schis-
ticolor (Bondrup-Nielsen et al. 1993) and in several
populations of Clethrionomys spp. (Kalela 1971, Yoc-
coz and Mesnager 1998), for which females are larger
than males (Bondrup-Nielsen and Ims 1990), the sex
ratio at the onset of the breeding season in the spring
is often more male biased than it is in autumn.
Second, the mean size of animals in the fall may
depend on factors such as reproductive activity, age
distribution, and population density. In particular, peak
density animals in cyclic populations are typically larg-
er than animals in other phases of the population cycle
(Chitty 1952, Krebs and Myers 1974, Boonstra and
Krebs 1979). Therefore, given that winter survival is
dependent on body size, one could expect peak density
animals to have lower winter survival rates than ani-
mals in other phases of the cycle. Note, however, that
the mean mass of the animals at the onset of winter in
1994 (the year with the highest population density in
the present study) was not higher than in the other years
(29.5 g vs. 30.6 g). Thus, population mean body mass
could not in this instance explain the large yearly dif-
ferences in survival rate over the winter.
CONCLUSION
Due to a standardized study setting with new ex-
perimental populations of tundra voles introduced to
the same 12 habitat patches over four years, we were
able to highlight winter demography. This has until
now been a little explored, but potentially very im-
portant, aspect of the ecology of northern small-mam-
mal populations. We identified both intrinsic and ex-
trinsic determinants of winter demography. Density-
dependent recruitment and body size-dependent sur-
vival probability over the winter contributed to the size
and demographic structure of the populations at the
onset of the breeding season in the spring. However,
in terms of yearly variation in rate of population
change, these intrinsic factors were relatively unim-
portant compared to events with catastrophic, density-
independent mortality that sometimes led to population
extinctions. These population crashes in winter were
3455
most likely climatically driven, and our results support
the idea that climate change, due to an increased fre-
quency in mild weather during the winter, can disrupt
the normal cyclic dynamics of northern populations of
voles and lemmings.
ACKNOWLEDGMENTS
This research was supported by various grants from the
Research Council of Norway. We thank the following people
for constructive comments on the manuscript: Harry P. An-
dreassen, Ottar Bjørnstad, Torbjørn H. Ergon, Karen Hodges,
Xavier Lambin, and two anonymous referees.
LITERATURE CITED
Aars, J., and R. A. Ims. 1999. The effect of habitat corridors
on rates of transfer and interbreeding between vole demes.
Ecology 80:1648–1655.
Aars, J., and R. A. Ims. 2000. Population dynamic and ge-
netic consequences of spatial density-dependent dispersal
in patchy populations. American Naturalist 155:252–265.
Aars, J., E. Johannesen, and R. A. Ims. 1999. Demographic
consequences of movements in subdivided root vole pop-
ulations. Oikos 85:204–216.
Bjørnstad, O. N., N. C. Stenseth, and W. Falck. 1995. A
gradient in small mammal density fluctuations: a statistical
modelling approach. Proceedings of the Royal Society of
London, Series B 262:127–133.
Bondrup-Nielsen, S., and R. A. Ims. 1990. Reversed sexual
size dimorphism in microtines: are females larger than
males or are males smaller than females? Evolutionary
Ecology 4:261–272.
Bondrup-Nielsen, S., R. A. Ims, R. Fredriksson, and K. Fred-
ga. 1993. Demography of the wood lemming (Myopus
schisticolor). Pages 493–507 in N. C. Stenseth and R. A.
Ims, editors. The biology of lemmings. Academic Press,
London, UK.
Boonstra, R., and C. J. Krebs. 1979. Viability of large- and
small-sized adults in fluctuating vole populations. Ecology
60:567–573.
Boonstra, R., and F. H. Rodd. 1983. Regulation of breeding
density in Microtus Pennsylvanicus. Journal of Animal
Ecology 52:757–780.
Bronson, F. H., and M. C. Kerbeshian. 1995. Reactions of
reproductively photoresponsive versus unresponsive mead-
ow voles to simulated winter conditions. Canadian Journal
of Zoology 73:1479–1488.
Chitty, D. 1952. Mortality among voles (Microtus agrestis)
at Lake Vyrnwy, Montgomeryshire, in 1936–9. Philosoph-
ical Transaction of the Royal Society of London, Series B
236:505–552.
Dark, J. 1983. Short photoperiods reduce winter energy re-
quirements of the meadow vole, (Microtus pennsylvanicus).
Physiology and Behavior 31:699–702.
Gundersen, G., J. Aars, H. P. Andreassen, and R. A. Ims.
2001. Inbreeding in the field: an experiment on root vole
populations. Canadian Journal of Zoology 79:1901–1905.
Hansen, T. F., N. C. Stenseth, and H. Henttonen. 1999. Mul-
tiannual vole cycles and population regulation during long
winters: an analysis of seasonal density dependence. Amer-
ican Naturalist 154:129–139.
Hanski, I., and H. Henttonen. 1996. Predation on competing
rodent species: a simple explanation of complex patterns.
Journal of Animal Ecology 65:220–232.
Hanski, I., P. Turchin, E. Korpimäki, and H. Henttonen. 1993.
Population oscillations of boreal rodents: regulation by
mustelid predators leads to chaos. Nature 364:232–235.
Hansson, L. 1984. Winter reproduction of small mammals in
relation to food conditions and population dynamics. Pages
225–234 in J. F. Merritt, editor. Winter ecology of small
3456 JON AARS AND ROLF A. IMS
mammals. Carnegie Museum of Natural History, Pitts-
burgh, Pennsylvania, USA.
Hansson, L. 1990. Ultimate factors in winter weight depres-
sion of small mammals. Mammalia 54:397–404.
Hansson, L. 1991. Regional and individual variation in body
growth in winter of bank voles Clethrionomys glareolus.
Acta Theriologica 36:357–362.
Hansson, L. 1992. Fitness and life history correlates of
weight variation in small mammals. Oikos 64:479–484.
Hansson, L. 1995. Size dimorphism in microtine rodent pop-
ulations: characteristics of growth and selection against
large-sized individuals. Journal of Mammalogy 76:867–
872.
Hansson, L. 1999. Intraspecific variation in dynamics: small
rodents between food and predators in changing land-
scapes. Oikos 86:159–169.
Hansson, L., and H. Henttonen. 1988. Rodent dynamics as
community processes. Trends in Ecology and Evolution 3:
195–200.
Ims, R. A. 1997. Determinants of geographic variation in
growth and reproductive traits in the root vole. Ecology
78:461–470.
Ims, R. A., and H. P. Andreassen. 1999. Effects of experi-
mental habitat fragmentation and connectivity on root vole
demography. Journal of Animal Ecology 68:839–852.
Ims, R. A., and H. P. Andreassen. 2000. Spatial synchroni-
zation of vole population dynamics by predatory birds. Na-
ture 408:194–196.
Iverson, S. L., and B. N. Turner. 1974. Winter weight dy-
namics in Microtus pennsylvanicus. Ecology 55:1030–
1041.
Kalela, O. 1971. Seasonal trends in the sex ratio of the grey-
sided vole, Clethrionomys rufocanus (Sund). Annales Zool-
ogici Fennici 8:452–455.
Karels, T. J., and R. Boonstra. 2000. Cocurrent density de-
pendence and independence in populations of arctic ground
squirrels. Nature 408:460–463.
Krebs, C. J. 1993. Are lemmings large Microtus or small
reindeer? A review of lemmings after 25 years and rec-
ommendations for future work. Pages 247–260 in N. C.
Stenseth and R. A. Ims, editors. The biology of lemmings.
Academic Press, London, UK.
Krebs, C. J., and J. H. Myers. 1974. Population cycles in
small mammals. Advances in Ecology Research 8:267–
399.
Lebreton, J.-D. 1991. Modeling density dependence, envi-
ronmental variability, and demographic stochasticity from
population counts: an example using Wytham Wood great
tits. Pages 89–102 in J. Blondel, A. Gosler, J.-D. Lebreton,
and R. McCleery, editors. Population biology of passerine
birds. Springer-Verlag, Berlin, Germany.
Leirs, H., N. C. Stenseth, J. D. Nichols, J. E. Hines, R. Ver-
hagen, and W. Verheyen. 1997. Stochastic seasonality and
nonlinear density-dependent factors regulate population
size in an African rodent. Nature 389:176–180.
Lindström, E., and B. Hörnfeld. 1994. Vole cycles, snow
depth and fox predation. Oikos 70:156–160.
Malcolm, J. R., and R. J. Brooks. 1993. The adaptive value
of photoperiod-induced shape changes in the collared lem-
ming. Pages 311–328 in N. C. Stenseth and R. A. Ims,
Ecology, Vol. 83, No. 12
editors. The biology of lemmings. Academic Press, San
Diego, California, USA.
Merritt, J. F., and J. M. Merritt. 1978. Population ecology
and energy relationships of Clethrionomys gapperi in a Col-
orado subalpine forest. Journal of Mammalogy 59:576–
598.
Ostfeld, R. S., and C. D. Canham. 1995. Density-dependent
processes in meadow voles: an experimental approach.
Ecology 76:521–532.
Ostfeld, R. S., C. D. Canham, and S. R. Pugh. 1993. Intrinsic
density-dependent regulation of vole populations. Nature
366:259–261.
Reid, D. G., and C. J. Krebs. 1996. Limitations to collared
lemming population growth in winter. Canadian Journal of
Zoology 74:1284–1291.
Spears, N., and J. R. Clarke. 1988. Selection in field voles
(Microtus agrestis) for gonadal growth under short photo
periods. Journal of Animal Ecology 57:61–70.
Steen, H., R. A. Ims, and G. A. Sonerud. 1996. Spatial and
temporal patterns of small-rodent population dynamics at
a regional scale. Ecology 77:2365–2372.
Stenseth, N. C. 1978. Energy balance and the Malthusian
parameter, m, of grazing small rodents. Oecologia 32:37–
55.
Stenseth, N. C. 1999. Population cycles in voles and lem-
mings: density dependence and phase dependence in a sto-
chastic world. Oikos 87:427–461.
Stenseth, N. C., O. B. Bjørnstad, and T. Saitoh. 1998. Sea-
sonal forcing on the dynamics of Clethrionomys rofocanus:
modeling geographic gradients in population dynamics. Re-
searches on Population Ecology 40:85–95.
Stenseth, N. C., and R. A. Ims. 1993. The biology of lem-
mings. Linnean Society Symposium Series. Academic
Press, London, UK.
Tast, J. 1966. The root vole, Microtus oeconomus (Pallas),
as an inhabitant of seasonally flooded land. Annales Zool-
ogici Fennici 3:127–171.
Tast, J. 1984. Winter success of root voles, Microtus oec-
onomus, in relation to population density and food con-
ditions at Kilpisjärvi, Finnish Lapland. Pages 59–66 in J.
F. Merritt, editor. Winter ecology of small mammals. Car-
negie Museum of Natural History, Pittsburgh, Pennsylva-
nia, USA.
Turchin, P., and I. Hanski. 1997. An empirically based model
for latitudinal gradients in vole population dynamics.
American Naturalist 149:842–874.
Turchin, P., and R. S. Ostfeld. 1997. Effects of density and
season on the population rate of change in the meadow
vole. Oikos 78:355–361.
Whitney, P. 1976. Population ecology of two sympatric spe-
cies of subarctic microtine rodents. Ecological Monographs
46:85–104.
Yoccoz, N. G., and R. A. Ims. 1999. Demography of small
mammals in cold regions: the importance of environmental
variability. Ecological Bulletins 47:137–144.
Yoccoz, N. G., and S. Mesnager. 1998. Are alpine voles larger
and more sexually dimorphic because adults survive better?
Oikos 82:85–98.
Yoccoz, N. G., K. Nakata, N. C. Stenseth, and T. Saitoh. 1998.
The demography of Clethrionomys rufocanus: from math-
ematical and statistical models to further field studies. Re-
searches on Population Ecology 40:107–121.