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Can Reindeer Overabundance Causea Trophic Cascade?
Rolf A. Ims,1,2,* Nigel G. Yoccoz,1,2 Kari Anne Brathen,1 Per Fauchald,1,2
Torkild Tveraa,2 and Vera Hausner1
1Department of Biology, University of Tromsø, 9037, Tromsø, Norway; 2Department of Arctic Ecology, NINA, Polar Environmental
Centre 9296, Tromsø, Norway
ABSTRACT
The region Finnmark, in northernmost Europe,
harbors dense populations of semi-domestic rein-
deer of which some exhibit characteristics of
overabundance. Whereas overabundance is evi-
dent in terms of density-dependent reductions in
reindeer body mass, population growth and abun-
dance of forage plants, claims have been made that
this reindeer overabundance also has caused a
trophic cascade. These claims are based on the main
premise that reindeer overgrazing negatively im-
pacts small-sized, keystone tundra herbivores. We
tested this premise by a large-scale study in which
the abundance of small rodents, hares and ptar-
migans was indexed across reindeer management
districts with strong differences in stocking densi-
ties. We examined the scale-dependent relations
between reindeer, vegetation and these small-sized
herbivores by employing a spatially hierarchical
sampling design within the management districts.
A negative impact of reindeer on ptarmigan,
probably as a result of browsing reducing tall Salix,
was indicated. However, small rodents (voles and
lemmings), which are usually the keystone herbi-
vores in the plant-based tundra food web, were not
negatively impacted. On the contrary, there was a
strong positive relationship between small rodents
and reindeer, both at the scale of landscape areas
and local patches, with characteristics of snow-bed
vegetation, suggesting facilitation between Nor-
wegian lemmings and reindeer. We conclude that
the recent dampening of the vole and lemming
population cycle with concurrent declines of rodent
predators in northernmost Europe were not caused
by large herbivore overgrazing.
Key words: tundra; lemming; ptarmigan; facili-
tation; food web; overgrazing; quasi-experiment;
Salix; spatial scaling; growth forms.
INTRODUCTION
Human beings have affected the abundance of
large herbivores since prehistoric times (for exam-
ple, Zimov and others 1995). Because large herbi-
vores often are determinants of ecosystem structure
and function (Cote and others 2004; Danell and
others 2006), the omnipresent strong hu-
man—large herbivore connection represents one of
the most widespread anthropogenic impacts on
ecosystems. There is a long and voluminous re-
search record on the ecology of large herbivores of
which most studies have focused on direct trophic
relations, that is, plant—herbivore or herbivore-
carnivore interactions. Recently, the scope has
been extended to emphasize the role of large her-
bivores as a key intermediate link between plants
and predators in a linear food chain context, in
particular, to establish whether large herbivores
can convey bottom–up or top–down trophic cas-
cades (Ripple and Beschta 2005; Pringle and others
2007). However, ecosystems typically consist of
several interconnected food chains forming com-
Received 21 July 2006; accepted 2 February 2007; published online 18
July 2007.
*Corresponding author; e-mail: [email protected]
Ecosystems (2007) 10: 607–622DOI: 10.1007/s10021-007-9060-9
607
plex, non-linear food webs (Paine 1980) in which
small-sized herbivores may play key roles. This
opens the possibility for interactions between dif-
ferent functional groups of herbivores (that is,
small and large) and possibilities for other, less
obvious cascades, which ultimately may result from
management of large herbivores (Suominen and
Danell 2006).
Reindeer (or caribou) are the most widespread
and abundant large herbivores in tundra ecosys-
tems, where they usually co-occur with a restricted
assemblage of smaller herbivores, composed of
small rodents (voles and lemmings), hares, geese
and ptarmigans (Bliss and others 1973). Due to
naturally low population densities and a vagrant
life style, with exploitation of available pulses of
plant production in space and time, reindeer are
usually thought to have little impact on vegetation
and other ecosystem components (Jefferies and
others 1994; Chernov and Matveyeva 1997). In
contrast, small rodents (especially lemmings) usu-
ally form the key link in the tundra food web in
terms of strong impacts on vegetation, other her-
bivores and predators (Elton 1942; Batzli 1975;
Batzli and others 1980; Finerty 1980; Krebs and
others 2003; Ims and Fuglei 2005). However,
exceptions to the prime ecosystem role of small
tundra rodents occur, for instance, when human
interventions cause overabundance of other her-
bivores (Jefferies and others 1994). The emergent
overabundance of geese on the coastal tundra in
Arctic America is one such exception (Jano and
others 1998; Jefferies and Rockwell 2002). Another
case, which we consider in the present paper,
concerns semi-domestic reindeer in the region of
Finnmark, northern-most Europe. In Finnmark
reindeer have peaked to density levels claimed as
‘‘an ecological disaster‘‘ (Moen and Danell 2003).
Strong direct impacts of reindeer on vegetation in
Finnmark have been demonstrated (Suominen and
Olofsson 2000; Brathen and Oksanen 2001; Bra-
then and others, (in press). Severe plant resource
limitation may then in turn impact other herbi-
vores and ultimately their predators. Indeed, such
cascading effects of reindeer overabundance have
been suggested by several authors to explain recent
severe population declines of predators depending
on small tundra herbivores such as small rodents
and ptarmigan (Tømmeraas 1993; Kjellen and Roos
2000; Angerbjorn and others 2001; Ratcliffe 2005).
However, as yet there are no published empirical
studies that can substantiate these suggestions.
In fact, there seems to be a general scarcity of
studies that have addressed impacts of large un-
gulates on smaller vertebrate herbivores (see Su-
ominen and Danell 2006 for a review). One reason
for this may be that such studies must encompass
spatial scales exceeding the logistic capabilities of
most experimental designs. Even for voles and
lemmings, that have relative small-scale space use,
studies addressing population level responses are
likely to require landscape-scale consideration
(Wiens and others 1993; Barrett and Peles 1999;
Hansson 2002). Moreover, when assessing the
impacts of wide-ranging, large ungulates such as
reindeer adequate study designs probably require
regional extents (Senft 1987). For instance, enclo-
sure studies typically obstruct normal foraging
patterns in large ungulates (Suominen and Danell
2006) and population processes in small mammals
(Krebs and others 1969).
In the present study, we evaluate the basic pre-
mise that high densities of semi-domestic reindeer
have resulted in a trophic cascade, that is, high
reindeer abundance negatively impacts small-sized
tundra herbivores by overgrazing their food re-
source. In Finnmark reindeer are managed in large,
separate summer pasture districts, often with per-
manent, strongly differing densities between
neighboring districts. Strong, negative spatial den-
sity-dependent effects on reindeer productivity and
sensitivity to severe winter climate (Fauchald and
others 2004; Tveraa and others 2007) and on plant
abundance (Brathen and others, in press) are evi-
dent among the districts. The term ‘‘deer over-
abundance‘‘ (sensu Caughley 1981; Cote and
others 2004) is therefore justified for characterizing
districts with the highest stocking densities. By
choosing ten replicate pairs of neighboring herding
districts with contrasting stocking densities, we
were able to establish an extraordinary large-scale,
quasi-experimental study design. Herbivore abun-
dance was indexed based on recordings of feces and
grazing signs. Thus inferences about the impacts of
reindeer density on the abundance of other tundra
herbivores, and whether this impact covaried with
the abundance of important plants, could be made
at level of herding districts. As our sampling was
done according to a spatially hierarchical design
within the herding districts, we also assessed the
spatial scale-dependent nature of the relations
between reindeer, small tundra herbivores and
vegetation.
MATERIAL AND METHODS
Focal Ecosystem
The study region is coast-near alpine tundra in
Finnmark at 70�N. This region forms the north-
608 R. A. Ims and others
ernmost tip of the European continent, delineated
by the Barents Sea towards the north and by birch
forests and continuous, coniferous taiga towards
the south. Coastal eastern Finnmark has either no
forests (exposed sites) or a forest limit of mountain
birch Betula pubescens at 100–150 m a.s.l. (more
sheltered sites), whereas the forest line in the cli-
matically more benign western parts is at 300–
500 m a.s.l. (Oksanen and Virtanen 1995; Moen
1999). The zonal vegetation we focus on in the
present study, the low alpine tundra, is dominated
by shrub tundra (Walker and others 2005). The
coastal tundra in Finnmark forms important sum-
mer pastures for reindeer (Rangifer tarandus taran-
dus). Other widespread herbivores are ptarmigan
(Lagopus spp.), hare (Lepus timidus) and small ro-
dents such as Norwegian lemming (Lemmus lem-
mus) and gray-sided vole (Clethrionomys rufocanus).
Other large herbivores that may occur locally in-
clude moose (Alces alces) and sheep (Ovis abies), but
these were rarely observed in the present study.
Reindeer have been present in Finnmark since
the area was deglaciated 10,000–15,000 BP (Sko-
gland 1994). Like tundra reindeer elsewhere in the
Arctic, herds migrate seasonally between inland
winter pastures and coastal summer pastures. Since
the sixteenth century, reindeer herds in Finnmark
have become semi-domesticated and are currently
managed entirely by the indigenous Sami people,
but maintaining the seasonal migration pattern
(Muga 1986). However, in contrast to the pristine,
unmanaged situation several severe range restric-
tions have taken place. The summer pastures are
now split into many separate management districts,
which are delineated by coastlines and reindeer
fences. These fairly large summer pasture districts
(range: 188–2,733 km2 for districts included in the
present study), constitute the basic unit within the
Norwegian husbandry management regime. Rein-
deer densities and reindeer weights at the district
level are recorded annually by the Norwegian
Reindeer Husbandry Administration, and are
available for the last 2–3 decades. Recent analyses
of these data (Fauchald and others 2004; Tveraa
and others 2007) show that although there have
been strong temporal fluctuations in densities with
some districts peaking to more than 20 reindeer/
km2, there are spatial contrasts between neigh-
boring districts, both with respect to reindeer den-
sity and calf weights, that have persisted for at least
two decades. Moreover, these contrasts give rise to
a strong negative spatial density-dependence in calf
weight and thus production (Figure 1). This nega-
tive density-dependence probably results from the
deteriorated quality of pastures in the high-density
districts (Brathen and others, in press) and we
hypothesize that this also may have affected other
herbivores.
In terms of biomass, reindeer are clearly the
dominant herbivore in some of the districts with
the highest average density (>10 reindeer/km2).
For instance, 10 reindeer/km2 with average indi-
vidual body masses of 50 kg corresponds to
approximately 10,000 lemmings/(or 100 lem-
mings/ha) (assuming a mean lemming body mass
of 50 g) or 1000 ptarmigans (assuming ptarmigan
body mass of 500 g). This is clearly more than the
observed peak densities of lemming or voles
(Stenseth and Ims 1993) or ptarmigan (Pedersen
and others 2004) in these tundra habitats. Despite
the lower biomass of the small herbivores com-
pared to reindeer the food web impact of rodents
may still be larger due to the higher metabolism
and secondary productivity of small herbivores
(Batzli 1975; Batzli and others 1980). Compared to
figures on the average biomass of wild ungulates in
the North American tundra, ranging between 0.17
and 3 kg/km2 (Bliss and others 1973), the current
situation in Finnmark appears to be abnormal.
Study Design
We employed a quasi-experimental study design
(Shadish and others 2002) for estimating the effects
of reindeer density by using neighboring districts
Figure 1. The relationship between reindeer density per
km2 and weight of slaughtered calves in the twenty
reindeer districts. Lines connect districts within 10 pairs
with contrasting densities (see Figure 2). Estimates of
yearly reindeer density and calf weights are averaged
over a 23-year period using the official statistics of the
Norwegian Reindeer Management Authorities.
Impacts of Reindeer Overabundance 609
with temporally persistent contrasts in reindeer
density. Pairs of such neighboring districts were
treated as ‘‘block units‘‘ in the design (and in the
statistical analysis), enabling us by design to control
for environmental factors (that is, geology, climate)
that vary on a large spatial scale. We paired
neighboring summer pasture districts based on the
criteria that a high-density district had over the two
last decades consistently lower calf weights and
higher reindeer density than the neighboring low-
density district with which it was paired (Figure 1).
Ten district pairs conformed to both criteria and
were included in the study (Figure 2), representing
more than half of the available summer grazing
areas in Finnmark. On average the reindeer density
in high-density districts was more than twice as
high as in the low-density districts (density ratio
high:low within pairs for period 1981–2003:
2.63 ± 0.70 [se]).
The selected summer districts represent large,
heterogeneous areas and we aimed at a sampling
design within districts that with a realistic effort
could achieve a balance between coverage and a
focus on areas of assumed highest importance as
pasture for reindeer. With respect to coverage we
assured that sampling units were drawn from sep-
arate siida regions (that is, areas belong to separate
cooperative groups of Sami herders within districts)
and different geographic regions (that is, based on
topographic features such as valleys, peninsulas
and mountain ranges) within the districts. Often
such geographical and social regions coincided. As
we expected to find the strongest evidence for food
web interactions in the vegetation strata where
herbivores concentrate their activities, we re-
stricted our sampling to strata within the low-al-
pine zone that had the most mesic and wet
vegetation types. These strata represent the most
Figure 2. The hierarchical
sampling design of the study.
The map shows the
delineation of the summer
herding districts forming the
10 pairs with contrasting
reindeer densities. An arrow
connects the two districts of
each pairs. The location of the
6–14 landscape areas of 2 · 2
km within the district pairs
are shown as small gray
squares. The landscape areas
are further subdivided into a
grid of 100 quadrates from
which a random subsample
(shaded quadrates) was
chosen. Within each selected
quadrate there is a 50 m
sampling line running from
the middle of the quadrate
towards a random position.
Plots (n = 11) were
established at 5 m intervals
along the sampling line. In
each plot fecal pellets or
grazing signs of the focal
herbivores were recorded
inside a triangle with 40 cm
sides. Plant abundance was
quantified by the number of
intercepts with pins attached
in each corner of the triangle.
610 R. A. Ims and others
productive tundra habitats in terms of plant pro-
ductivity. Dryer vegetation types have generally
very sparse vegetation and offer too little food and
vegetation cover to be important, in particular, for
the smaller herbivores in question. Vegetation
strata were delineated based on satellite images and
ERDAS GIS software (ERDAS 2003) and previous
classifications of vegetation types in Finnmark
(Johansen and others 1995). The stratification and
selection procedures were as follows: A 2 · 2 km
grid of landscape areas was superimposed on the
areas of the district situated in the low alpine zone.
Next we identified landscape areas with more than
average amounts of mesic and wet vegetation for
the district. Finally, we discarded landscape areas
that included more than 50% forest, lakes, sea,
glaciers or included a major road, because such
factors may influence the presence of reindeer
independently of pasture quality. The remaining
stratum fulfilling the above criteria was then sub-
jected to random selection of landscape areas with
the restriction that there should be a minimum of
two areas within each siida/geographic region per
district. Above this minimum the number of se-
lected landscape areas increased with the area of
the focal stratum of the region. The number of se-
lected landscape areas per district then varied be-
tween 6 and 14 (Table 1). All landscape areas of a
district pair were sampled within the same time-
period during July and August in the year 2003,
and two persons analyzed most landscape areas in
one day. Districts belonging to the same district pair
were sampled simultaneously. Two initially se-
lected landscape areas were not accessible due to
very steep terrain, and other randomly chosen
landscape areas replaced them both.
The selected 2 · 2 km landscape areas were
further subdivided into1000.04 km quadrates
among which 25 were randomly selected (Fig-
ure 2). The center of each selected area was a start
position for a sampling line, the direction of which
was given by a random GPS position on a circle
with a 50 m radius from the center. The sampling
lines were sub-sampled at plots every 5 m along
the line with a triangular frame with sides of
40 cm (Figure 2).
If a part of a sampling line had to be discarded,
that is, because of terrain or wetness (lake, large
river or very wet mire), snow cover (more than a
5 m section running through snow), large boulder
field (more than half of the sampling line running
over boulders void of vegetation), or the sample
line was below the tree line, a new sampling line
was randomly selected from the same position or
new position. If no new acceptable start position
was found, the sampling square was discarded.
Most rejections were caused by sampling squares
located below the tree-line and most often this
occurred in districts of low reindeer densities. Still
this did not appear to cause any major difference in
the altitude of sampling lines between high and
low-density districts (average altitude in high-
density districts: 396.9 ± 34.1 m a.s.l., in low den-
sity districts: 374.9 ± 38.2 m a.s.l.). Overall the
numbers of landscape areas and sampling lines
were similar in low and high-density districts
(Table 1).
Indices of Herbivore Abundance andHabitat Variables
Because herbivores produce conspicuous feces in
the form of relatively large-sized pellets (or pats),
the frequency of fecal pellets can be used success-
fully as indices of abundance (Neff 1968; Putman
1984). In the present study we recorded the pres-
ence–absence of fecal pellets of hares (Hulbert and
others 1996), ptarmigan (compare Schaefer and
others 1996) and reindeer (Edenius and others
2003; Van der Wal and Brooker 2004) in the tri-
angular plots along the sampling lines (Figure 2).
The two ptarmigan species present in the region,
the willow ptarmigan (L. lagopus) and the rock
ptarmigan (L. mutus), cannot be distinguished
based on fecal pellet morphology. Small rodents
(vole and lemming) pellets are more difficult to
detect due to their small size and we therefore re-
corded, as presence or absence, the much more
conspicuous signs of rodent grazing activity (cut
vegetation, runways and burrows) in the plots.
Table 1. Numbers of Surveyed Landscape Areasand Sampling Lines in High and Low Density Dis-tricts in the 10 District Pairs (see Figure 1)
Landscape
areas
Sampling lines
District pair Low High Low High
1 6 7 52 50
2 5 6 35 41
3 6 6 78 84
4 8 8 67 79
5 7 6 37 59
6 8 6 40 83
7 7 7 63 81
8 10 8 76 89
9 10 7 124 106
10 9 14 78 132
SUM 76 75 650 804
Impacts of Reindeer Overabundance 611
Previous studies using similar methodology have
shown that such small rodent activity indices are
proportional to local abundance (Lambin and oth-
ers 2000). The different small rodents species can-
not be identified with certainty based on such
activity signs. However, the dominant species in
the study regions are usually the gray-sided vole
and the Norwegian lemming (N.G.Yoccoz and
R.A Ims, unpublished).
Vole and lemming populations in Finnmark ex-
hibit 4–5 years population density cycles (Ekerholm
and others 2001; Angerbjorn and others 2001),
which are fairly synchronized across species and
geographic areas (Hansson and others 1978; Chris-
tiansen 1983; Yoccoz and Ims 2004). Accordingly
the abundance in a particular year will depend on
the cyclic phase. The results from an ongoing large-
scale monitoring program based on live-trapping
(Yoccoz and Ims 2004) showed that small rodent
peak densities were attained in the fall of 2002 in
the entire region, and that the populations had
crashed to very low densities by the spring of 2003.
Thus signs of small rodent activity observed during
our field campaign in summer 2003 originated
mainly from the preceding winter period and thus
reflect spatial variation in rodent densities at the
culmination of the peak phase. Because food limi-
tation in small rodents is expected to kick in at the
culmination of the peak phase (Turchin and Batzli
2001), the timing of our study was ideal with re-
spect to testing for effects of reindeer overabun-
dance on small rodent populations.
Although activity signs of small rodents last for
less than a year, pellets of the larger herbivores may
last for a longer time period. Thus the prevalence of
fecal pellets must be taken as an index of cumula-
tive use, especially by reindeer. Of concern here is
that the spatial distribution of feces actually reflects
feeding patterns. Previous studies of other deer
species have shown that this indeed is the case
(Putman 1984; Schutz and others 2006). The dif-
ference in the recorded frequency of reindeer pel-
lets between the high and low-density district
(within pairs) was consistent with the correspond-
ing long-term difference based on yearly reindeer
counts obtained from official statistics (Figure 3).
During sampling we quantified the abundance of
plants with the point intercept method (Jonasson
1988; Frank and McNaughton 1990; Brathen and
Hagberg 2004) by registering the number of inter-
cept of plants with three pins forming the corners
of the triangular frame (Figure 2). For a given
growth form the number of point intercepts is
proportional to biomass (Brathen and Hagberg
2004). For bryophytes only one intercept per pin
was registered, hence bryophyte cover rather than
abundance was estimated. One side (that is, two
pins) of the triangle was placed exactly parallel to
the left side of a measurement ribbon running from
the start to the end position of the sampling line
(Figure 2). For the purpose of the present study we
focus on 11 vascular plant species or growth forms
and two bryophyte growth forms (Table 2). The
separate species were dominant plants, whereas
less common species were grouped according to
growth form. Although growth forms account for
the main structure of the vegetation, they are also
indicators of ecosystem function, that is, they cor-
relate with plant functionality (for example, Cha-
pin and others 1996), and represents important
forage items and habitat indicators for herbivores.
We recorded topographical variables supposed to
be important to herbivores, that is, altitude, slope
and an index of terrain ruggedness (Neteler and
Mitasova 2002), at the level of quadrates by
extracting this information from a terrain model
with a spatial resolution of 25 · 25m.
Statistical Analysis
Separate statistical analyses were done at three
spatial scales in the hierarchical sampling design;
Figure 3. The relationship between reindeer density per
km2 and the frequency of plots (within sampling lines)
with reindeer feces. Lines connect districts within the 10
pairs with contrasting densities (see Figure 2). Estimates
of yearly reindeer density and calf weights are averaged
over a 23-year period using the official statistics of the
Norwegian Reindeer Management Authorities, whereas
the estimate of feces frequency was obtained in 2003
according to our study design (see main text). District
pair 6 had a reversed density of reindeer in 2003 com-
pared to the long-term average (Anonymous 2004).
612 R. A. Ims and others
that is, the scales of sampling lines, landscape areas
and herding districts (Figure 2). The smallest spatial
scale (that is, the plots within sampling lines) was
not considered, because the frequencies of herbi-
vore recordings were too low at this scale to allow
for robust analyses.
At the largest scale (that is, the herding districts)
we used the power of our quasi-experimental de-
sign to assess the impacts of long-term spatial
contrast in reindeer stocking densities on the in-
dexed abundance of the other herbivores (that is,
small rodents, ptarmigans and hares). The size of
the effect of reindeer abundance was estimated as
nominal contrasts (that is, differences) between the
high and low-density districts within pairs. In this
analysis the response variables (indexed herbivore
abundance) were the frequency of plots per sam-
pling line with recordings of the herbivores aver-
aged over all sampling lines and landscape areas in
the districts. Thus the 20 herding districts were the
quasi-experimental units (that is, replicates). Dis-
trict pair was included as a random (that is,
‘‘block‘‘) effect in a mixed linear model framework
(Pinheiro and Bates 2000), whereas the three
topographical variables (altitude, slope and rug-
gedness) were entered as district level average
values.
For the two smaller spatial scales considered (that
is, landscape areas and sampling lines), we used
linear mixed models to predict frequencies of small
rodents, ptarmigans and hares (response variable)
as a function of reindeer abundance as indexed by
the pellet recordings (predictor variable). In these
models the abundance of the 13-plant species/
growth forms (Table 2) and the three topographical
variables (see above) were included as covariates.
At both scales, both the response (that is, indexed
herbivore abundance, see above) and predictor
variables were quantified at the sampling line level.
Plant predictors were quantified as the number of
point intercepts per line and a log (x + 1) trans-
formation was used to meet the requirements of
linear modelling (that is, linear relationships and
adequate spread of predictor values). At the land-
scape level, average values based on all sampling
lines were used. Levels above in the sampling
hierarchy (districts for landscape areas, whereas
districts and landscape areas for lines) were mod-
elled as random effects. To be able to compare the
estimates across species and scales we used a ‘‘full
model‘‘ with all predictor variables included in all
analyses. Eventual non-linear relations were con-
sidered by using additive models (Wood 2006) and
when present they were adequately described by
second order polynomial terms. The significance of
model parameters was assessed according to their
95% confidence intervals. The residuals of all
models were checked and found to satisfactorily
meet the assumptions of linear models (stable
variance and no spatial auto-covariance).
RESULTS
Overall Abundance and Distribution ofHerbivores
Table 3 summarizes the average indexed abun-
dance of the recorded herbivores at the four levels
in our hierarchical sampling design, whereas Fig-
ure 4 depicts the spatial distribution of recordings at
the landscape level. Reindeer were the most fre-
quently recorded herbivore followed by small ro-
dents, ptarmigans and hares (Table 3). In particular
reindeer, but also small rodents were widely dis-
tributed (Figure 4) with at least 2/3 of the landscape
areas recording their presence (Table 3). Ptarmigans
and in particular hares, had a more occasional
representation on the landscape scale (Figure 4)
and hares were the only herbivore missing from a
fraction of the herding districts (Table 3).
Impacts of Reindeer Stocking DensitiesAcross Herding Districts
At the spatial scale of herding districts we evaluated
the potentially negative impact of reindeer stocking
density on the abundance of other herbivores by
Table 2. The Overall Abundance of Plant Speciesor Growth Forms used as Predictors in the Statis-tical Models of Herbivore Abundance at the Scale ofLandscape Areas and Sampling Lines
Plant species/growth form Estimate (SE)
Mat grass (Nardus stricta) 2.08 (0.41)
Grasses (other) 7.82 (1.53)
Sedges 5.43 (0.49)
Small dicotyledons 2.93 (0.63)
Bilberry (Vaccinium myrtillus) 3.55 (0.41)
Deciduous ericoids (other) 5.62 (0.52)
Crowberry (Empetrum nigrum
ssp. hermaphroditum)
10.23 (0.61)
Evergreen ericoids (other) 3.15 (0.57)
Tall Salix 0.31 (0.11)
Prostrate Salix 2.03 (0.22)
Dwarf birch (Betula nana) 4.92 (1.29)
Acrocarp mosses 8.36 (0.72)
Pleurocarp mosses 3.32 (0.55)
The abundance estimates are expressed as the mean number of point intercepts(standard error in parentheses) per sampling line. Nomenclature follows Lid andLid (2005).
Impacts of Reindeer Overabundance 613
means of nominal contrasts; that is, estimated dif-
ferences in the indexed abundance between high
and low-density districts within the 10 pairs. There
was a negative effect of reindeer stocking density
on the abundance of ptarmigan, as the effect size
was large relative to the reference level, but the
confidence interval was too wide to warrant a firm
conclusion (Table 4). For hares the effect estimate
was also negative, but much smaller and more
uncertain than for ptarmigans. For small rodents,
which were generally much more abundant and
widespread than hares and ptarmigans, the contrast
estimate indicated that there was no evidence for a
biologically significant effect of reindeer stocking
density.
Spatial Scale Dependent Relations withinHerding Districts
At the two smaller spatial scales (that is, landscape
areas within herding districts and sampling lines
within landscape areas) we assessed the relations
between small rodent, ptarmigan and hare abun-
dance as response variables, and reindeer abun-
dance, vegetation variables and topographical
variables as predictors. At both spatial scales, but
most strongly at the landscape scale, the abun-
dance of small rodents showed a distinct non-
linear, positive relation to reindeer abundance as
modeled by a second-order polynomial (Table 5;
Figure 5). Small rodent abundance was also re-
lated to several vegetation variables, in particular
at the scale of sampling lines. At the sampling line
scale small rodent abundance increased with
increasing cover of pleurocarp mosses, with
increasing abundance of prostrate Salix and small
dicotyledons, whereas the effects of sedges and
most strongly crowberry Empetrum nigrum ssp.
hermaphroditum were negative (Table 5). The
strong negative relation between small rodents
and crowberry was also clearly evident at the scale
of landscape areas. In addition the abundance of
small rodents increased with the abundance of
dwarf birch at the landscape scale.
The abundance of hares and ptarmigans was not
significantly related to reindeer abundance at the
Table 3. The Proportion of Sampling Units with Recorded Presence of Herbivores according to the FourLevels in the Hierarchical Study Design (Figure 1)
Herbivore Spatial scale
Plots (n = 15,959) Lines (n = 1,454) Landscapes (n = 151) Districts (n = 20)
Reindeer (%) 7.53 43.8 87.4 100
Small rodents (%) 3.37 19.3 66.9 100
Ptarmigan (%) 0.58 5.2 39.7 100
Hare (%) 0.19 2.0 14.6 60
Figure 4. A bubble plot
showing the spatial
distribution of indexed
herbivore abundance at the
scale of landscape areas. The
sizes of bubbles are
proportional to the number
of plots per sampling line
with recorded presence of an
herbivore. Points denote
landscapes without recorded
presence of herbivores.
Coordinates are in UTM Zone
33.
614 R. A. Ims and others
spatial scales of landscape areas or sampling lines.
At the scale of sampling lines, both hares and
ptarmigans exhibited a positive association with tall
Salix shrubs (Table 5). This relation was also evi-
dent at the landscape scale for hares, whereas it was
no longer significant for ptarmigans at this scale.
Ptarmigans were most frequently recorded at high
altitude sampling lines within landscapes.
A separate analysis of indexed abundance of
reindeer against topography and plant variables
revealed that reindeer abundance could be pre-
dicted by several plant variables at the scale of
sampling lines, whereas only altitude appeared to
be a significant predictor at the landscape scale
(Table 6). Among the most influential predictor
variables at the line scale prostrate Salix and pleu-
rocarp mosses were positively related to reindeer
abundance, whereas tall Salix and reindeer abun-
dance exhibited a negative association.
DISCUSSION
The particular management setting in Finnmark
with persistent differences in reindeer stocking
densities between neighboring summer herding
districts provided an ample opportunity for assess-
ing the impact of reindeer overabundance on other
tundra herbivores. Concordant evidence for rein-
deer overabundance was available in terms of
strong spatial density-dependence in reindeer body
mass and climate-sensitive demography (Fauchald
and others 2004; Tveraa and others 2007) and in
terms of negative grazing impact on vegetation
(Brathen and Oksanen 2001; K.A. Brathen and
others, in press). On this basis we could evaluate
the claim that plant resource deterioration due to
reindeer overabundance limits the abundance of
other tundra herbivores and eventually the wider
(that is, cascading) consequences of this at the
ecosystem level.
The strongest inference about the impact of
reindeer could be made at the scale of herding
districts due to the quasi-experimental layout of
paired high-density and low-density summer pas-
ture districts. A negative impact of a high reindeer
stocking density was indicated for ptarmigans at
this scale. Although the effect estimate was some-
what uncertain in a statistical sense, its biological
significance was underpinned by the significance of
tall Salix shrubs in the relation between reindeer
and ptarmigans. Within the districts there was a
negative association between the abundance of
reindeer and tall Salix shrubs. This association is
consistent with the strong negative effects of rein-
deer summer browsing on tall Salix found in several
previous studies (Ouellet and others 1994; Man-
seau and others 1996; den Herder and others
2004). On the other hand there was a positive
association between ptarmigan and tall Salix. The
willow ptarmigan L. lagopus is strongly dependent
on Salix (willow) shrubs both as forage and habitat
structure providing cover on the otherwise barren
tundra, especially in winter (Andreev 1988).
Accordingly, van Herder and others (2004) pre-
dicted that willow ptarmigan should be one of the
most vulnerable herbivore species to reindeer
overabundance due to the strong negative effect of
reindeer browsing on the growth and distribution
of tall Salix. Our study is the first to provide
empirical results in support for this prediction.
Hares were also associated with tall Salix shrubs
within the reindeer herding districts, as could be
expected based on prior knowledge about food and
habitat selection for the mountain hare (for
example, Pullianen and Tunkkari 1987). Conse-
quently, hares and ptarmigan have been found to
be positively associated in the arctic tundra (Klein
and Bay 1994; Schaefer and others 1996). How-
ever, although the effect of the high reindeer
stocking density was negative, as could also be
Table 4. Estimated Effects of High Reindeer Density on Other Herbivores at the Herding District Level
Herbivore Estimate With covariates Without covariates
Small rodents Reference (low density) 0.400 [0.200, 0.600] 0.350 [0.190, 0.510]
Effect of reindeer density ) 0.037 [)0.213, 0.139] ) 0.019 [)0.193, 0.155]
Ptarmigan Reference (low density) 0.047 [0.004, 0.090] 0.081[0.055, 0.107]
Effect of reindeer density ) 0.030 [)0.063, 0.003] )0.029 [)0.064, 0.006]
Hare Reference (low density) 0.052 [0.028, 0.076] 0.030 [0.012, 0.048]
Effect of reindeer density )0.007 [)0.027, 0.013] )0.012 [)0.039, 0.015]
The effect size is the difference in frequency of plots with recorded presence of herbivores between districts (within pairs) with high and low reindeer density. The reference level is theestimated frequency of plots with herbivore recording in districts with low reindeer density. Estimates both from models with and without topographical covariates are given and thereference levels for the models with covariates are adjusted to the mean of the covariate values of each district. Uncertainty estimates in brackets are 95% confidence intervals.
Impacts of Reindeer Overabundance 615
Tab
le5.
Th
eC
oeffi
cien
ts(±
95%
CI)
of
the
Models
of
Indexed
Herb
ivore
Abu
ndan
ceat
the
Sca
les
of
Lan
dsc
ape
Are
as
an
dSam
plin
gLin
es
as
aFu
nct
ion
of
Indexed
Rein
deer
Abu
ndan
ce,
Pla
nt
Abu
ndan
cean
dTopogra
ph
ical
Vari
able
s
Pre
dic
tor
vari
ab
leS
mall
rod
en
tsP
tarm
igan
Hare
Lin
eL
an
dsc
ap
eL
ine
Lan
dsc
ap
eL
ine
Lan
dsc
ap
e
Inte
rcept
0.2
31
[)0.0
33,
0.4
94]
0.1
67
[)0.3
78,
0.7
16]
0.0
11
[)0.0
57,
0.0
79]
0.0
36
[)0.1
60,
0.2
33]
)0.0
16
[)0.0
54,
0.0
22]
)0.0
42
[)0.1
28,
0.0
43]
Rein
deer
abu
ndan
ce0.0
22
[)0.0
56,
0.0
99]
)0.1
90
[)0.4
39,
0.0
60]
)0.0
05
[)0.0
17,
0.0
08]
)0.0
21
[)0.0
57,
0.0
14]
0.0
01
[)0.0
05,
0.0
08]
0.0
04
[)0.0
09,
0.0
18]
Rein
deer
abu
ndan
ce^
20.0
30
[0.0
16,
0.0
43]
0.1
57
[0.0
82,
0.2
32]
--
--
Mat
gra
ss)
0.0
08
[)0.0
66,
0.0
50]
0.0
31
[)0.0
98,
0.1
61]
0.0
01
[)0.0
18,
0.0
21]
0.0
21
[)0.0
25,
0.0
68]
0.0
04
[)0.0
07,
0.0
14]
0.0
03
[)0.0
15,
0.0
21]
Gra
sses
(oth
er)
0.0
10
[)0.0
42,
0.0
62]
)0.0
37
[)0.1
94,
0.1
20]
)0.0
05
[)0.0
22,
0.0
13]
0.0
26
[)0.0
30,
0.0
83]
0.0
06
[)0.0
03,
0.0
15]
)0.0
00
[)0.0
22,
0.0
22]
Sedges
)0.0
66
[)0.1
14,)
0.0
18]
0.0
46
[)0.0
77,
0.1
68]
0.0
003
[)0.0
15,
0.0
16]
)0.0
11
[)0.0
55,
0.0
33]
0.0
00
[)0.0
09,
0.0
08]
0.0
09
[)0.0
09,
0.0
26]
Sm
all
dic
oty
ledon
s0.0
92
[0.0
18,
0.1
65]
)0.0
38
[)0.2
19,
0.1
43]
)0.0
31
[)0.0
56,
)0.0
07]
)0.0
61
[)0.1
26,
0.0
04]
)0.0
07
[)0.0
20,
0.0
05]
0.0
06
[)0.0
19,
0.0
31]
Bil
berr
y0.0
29
[)0.0
59,
0.1
17]
0.1
73
[)0.0
68,
0.4
15]
)0.0
19
[)0.0
48,
0.0
10]
)0.0
37[)
0.1
24,
0.0
50]
0.0
00
[)0.0
15,
0.0
15]
0.0
05
[)0.0
29,
0.0
39]
Deci
du
ou
seri
coid
s(o
ther)
)0.0
24
[)0.1
11,
0.0
62]
0.1
00
[)0.1
68,
0.3
69]
0.0
17
[)0.0
11,
0.0
45]
)0.0
10
[)0.1
07,
0.0
86]
)0.0
08
[)0.0
23,
0.0
07]
)0.0
02
[)0.0
40,
0.0
35]
Cro
wberr
y)
0.1
06
[)0.1
67,)
0.0
46]
)0.1
86
[)0.3
51,
)0.0
22]
)0.0
02
[)0.0
22,
0.0
17]
)0.0
40
[)0.0
99,
0.0
19]
0.0
05
[)0.0
05,
0.0
15]
0.0
13
[)0.0
11,
0.0
36]
Everg
reen
eri
coid
s(o
ther)
0.0
32
[)0.0
37,
0.1
00]
0.0
32
[)0.1
80,
0.2
43]
0.0
09
[)0.0
135,
0.0
31]
0.0
12
[)0.0
64,
0.0
88]
0.0
14
[0.0
02,
0.0
25]
0.0
07
[)0.0
23,
0.0
37]
Tall
Sa
lix
)0.0
80
[)0.2
21,
0.0
62]
0.1
24
[)0.0
95,
0.3
43]
0.0
61
[0.0
156,
0.1
07]
0.0
24
[)0.0
54,
0.1
03]
0.0
45
[0.0
21,
0.0
69]
0.0
32
[0.0
02,
0.0
63]
Pro
stra
teS
ali
x0.0
90
[0.0
22,
0.1
59]
0.1
45
[)0.0
05,
0.2
95]
)0.0
02
[)0.0
24,
0.0
20]
0.0
13
[)0.0
41,
0.0
67]
0.0
02
[)0.0
10,
0.0
13]
)0.0
04
[)0.0
25,
0.0
17]
Dw
arf
bir
ch)
0.0
28
[)0.0
84,
0.0
28]
0.1
07
[0.0
02,
0.2
12]
)0.0
04
[)0.0
20,
0.0
13]
0.0
17
[)0.0
21,
0.0
54]
)0.0
06
[)0.0
15,
0.0
03]
0.0
07
[)0.0
22,
0.0
08]
Ple
uro
carp
moss
es
0.1
37
[0.0
69,
0.2
05]
)0.0
43
[)0.1
72,
0.0
86]
0.0
02
[)0.0
18,
0.0
22]
0.0
01
[)0.0
45,
0.0
48]
)0.0
02
[)0.0
12,
0.0
09]
)0.0
04
[)0.0
23,
0.0
14]
Acr
oca
rpm
oss
es
0.0
18
[)0.0
51,
0.0
87]
)0.0
41
[)0.2
18,
0.1
35]
0.0
30
[0.0
09,
0.0
52]
0.0
60
[)0.0
03,
0.1
23]
)0.0
07
[)0.0
18,
0.0
05]
)0.0
17
[)0.0
41,
0.0
08]
Alt
itu
de
(*100)
0.0
03
[)0.0
59,
0.0
66]
0.0
12
[)0.5
7,
0.0
81]
0.0
27
[0.0
11,
0.0
43]
0.0
12
[)0.0
13,
0.0
37]
0.0
01
[)0.0
08,
0.0
09]
0.0
02
[)0.0
08,
0.0
13]
Slo
pe
0.0
50
[)0.0
34,
0.1
35]
)0.0
20
[)0.2
40,
0.2
00]
0.0
22
[)0.0
06,
0.0
49]
0.0
04
[)0.0
75,
0.0
83]
0.0
03
[)0.0
11,
0.0
17]
)0.0
06
[)0.0
36,
0.0
25]
Ru
ggedn
ess
)0.1
38
[)0.3
32,
0.0
56]
0.0
30
[)0.4
72,
0.5
31]
)0.0
42
[)0.1
05,
0.0
22]
0.0
01
[)0.1
79,
0.1
81]
0.0
00
[)0.0
33,
0.0
33]
0.0
20
[)0.0
50,
0.0
90]
Sig
nifi
can
tco
effici
ents
(th
at
is,
thos
efo
rw
hic
hth
eco
nfiden
cein
terv
al
did
not
incl
ude
zero
)are
inbol
d.
Pol
ynom
ial
term
sfo
rth
ere
indee
rabu
ndan
cew
ere
only
incl
uded
inca
ses
inw
hic
ha
non
-lin
eari
tyw
as
evid
ent.
616 R. A. Ims and others
expected from reindeer overabundance, the confi-
dence interval was too wide to provide any statis-
tical evidence for this. It should be noted, however,
that the precision of the analysis of hare abundance
was low at the scale of herding districts due to the
very few and patchily distributed recordings of
hares (Figure 4). It is likely that the only occasional
presence of hare to a large extent mirrors that of
tall Salix shrubs, which appear to exhibit an
equivalent rarity and patchy distribution in the
reindeer summer pastures in Finnmark (see the
large standard error of the mean tall Salix abun-
dance in Table 2).
Lemmings, and also to some extent voles, usually
dominate among tundra herbivores in terms of
biomass and impact on other components of the
plant-based food (Finerty 1980; Batzli and others
1980; Ims and Fuglei 2005). Thus the greatest po-
tential for a strong trophic cascade caused by
reindeer overabundance lies in a negative impact
on the abundance of small rodents. However, de-
spite the fact that reindeer biomass in the most
densely stocked districts now clearly outweighs
small rodent biomass, we found no evidence for a
negative effect of this high reindeer density on
small rodent abundance at the scale of reindeer
herding districts. Rather opposite, at the two
smaller spatial scales (that is, sampling lines and
landscape areas within herding districts) there were
strong positive, non-linear associations between
indexed abundance for reindeer and small rodents.
Both small rodents and reindeer were associated
with plants characterizing snow bed vegetation
such as prostrate Salix (mostly S. herbacea), small
dicotyledons and mosses (Moen 1999). This indi-
cates that most of the small rodent signs recorded in
our study stem from the Norwegian lemming,
which typically spend the winters in snow bed
vegetation (Kalela 1961; Stenseth and Ims 1993).
In snow beds lemmings find both thermal insula-
tion (under a thick snow cover) and their preferred
winter food; that is, mosses. Reindeer typically
exploit snow beds in the summer (Edenius and
others 2003), probably due to the availability of
young nutritious plant items when vegetation
elsewhere is in a phenologically more advanced
and less palatable state. Thus the positive associa-
tion between lemmings and reindeer may therefore
at least partially, be due to the fact that they
coincide spatially in areas with snow bed character.
So why does not this distinct spatial overlap be-
tween the two herbivores lead to resource compe-
tition and a negative impact of reindeer
overabundance on lemmings? Although lemmings
and reindeer overlap spatially they are temporally
segregated because snow beds are winter habitats
for lemmings and summer habitats for reindeer.
This temporal separation of habitat and the fact that
the Norwegian lemming predominantly forage on
mosses in winter (Batzli 1993), which are avoided
by reindeer in the summer (Batzli and others
1980), limits the scope for resource competition.
Quite to the contrary of a situation with competi-
tive interaction between the two herbivores, lem-
mings may increase summer pasture quality for
reindeer by removing mosses and thus disturbing
the moss cover (Moen and others 1993; Virtanen
2000). Such disturbance of the moss cover may
enhance establishment of more palatable vascular
plants for reindeer (Virtanen 2000; van der Wal
and Brooker 2004). Our finding that there was a
higher abundance of small dicotyledons in summer
where lemmings had been numerous in the winter
is consistent with such an effect of lemming winter
activity. Moreover, the large quantities of excreta
left by lemmings in snow beds at the end of the
peak density winters may have a substantial posi-
tive effect on plant growth and plant quality in the
spring due to release of nutrients from lemming
feces (Schults 1969). The winter activity by lem-
mings may also reduce the amount of standing
dead vascular plant tissue, tissue that potentially
shades the photosynthetic activity of the new
spring growth, further enhancing the productivity
of the plants. The strong positive association be-
Figure 5. Box plot depicting the non-linear, positive
relation between small rodent and reindeer abundance at
the scale of landscape areas. Indexed reindeer abun-
dances (that is, number of plots per sampling line with
recorded presence) are lumped into four categories
Impacts of Reindeer Overabundance 617
tween reindeer and small rodents, even when plant
abundance was statistically accounted for, indicates
that there may be a facilitating effect operating
between these herbivores through plant quality or
productivity. Whatever the mechanism underlying
such a facilitation, our study contradicts the pro-
posed negative cascading effect of reindeer on small
rodents and their predators.
Several of the relations between the herbivores
and habitat variables appeared to be scale depen-
dent, and most of them appeared at the smallest
spatial scale (that is, the sampling line scale), which
is consistent with results from studies in different
ecosystems (for example, Palmer and others 2003).
The predominant small-scale plant-herbivore rela-
tion in the present study may be explained by the
small-scale patchiness of important habitat ele-
ments such as snow beds (Edenius and other 2003)
and Salix thickets (den Herder and others 2003). In
the case of small rodents the shifting influence of
some plants depending on scale may also be due to
shifting habitat selection on a temporal scale. For
instance, at the local scale (lines) lemming will not
co-occur in winter with dwarf birch (which are not
found in snow beds), but the abundance of lem-
mings at the landscape scale may still depend on
dwarf birch (see Table 5) as this plant is an
important structure in small rodent summer habi-
tats (Hamback and others 1998). The only variable
predicting (high) reindeer abundance at the scale of
landscape areas was (high) altitude possibly
reflecting both avoidance of insect harassment at
this spatial scale (Hagemoen and Reimers 2002)
and a favorable altitudinal gradient in plant phe-
nological stages (Albon and Langvatn 1992).
Crowberry appeared to be a strong negative
predictor of small rodent abundance both at the
landscape and the line scales. Crowberry is cur-
rently the dominating species in tundra vegetation
of northern Fennoscandia (Table 2). This ericoid is
virtually unpalatable to herbivores (Tybirk and
others 2000), has a strong allelopathic effect on
other plants (Wardle and Nilsson 1997) and tends
to immobilize nutrients in the soil reducing overall
primary productivity (Nilsson 1994). Thus crow-
berry can be classified as an invasive species (for
example, Wardle and others 1998) that needs an
efficient disturbance regime to be restricted within
its fundamental niche. Such disturbance regimes
are both present in the boreal forest in terms of fires
(Wardle and others 1998), and in middle and high
arctic tundra in terms of permafrost and cryotur-
bation (Bliss and others 1973; Epstein and others
2004). However, in alpine and low Arctic heaths,
where such abiotic disturbances are mainly absent,
only extreme impacts of herbivores appear to be
able to alleviate the dominance of crowberry. One
such extreme herbivore impact, which occurs very
locally along fences separating semi-domestic herds
in Finnmark, is the intense trampling by reindeer
Table 6. The Coefficients (±95% CI) of the Models of Indexed Reindeer Abundance at the Scales ofLandscape Areas and Sampling Lines as a Function of Plant Abundance and Topographical Variables
Predictor variable Spatial scale
Line Landscape
Intercept 0.382 [0.003, 0.761] )0.669 [)1.730, 0.392]
Mat grass )0.067 [)0.142, 0.008] 0.182 [)0.043, 0.406]
Grasses (other) 0.020 [)0.046, 0.087] 0.212 [)0.056, 0.480]
Sedges )0.035 [)0.097, 0.028] 0.037 [)0.177, 0.251]
Small dicotyledons 0.047 [)0.049, 0.142] )0.149 [)0.458, 0.159]
Bilberry 0.120 [0.006, 0.234] )0.254 [)0.674, 0.165]
Deciduous ericoids (other) )0.112 [)0.223, )0.000] 0.122 [)0.338, 0.582]
Crowberry )0.002 [)0.080, 0.076] 0.112 [)0.184, 0.407]
Evergreen ericoids (other) 0.074 [)0.014, 0.163] 0.008 [)0.360, 0.376]
Tall Salix )0.193 [)0.376, )0.010] )0.066 [)0.448, 0.317]
Prostrate Salix 0.191 [0.104, 0.279] 0.092 [)0.166, 0.349]
Dwarf birch )0.014 [)0.088, 0.060] )0.009 [)0.202, 0.183]
Pleurocarp mosses 0.184 [0.095, 0.273] 0.069 [)0.155, 0.293]
Acrocarp mosses )0.005 [)0.095, 0.085] 0.172 [)0.133, 0.477]
Altitude (*100) 0.044 [)0.041,0.129] 0.180 [0.051, 0.309]
Slope 0.084 [)0.026, 0.193] 0.015 [)0.368, 0.398]
Ruggedness )0.208 [)0.459, 0.044] )0.089 [)0.960, 0.783]
Significant coefficients (that is, those for which the confidence interval did not include zero) are in bold.
618 R. A. Ims and others
that causes erosion (Evans 1996). However, rein-
deer grazing, even in the most densely stocked
districts in Finnmark, is not able to affect crowberry
abundance on a large spatial scale (Brathen and
others, in press). The only tundra herbivore with
the capacity to affect crowberry on a large scale is
probably lemmings during high-amplitude peak
years. In such years lemmings occupy even crow-
berry heaths in great numbers, where they mow
down the shrub layer presumably to get access to
the ground level mosses (Oksanen and Oksanen
1981). If such intense grazing events coupled with
mobilization of nutrients due to large amounts
lemming excreta occurred frequently, the domi-
nance of crowberry might be reduced, giving way
to a more biologically diverse and productive eco-
system state.
Although lemming and vole peak years re-occur
cyclically at 3–5-year intervals in northern Fenno-
scandia (Stenseth and Ims 1993), most lemming
peaks during the last century have been small
(Angerbjorn and others 2001) and there seem to be
periods of 20–30 years between peak years with
substantial impacts on the vegetation (Henttonen
and Kaikusalo 1993; Virtanen 2000). Moreover,
during the last two decades the small rodent pop-
ulation cycles in northern Fennoscandia have be-
come substantially weaker (Henttonen and
Wallgren 2001; Yoccoz and others 2001; Hornfeldt
2004). A number of factors have been proposed to
explain these changes (Hornfeldt 2004), among
which climate change appears to be the most
credible ultimate cause (Callaghan and others
2004; Ims and Fuglei 2005). The recent population
declines of Arctic specialist small rodent predators
(Kjellen and Roos 2000; Tannerfeldt and others
2002; Hornfeldt and others 2005) represent most
likely a bottom-up effect of the fading small rodent
cycle. Based on the large-scale connection between
abundance of crowberry and lemming revealed in
the present study we highlight the possibility of a
top-down effect due to the relaxed lemming dis-
turbance on tundra heath vegetation. In areas and
time periods without substantial lemming peaks
crowberry may expand with possible negative
feedback effects on lemmings, other herbivores and
their predators.
CONCLUSION
Our large-scale study provided results that were
consistent with the prediction (Van Herder and
others 2004) that ptarmigans may be the tundra
herbivores most sensitive to reindeer overabun-
dance and that this may lead to a trophic cascade
whereby predators specialized on ptarmigan such
as gyr falcon Falco rusticolus ultimately may be af-
fected (Tømmeraas 1993). The reindeer—ptarmi-
gan connection is most likely due to the negative
impacts of heavy reindeer browsing on tall Salix,
which both provides essential habitat and food for
the willow ptarmigan. Thickets of tall Salix shrubs
in the tundra landscape provide habitat and re-
sources for many other species as well and are
thereby probably hot spots for many food web
interactions not considered in the present study.
Thus future studies should investigate the conse-
quences of reindeer-induced loss of tall Salix.
On the other hand, our study did not support the
most severe trophic cascade believed to result from
reindeer overabundance. Such a cascade would be
induced if reindeer overgrazing negatively im-
pacted small rodents, which are normally the
keystone herbivores in the plant-based tundra food
web. However, on the contrary we found a strong
positive association between small rodents and
reindeer, which may be due to a facilitating effect
of lemming winter activity on reindeer summer
pasture quality. This possibility emphasizes the
need for obtaining a better understanding of the
consequences of the recent weakening of the small
rodent cycles on the long-term development of
tundra vegetation (Ims and Fuglei 2005).
ACKNOWLEDGEMENTS
We are grateful to Johan Ingvald Hætta and Anders
Aarthun Ims for information about reindeer herding
districts, to Torstein Engelskjøn for providing a flora
database, Bernt Johansen for providing satellite
images, The Norwegian Coast Guard and Jan Kare
Amundsen for transportation during field work,
Sunna Pentha for field assistance, and to Marianne
Iversen and Siw Killengreen for great leadership
during field work. This study, which is a contribution
from the ‘‘Ecosystem Finnmark‘‘ project, was fi-
nanced by the Norwegian Research Council.
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