B I O L O G I CA L C O N S E RVAT I O N
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available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/biocon
Structural characteristics of a low Arctic tundra ecosystem
and the retreat of the Arctic fox
Siw T. Killengreen, Rolf A. Ims*, Nigel G. Yoccoz, Kari Anne Bråthen,
John-André Henden, Tino Schott
Department of Biology, University of Tromsø, NO-9037 Tromsø, Norway
A R T I C L E I N F O
A B S T R A C T
Article history:
We conducted a large-scale, campaign-based survey in Finnmark, northern Norway to eval-
Received 19 July 2006
uate the proposition that declining Arctic fox populations at the southern margin of the
Received in revised form
Arctic tundra biome result from fundamental changes in the state of the ecosystem due
24 October 2006
to climatic warming. We utilized the fact that the decline of the Arctic fox in Finnmark
Accepted 25 October 2006
has been spatially heterogeneous by contrasting ecosystem state variables between regions
Available online 12 December 2006
and landscape areas (within regions) with and without recent Arctic fox breeding.
Keywords:
and the most recent breeding records of Arctic fox, we found patterns largely consistent
Climate warming
with a previously proposed climate-induced, bottom-up trophic cascade that may exclude
Within the region of Varanger peninsula, which has the highest number of recorded dens
Ecosystem state
the Arctic fox from tundra. Landscape areas surrounding dens without recent Arctic breed-
Climate sensitive plants
ing were here more productive than areas with recent breeding in terms of biomass of pal-
Lemmings
atable and climate sensitive plants, the number of insectivorous passerines and predatory
Red fox
skuas. Even the frequency of unspecified fox scats was the highest in landscape areas
Reindeer
where arctic fox breeding has ceased, consistent with an invasion of the competitively
dominant red fox. The comparisons made at the regional level were not consistent with
the results within the Varanger region, possibly due to different causal factors or to deficiencies in Arctic fox monitoring at a large spatial scale. Thus long-term studies and adequate monitoring schemes with a large-scale design needs to be initiated to better
elucidate the link between climate, food web dynamics and their relations to Arctic and
red foxes.
2006 Elsevier Ltd. All rights reserved.
1.
Introduction
The Arctic is currently subject to changes threatening the
integrity of tundra ecosystems (CAFF, 2003). Global warming,
which is expected to be most pronounced in polar regions,
is particularly highlighted (Callaghan et al., 2004b; Foley,
2005; Hinzman et al., 2005; Chapin et al., 2005). However, climate change takes place in conjunction with several other
anthropogenic stressors, such as intensified land use (CAFF,
2003; ACIA, 2004). Although the entire Arctic region may be
subject to change, the low Arctic tundra zone (Bliss et al.,
1973) may be particularly prone to early and rapid change, because it balances against more southern and vastly different
ecosystem states (Epstein et al., 2004).
It has been proposed that upper trophic levels (i.e. predators) may be particularly sensitive to fundamental ecosystem
alterations (Schmitz et al., 2003; Sergio et al., 2005; Voigt et al.,
2003). Tundra ecosystems have typically a tri-trophic, plantbased food web topped by a guild of predators preying mainly
on herbivorous small mammals (lemmings and voles) (Elton,
* Corresponding author: Tel.: +47 77646476.
E-mail address: [email protected] (R.A. Ims).
0006-3207/$ - see front matter 2006 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2006.10.039
460
B I O L O G I C A L C O N S E RVAT I O N
1942; Wiklund et al., 1999; Krebs et al., 2003; Ims and Fuglei,
2005). Some of these small mammal predators, such as the
Arctic fox Alopex lagopus (Angerbjörn et al., 2004; Fuglei,
2005), are found exclusively in the Arctic region and should
for this reason be particularly vulnerable to global warming
(CAFF, 2003; ACIA, 2004; Callaghan et al., 2004a).
In a seminal paper Hersteinsson and MacDonald (1992)
analyzed harvest statistics and demonstrated that the Arctic
fox during the last century had exhibited a warming related
retreat of from the southern edge of the Arctic. They proposed
an underlying process scenario that involved a bottom-up trophic cascade by which a warming-induced increase in primary productivity (i.e. plant biomass) in turn gave way to a
higher secondary productivity (i.e. prey biomass) available to
the northward expanding red fox expelling the competitive
subordinate Arctic fox. Hersteinsson and MacDonald (1992)
wrote, however, that they were ‘‘mindful’’ with regard to the
exact mechanisms in the paucity of data on variables other
than fox harvest rates and climatology. Indeed, in Fennoscandia where the Arctic fox is on the verge of regional extinction,
several other explanations for the ‘‘Arctic fox problem’’ have
been forwarded (for reviews see Hersteinsson et al., 1989; Angerbjörn et al., 1995; Linnell et al., 1999a). As a result management actions (such as population enhancement by
introduction of captive bred Arctic foxes in Norway) are now
undertaken that implicitly assume that no fundamental
change of the ecosystem underlies the Arctic fox decline.
In the present study, we aim to provide the first direct evaluation of Hersteinsson and McDonald’s proposition that the
retreat of the Arctic fox from the southern edge of the Arctic
is ultimately due to a climate-induced change in ecosystem
structure. We do this by analyzing relevant ecosystem state
variables measured during a large-scale, targeted field campaign encompassing regions in eastern Finnmark, northern
Norway with current presence or absence of the Arctic fox.
According to Hersteinsson and MacDonald (1992) we predicted that tundra areas where arctic fox breeding had ceased
should show increased biomass of plants likely have increased under warmer climate and, moreover equivalent
responses in variables reflecting higher trophic levels consistent with a bottom-up trophic cascade.
2.
Materials and methods
2.1.
General characteristics of the study area
The region of eastern Finnmark forming the northeastern tip
of Norway at 70–71N, is bio-climatically classified as low Arctic tundra (Walker et al., 2005). The Finnmark tundra, which is
most clearly defined on the low-altitude peninsulas bordering
the Barents sea (Fig. 1), constitutes the westernmost fringe of
the vast Euro-Asian tundra (Virtanen et al., 1999). The study
area is low-altitude (<400 m a.s.l.), relatively coast-near tundra. The climate is characterized by relatively mild winters
due to the influence of the North Atlantic current and permafrost occurs only very scattered (Virtanen et al., 1999). To the
south, the study area is connected with tundra-like, highaltitude areas often termed mountain tundra. This mountain
tundra extends far south on the Scandinavian Peninsula and
1 3 5 ( 2 0 0 7 ) 4 5 9 –4 7 2
is surrounded by sub-alpine boreal forest (Ahti and HämetAhti, 1969; Oksanen and Virtanen, 1995). In eastern Finnmark,
the boreal forest extends northwards as narrow belts in the
valleys to the inner parts of the fjords (Oksanen and Virtanen,
1995). The coast-near Finnmark tundra is classified as erect
shrub tundra (Walker et al., 2005), although there is a large intra-zonal variation caused by topography and substrate types
(Moen, 1999; Virtanen et al., 1999; Karlsen et al., 2005). At altitudes above 400 m the vegetation is very sparse.
There is recent evidence that temperatures have increased
in Finnmark during the last century (Hanssen-Bauer, 1999).
Another concurrent change is a steep increase in the density
and grazing impacts of semi-domestic reindeers (Moen and
Danell, 2003). However, apart from a few reports demonstrating changes in the vegetation being compatible with both the
impacts of climate warming and intensified grazing pressure
(e.g. Tømmervik et al., 2004), the broader implications of
these changes for the structure and functioning of the tundra
ecosystem have not yet been addressed.
2.2.
General study design
Our study approach is a campaign-based, large-scale survey
conducted during the summer of 2004. The design of the
survey is guided by the current distribution of the Arctic fox
dens in eastern Finnmark. Traditional Arctic fox dens, which
are clearly visible in the tundra landscape, even many decades
after they have been abandoned, are found widespread in
Finnmark (Frafjord, 2003). All dens, for instance detected by
aerial surveys (e.g. Angerbjörn et al., 1999), have been entered
in a database established by the Arctic fox monitoring program
of the Norwegian Directorate for Nature Management
(Andersen et al., 2004). In this ‘‘den database’’ records of recent
Arctic fox activity at dens, including breeding have been registered by means of visits at dens at a yearly basis. It is clear from
this database that the large majority of known Arctic dens in
eastern Finnmark (and elsewhere in Norway) now are abandoned. Recent analyses focusing on local den characteristics
from a sample of dens from several geographic areas in Fennoscandia (i.e. mostly mountain tundra south of the present survey area), have shown that the probability of Arctic fox den
occupancy increases with the altitude and distance from red
fox dens (Linnell et al., 1999b; Tannerfeldt et al., 2002; Dalerum
et al., 2002; Frafjord, 2003). Still most dens in Finnmark are now
abandoned regardless of altitude and known red fox presence.
In this study, we restrict our investigation to altitudes with the
highest probability of Arctic fox presence (i.e. altitudes with
Arctic fox breeding during the last 5 years before our field work
in summer 2004) as to highlight variation in the state of the
ecosystem within the altitudes presumably best suited for Arctic fox in the study region.
The survey design encompassed two spatial scales: On the
large scale we selected 5 study regions based on the criteria
that they should be similar in topography, altitude and distance from the coast (Fig. 1). Two of these study regions (VARANGER and LAKSEFJORD; Table 1) had many recorded Arctic
fox dens in the database, while three nearby study regions
had no records of Arctic fox dens (RAKKONJARGA, BEKKARFJORD and NORDKINN; Table 1) on the tundra plateaus ranging
from 100 to 400 m above the sea level (Fig. 2).
B I O L O G I C A L C O N S E RVAT I O N
461
1 3 5 ( 2 0 0 7 ) 4 5 9 –4 7 2
Fig. 1 – The survey-design with the five study regions in eastern Finnmark with the position of landscape blocks (black
squares) and a schematic outline of the sampling design (see main text for an explanation of the sampling methods).
On a smaller scale, within the regions, we selected 38 landscape blocks sized 4 km2 (2 · 2 km) for measurements of ecosystem state variables. In regions with recorded Arctic fox
dens, we placed landscape blocks so that they were centered
on known dens. Based on records provided by the den database (Andersen et al., 2004), three categories of dens (and thus
landscape blocks with dens) could be defined:
(1) Breeding dens: Dens with known or very probable Arctic
fox breeding during the last 5 years (2000–2004).
(2) Active dens: Dens with signs such as burrowing, scats
and prey remains indicating presence of Arctic fox during the last 5 years, but with no indication of breeding
Arctic foxes.
(3) Abandoned (old) dens: Evidently old, unused dens without any sign of recent Arctic fox presence.
In the study region VARANGER, which had the largest number of known dens (N = 21) and the most recent breeding records of Arctic foxes, all three categories could be used in the
selection of landscape blocks. There were only three dens with
confirmed breeding and one den with probable breeding and
all were selected as breeding den blocks (n = 4). In VARANGER,
we selected 4 active den blocks and 4 abandoned den blocks ran-
Table 1 – Sample sizes at the level of regions and
landscape blocks
Landscape block category
Region name
Breeding
Active
VARANGER
LAKSEFJORD
RAKKONJARGA
BEKKARFJORD
NORDKINN
4 (41)[0]
0
0
0
0
4 (46)[0]
4 (40)[0]
0
0
0
Abandoned Reference
4 (41)[0]
0
0
0
0
3
4
5
5
5
(31)[0]
(40)[0]
(39)[14]
(46)[3]
(44)[8]
The number of landscape blocks are given by numbers in bold,
number of quadrates (i.e. lines) sampled in parentheses and
number of quadrates discarded due to extensive boulder fields in
brackets. There were no known Arctic fox dens in the regions with
only reference block represented in the survey. Abbreviations of
the region names used in the figures are indicated by bold letters.
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B I O L O G I C A L C O N S E RVAT I O N
500
1 3 5 ( 2 0 0 7 ) 4 5 9 –4 7 2
Between
een Regions
Within Region
VARANGER
LAKSEFJORD
Altitude (m)
400
300
200
100
0
VAR
RAK
LAK
BEK
NOR
VAR
VARBreed VARActive
VAROld
Lak
LakActive
Fig. 2 – The altitude distribution of the sampling lines in the reference block in the five study region and in the different types of
landscape block type within the two regions with Arctic fox dens (VARANGER and LAKSEFJORD). Reference blocks are denoted
with first three letters of the region names without any extension (e.g. VAR for VARANGER and LAK for LAKSEFJORD), whereas
the different extensions of the region names denote landscape blocks with breeding dens (breed), active dens (active) and old/
abandoned dens (old). The distributions of altitudes are given as averages, standard deviation bars and ranges.
domly from the collection of dens within these categories with
the constraint that they should be in the approximate same
range of altitudes as the breeding den blocks (Table 1, Fig. 2).
In the study region LAKSEFJORD, there were four dens classified
as active, which decided the selection of den blocks. In both regions with Arctic fox dens (i.e. VARANGER and LAKSEFJORD)
we included a sample of reference blocks. The reference blocks
were placed in a random direction 5 km from a den with recent
presence Arctic fox (either breeding or active den) with the
restriction that they should not be closer to other known dens.
This distance criterion should ensure that the reference blocks
were outside known Arctic fox territories (Landa et al., 1998). In
the three study regions without known Arctic fox dens
(NORDKINN, RAKKONJARGA and BEKKARFJORD), we randomly selected landscape blocks with the constraints that
they should be within the same altitude range as LAKSEFJORD
and VARANGER. We also used the selection criterion that no
landscape block should include human settlement or major
roads. The number of reference block to be sampled per region
was constrained by logistics and time. One team with two
persons could analyze one landscape block in one day. There
were 2–3 teams working in parallel and the sampling was done
during July and early August in 2004.
2.3.
Data sampling and state variables
Like other campaign-based surveys of a large number of remote sites (e.g. Angerbjörn et al., 1999; Krebs et al., 2003),
we had to focus on an efficient sampling scheme and a set
of ecosystem state variable that both could be measured in
a standardized manner during a short time interval (i.e. one
day) and that still could reflect the state of the plant-based
trophic system.
2.3.1.
Selection of sampling quadrates
For the purpose of obtaining unbiased estimates of ecosystem
state variables within the selected 2 · 2 km landscape blocks,
they were further subdivided in 100 square areas of
200 · 200 m from which we randomly drew a number of sampling areas (Fig. 1). The selection of sampling areas was done
with the restriction that areas overlapping a circle with a
diameter of 200 m surrounding the den (or the central point
of reference blocks) were omitted. The omission of the immediate area around the den was done to ensure that none of
the measurements taken should be affected by the local fertilization and disturbance effects that are known to be associated with Arctic fox activity (Bruun et al., 2005). The center of
each of the selected areas was a start position for a 50 m sampling line whose direction was given by a random GPS position
on a circle of 50 m radius from the center. The sampling lines
were sub-sampled at plots every 5 m along the line with a triangular sampling frame with sides of 40 cm (Fig. 1). If a part of
the sampling line had to be discarded, i.e. because of wetness
(lake, large river or very wet mire), snow cover (more than a
5 m section running through snow) or a big boulder field
(more than half of the sampling line running over boulders
void of vegetation) a second direction given by a new random
GPS position was assessed. If a part of the second direction
also had to be discarded, a new start position for the sampling
line was found by moving from the original position in the
first selected GPS direction until an acceptable start position
was found. If no new acceptable start position within the area
was found, the area was discarded. The rejections of areas
were exclusively due to extensive boulder fields, and all were
in the regions without recorded Arctic fox dens (Table 1). The
number of lines sampled per landscape block was decided by
how many could be covered during one day and this was on
average 9 lines per block (Table 1).
2.3.2.
Plants
The abundance of all vascular plant species was recorded in
the triangular sampling frames (Fig. 2) according to the point
intercept method (Jonasson, 1988). For a given growth form
the number of point intersects is proportional to biomass
(e.g. Frank and McNaughton, 1990; Wardle et al., 2003; Bråthen and Hagberg, 2004). Moss (acrocarp, pleurocarp or
B I O L O G I C A L C O N S E RVAT I O N
Sphagnum) and lichen cover were also recorded. To optimize
sampling effort with respect to the tradeoff between withinand between-plot sampling variance (Bråthen and Hagberg,
2004), we used only three pins per sample triangle allowing
for a larger number of plots per sampling line and sampling
lines per landscape block. One side (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 (Fig. 1). Given our focus on the functional importance of plant primary production in a food web context,
we initially focused on 26 plant variables represented by relatively abundant individual plant species or growth forms
composed of less abundant species (see Table 2). We then
used ordination as a exploratory tools to select a smaller
subset of these plant variables that adequately reflected the
structure in the total plant data set and which could subject
to quantitative statistical analysis. For this purpose we used
two ordination techniques: Non-symmetric correspondence
analysis (Pélissier et al., 2003) and co-inertia analyses (Dray
et al., 2003). The results of the two ordinations were consistent and resulted in the final selection of eight plant response variables (Table 2).
2.3.3.
Herbivores
Vertebrate herbivores (mostly mammals) dominate secondary
production in tundra ecosystem (Batzli et al., 1980; Krebs
Table 2 – Individual plant species or growth forms
analyzed with the mean abundance (number of intercepts per sampling frame)
Species/growth form
Empetrum nigrum ssp. hermaphroditum (Crowberry)*
Betula nana (Dwarf birch)*
Vaccinium myrtillus (Bilberry)*
Vaccinium vitis-idaea
Rubus chamaemorus
Cornus suecica
Bistorta vivipara
Nardus stricta (Mat grass)*
Carex bigelowii (Stiff sedge)*
Deschampsia flexuosa
Graminoids others*
Poaceae spp. Others
Pinguicula spp.
Equisetum spp.
Lycopodium spp.
Decideous shrubs others
Evergreen shrubs others
Prostrate Salix*
Erect Salix
Tall herbs
Small herbs
Wintergreen herbs
Sphagnum mosses
Acrocarp mosses*
Pleurocarp mosses
Lichens
Mean
abundance
0.831
0.754
0.632
0.135
0.009
0.053
0.023
0.207
0.083
0.339
0.332
0.068
0.001
0.011
0.004
0.046
0.028
0.141
0.020
0.013
0.060
0.001
0.057
1.273
0.037
0.641
Eight species or growth forms marked with an asterisk were found
to represent the main structure in the vegetation according to
ordination analyses. Nomenclature follows Lid and Lid (2005).
1 3 5 ( 2 0 0 7 ) 4 5 9 –4 7 2
463
et al., 2003). We estimated relative density indices of hares (Lepus timidus), ptarmigans (Lagopus spp.) and reindeer (Rangifer
tarandus) from the presence-absence records of faecal pellets
in the plant sampling triangles. Voles and lemmings pellets
are more difficult to detect both due to small size and subterranean activity and we recorded (as presence-absence in the
sampling triangles) more conspicuous signs of rodent grazing
activity (cut vegetation, runways and burrows) from the previous winter. The different species of small rodents are difficult
to differentiate based on such signs, however. The relative
species composition and abundance at the scale of the study
regions in summer 2004 was obtained from a separate trapping study. The trapping, which was done according to the
‘‘small quadrate method’’ (Myllymäki et al., 1971), was conducted for two days in late June in two vegetation strata:
Heath vegetation with high cover of shrubs representing preferred habitat by the grey-sided vole (Clethrionomys rufocanus)
and moister graminoid or moss rich tundra preferred by Norwegian lemmings (Lemmus lemmus) or tundra voles (Microtus
oeconomus). Due to logistic reasons this trapping sub-study
was not linked to the block-design of main study. Instead
the trapping was conducted along roads crossing the tundra
plateaus of the five regions. The trapping effort varied from
18 to 25 small quadrates per study region.
2.3.4.
Predators and their diets
The assemblage of vertebrate predators on southern tundra
consists mainly of small to medium sized mammals (mustelids: least weasel, Mustela n. nivalis, stoat Mustela erminea and
wolverine Gulo gulo and foxes) or avian predators such as raptors (mainly rough-legged buzzards Buteo lagopus and owls)
and skuas (long-tailed skua Stercorarius longicaudus and parasitic skua Stercorarius parasiticus Wiklund et al., 1998, 1999).
Raptors are usually only present in the peak years of the rodent cycle. As 2004 was a typical low-phase year of the cycle
in all study regions very few direct observations of raptors
were made. In order to get an index of the prevalence of raptors in the study blocks we recorded pellets with regurgitated
prey remains originating from avian predators. Pellet counts
and sampling were done along straight-line transects between the sampling areas within study blocks. The average
distance of these transects were 3.96 km per block (range:
1.8–5.2 km). The transects were walked by a team of two
observers: One observer keeping strict to the line according
to GPS, whereas the other systematically visited elevated
points on the otherwise flat tundra (e.g. large stones, small
hills or outcrops) within approximately 100 m from the line.
Raptor pellets (and fox scats; see below), which are usually
deposited at such elevated points, were recorded. Most of raptor pellets in the study regions is most likely from three species (rough-legged buzzards, snowy owls Bubo scandiaca and
short-eared owls Asio flammeus). However, species identification is fraught with uncertainties, so raptor pellets were treated as one generic category in the analysis.
Fox scats were found frequently by this transect sampling
procedure and were recorded in the same manner as the raptor
pellets. Species identification (red vs. Arctic fox) from faeces
can only be done on very fresh specimens by DNA extraction
(Dalén et al., 2004). Here we will use the scat counts as a generic
measure of intensity of use of the different landscape blocks by
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B I O L O G I C A L C O N S E RVAT I O N
foxes, although there are all reasons to believe that the majority
of scats stem from red foxes (Frafjord, 2000). Scat counts have
also been used as an index of fox population density in previous
studies (Webbon et al., 2004). We collected all the fox scats recorded in the transects (N = 230) for diet analyses assuming that
diet reflect prey availability. Previous studies of Arctic fox diets
in Fennoscandia have found that Arctic fox and red fox diets in
mountain tundra habitats differ only slightly and that the differences can mainly be attributed to difference in habitat (e.g.
altitude) (Frafjord, 2000; Elmhagen et al., 2002).
The contents of individual scats were examined by fragmenting them by hand. Remains of different prey items were
sorted and their volumes were assessed by eye. Due to a small
number of scats in certain landscapes we only considered
three prey categories in the statistical analysis. These were
small mammals (mainly Norwegian lemmings, grey-sided
voles and tundra voles, average volume 45%), birds (average
volume: 15%) and reindeer (average volume: 16%).
2.3.5.
Bird counts
Apart from the herbivorous ptarmigans, raptors and skuas,
passerines and waders dominate the tundra bird community.
These mainly insectivorous birds reflect landscape and vegetation patterns as well as they constitute alternative prey to
herbivores for Arctic foxes in particular in years with low
abundance of small rodents (e.g. Sutherland, 1988). Bird
counts were done along the straight line transects between
the sampling quadrates within the landscape blocks
(see above). All birds seen at the distance classes: 0–50 m,
50–100 m and >100 m were recorded. Due to the small number
of observations at the block level we lumped the counts over
all distance classes and into the three taxonomic categories;
passerines, waders and skuas (mainly long-tailed skua).
2.4.
Statistical analyses
The study design calls for comparisons of ecosystem state
variables at two focal scales. At the largest scale (regional)
we conducted comparisons (planned contrasts implemented
at ‘‘treatment contrasts’’ in the program package R, see Crawley,
2005) between study regions. In these regional contrasts, we
only included the reference blocks. The region VARANGER
was used as the reference level for the regional contrasts on
the grounds that VARANGER presently appears to be the best
Arctic fox region in eastern Finnmark. At a smaller scale within the regions with known Arctic fox dens (VARANGER and
LAKSEFJORD), we quantified differences between landscape
blocks without dens (i.e. reference blocks) and landscape
blocks with dens of the different categories (i.e. breeding,
active and abandoned/old dens). The reference blocks in each
of the two regions were used as the reference level for these
intra-regional contrasts. In all contrasts analyses landscape
blocks were used as the focal study units (i.e. replicates). The
data were aggregated by summing up the number of point
intercepts (plants) or presence records (reindeer pellets) per
sampling line. In the case of plant variables the data were entered the analysis at the level of sampling lines with block as a
random variable, whereas for reindeer pellets the records
were averaged over all lines per landscape block and the
blocks were then the units in the analyses. Counts of birds,
1 3 5 ( 2 0 0 7 ) 4 5 9 –4 7 2
fox scats and raptor pellets along the walked transects in each
landscape block were entered into the analysis as number of
observations per km. All the count variables (when aggregated
at the line or block levels) exhibited empirical distributions
that were adequate for contrasts analysis derived from general linear models. Including altitude of the sampling line in
the linear model improved the precision of estimates for some
plant variables so all contrast of plants abundance are adjusted for altitude. We tried two other topographical covariates in the linear models, namely the average terrain
curvature and slope for the sampling lines within the blocks,
but these variables proved to be relatively unimportant. The
statistical significance of the contrasts at both scales was evaluated according to their 95% confidence intervals.
Diet based on fox scat contents was analysed by compositional analysis (Aebischer et al., 1993) by averaging the proportional contents of the three main prey categories (small
mammals, birds and reindeer) over all scats per landscape
block. Contrasts were estimated as difference between proportions in the case of small mammals or the log-ratios against
small mammals for reindeer and birds. Bootstrapping was
used to calculate 95% confidence intervals for the diet contrasts, since parametric assumptions were unlikely to hold.
3.
Results
3.1.
Plants
For the contrasts between regions, the reference blocks in
VARANGER (i.e. the region with most recent Arctic fox breeding) had more bilberry and acrocarp mosses than all the other
regions (Fig. 3). Except for a significant higher abundance of
dwarf birch and crowberry and less prostrate Salix in VARANGER than in NORDKINN, there were no other clear differences
between the reference blocks at the regional level.
Within both regions with known fox dens (i.e. VARANGER
and LAKSEFJORD) landscape blocks with active dens had less
crowberry than the reference blocks (Fig. 3). No other differences were found within LAKSEFJORD, while there were several substantial differences among the landscape block
categories in VARANGER. Most notable, blocks with breeding
Arctic fox had less biomass of the two deciduous shrubs bilberry and dwarf birch as well as the two graminoids mat grass
(Nardus stricta) and stiff sedge (Carex bigelowii) than the two
other block categories with Arctic fox dens without records recent breeding. The low plant biomass in landscape blocks with
recent Arctic fox breeding was most notable in the case of bilberry for which even the randomly selected reference blocks
had higher biomass. Abandoned dens on the other hand had
substantially more bilberry than the reference blocks, and
both abandoned and active dens had more mat grass and stiff
sedge than the reference blocks in VARANGER (Fig. 3).
3.2.
Herbivores
Small rodent populations had crashed already in the fall prior
to this survey (Ims and Yoccoz unpublished). Consequently, our
trapping survey showed that small rodent densities were low
in early summer in all study regions with the grey-sided vole
B I O L O G I C A L C O N S E RVAT I O N
Bilberry
15
Crowberry
5.62
(1.73)
10.82 (1.68)
Contrast
10
5
15
14.26
(1.87)
11.60 (1.81)
10
5
0
0
-5
-5
-10
-10
-15
-15
RAK
K
LAK
BEK
NOR
VAR Breed
VAR Active
VAR Old
RAK
K
LAK Active
LAK
BEK
Dwarf birch
15
NOR
VAR Breed
VAR Active
VAR Old
LAK Active
Prostrate willow
12.24
(1.97)
9.38 (1.91)
10
Contrast
465
1 3 5 ( 2 0 0 7 ) 4 5 9 –4 7 2
0.36 (0.69)
6
0
(0.71)
4
5
2
0
0
-5
-2
-10
-4
-15
RAK
K
LAK
BEK
NOR
VAR Breed
VAR Active
VAR Old
RAK
K
LAK Active
LAK
BEK
Nardus stricta
Contrast
10
NOR
VAR Breed
VAR Active
VAR Old
LAK Active
Carex bigelowii
0.60 (1.27)
0.50
(1.32)
5
2
0
-2
0.49
(0.49)
0.32 (0.47)
4
0
-4
-5
RAK
K
LAK
BEK
NOR
VAR Breed
VAR Active
VAR Old
LAK Active
RAK
K
LAK
BEK
Other graminoids
3
VAR Breed
VAR Active
VAR Old
LAK Active
Acrocarp mosses
0.66
(0.52)
-0.21 (0.50)
2
Contrast
NOR
10
22.45 (3.30)
5
0
1
-5
0
-10
-1
14.33
(3.35)
-15
-2
-20
-3
-25
RAK
K
LAK
BEK
NOR
VAR Breed
VAR Active
VAR Old
LAK Active
RAK
K
LAK
BEK
NOR
VAR Breed
VAR Active
VAR Old
LAK Active
Fig. 3 – Contrasts (i.e. differences) in abundance (i.e. number of point intercepts per sampling line with 95% c.i.) of eight
influential plant species/growth forms. The contrasts regard two spatial scales: between the five study regions (left panel for
each species/growth form) and between landscape block categories within study regions (right panels) with active Arctic fox
dens (VARANGER and LAKSEFJORD) (see Fig. 2). For the four regional contrasts and the three contrasts within the region
VARANGER the reference block in VARANGER was used as the reference level, whereas within the region LAKSEFJORD the
reference blocks in LAKSEFJORD was used as the reference level. Thus for the contrasts between regions a positive value
means higher abundance in VARANGER than the contrasted region, whereas a positive value within the regions VARANGER
or LAKSEFJORD indicate higher abundance in the contrasted block category than in the reference blocks. The mean number of
intercepts per sampling line for the two reference levels (VARANGER and LAKSEFJORD) at the average altitude over all
sampling lines is given in each plot (i.e. above the error bars) with standard errors in parentheses. Note the different scaling
of the Y-axis for the different species and growth forms.
as the generally dominant species (Table 3). Due to the low
densities of small rodents in winter/spring there were too
few records of small rodent signs in the sampling lines for a
meaningful comparisons between the landscape blocks. Pellets of ptarmigans and hares were also generally too scarce
for analysis. Reindeer pellets were, however, recorded relatively frequently. Contrast analyses of reindeer pellet counts
indicated that there were no differences in the density of rein-
deer between the different regions or between the different
landscape block categories within the regions VARANGER
and LAKSEFJORD (Fig. 4).
3.3.
Predators
The number of fox scats and raptor pellets per km transect
line varied significantly among the regions (Fig. 4). In general,
466
B I O L O G I C A L C O N S E RVAT I O N
1 3 5 ( 2 0 0 7 ) 4 5 9 –4 7 2
Table 3 – Species composition of small rodents in the different study regions as indicated by density indices (mean
number of animals caught in small quadrates expressed as frequencies per 100 trap nights ± SE) in late June in 2004
Study region
Species
VARANGER
Grey-sided vole
Tundra vole
Norwegian lemming
1.67 ± 0.50
0.0 ± 0.0
0.0 ± 0.0
LAKSEFJORD
RAKKONJARG
2.08 ± 1.00
0.67 ± 0.42
0.0 ± 0.0
BEKKARFJORD
NORDKINN
0.67 ± 0.42
0.0 ± 0.0
0.0 ± 0.0
2.58 ± 0.83
0.0 ± 0.0
0.0 ± 0.0
0.67 ± 0.42
0.0 ± 0.0
0.0 ± 0.0
Reindeer
Contrast
1.0
0.32
(0.20)
0.75 (0.19)
0.5
0.0
-0.5
-1.0
RAK
LAK
BEK
NOR
VAR Breed
VAR Active
VAR Old
LAK Active
Fox feces
Contrast
4
2.67
(1.63)
0.92 (0.96)
2
0
-2
-4
RAK
LAK
BEK
NOR
VAR Breed
VAR Active
VAR Old
LAK Active
Raptor pellets
Contrast
1.0
0.61
(0.78)
0.07 (0.26)
0.5
0.0
-0.5
-1.0
RAK
LAK
BEK
NOR
VAR Breed
VAR Active
VAR Old
LAK Active
Fig. 4 – Contrasts (with 95% c.i.) between and within the study regions in the density of reindeer pellets (frequency of
sampling frames with pellets), foxes scats and raptors pellets (number scats and pellets per km transect line). See Fig. 3 for a
description of the interpretation of the contrasts.
the region LAKSEFJORD stood out as the region with the highest frequencies of both foxes and raptors. Within VARANGER
the frequency of fox pellets was much higher in blocks with
dens classified as active than the other categories. Moreover,
blocks with abandoned dens had a somewhat higher frequency of scats than the reference blocks. Blocks with breeding Arctic foxes in VARANGER and blocks with active dens in
LAKSEFJORD did not differ from the reference blocks neither
in terms of fox scat and raptor pellet frequency. All blocks
with dens in VARANGER tended to have more raptor pellets
than the reference blocks, but both the absolute frequencies
and differences in pellet counts were small in this region.
Small mammals generally dominated fox diet and there were
no clear differences in the proportion of small mammals
either between or within the regions (Fig. 5). However, the
confidence intervals for the contrasts were wide. The ratios
of birds to small mammals were higher in BEKKARFJORD than
in VARANGER at the regional level, whereas blocks with abandoned dens appeared to have a higher relative proportion of
birds than the reference blocks within VARANGER (Fig. 5).
The ratio reindeers to small mammals were less in VARAN-
GER than in most of the regions without recent records of Arctic fox breeding. There were no clear differences in the
relative amount of reindeers in the diet among the different
landscape block categories in VARANGER and LAKSEFJORD.
3.4.
Insectivorous birds and skuas
Bird counts differed significantly both between regions and
within landscape blocks in VARANGER (Fig. 6). At the regional
level VARANGER and RAKKONJARGA had very similar abundances, while BEKKARFJORD and NORDKINN had lower abundances than VARANGER for all three taxonomic categories
considered. In the comparisons between VARANGER and
LAKSEFJORD, skuas were less and passerines clearly more
abundant in LAKSEFJORD than in VARANGER. The differences
between the landscape block categories within VARANGER
tended to be higher than those between regions, while there
were no differences between landscape blocks in LAKSEFJORD. Within VARANGER skuas were most common in landscape blocks with active dens, while passerines and waders
were by far most common in landscape block with abandoned
B I O L O G I C A L C O N S E RVAT I O N
467
1 3 5 ( 2 0 0 7 ) 4 5 9 –4 7 2
Contrast
% Small Mammals
60
40
2
20
0
-20
-40
-60
RAK
LAK
BEK
NOR
VAR Breed
VAR Active
VAR Old
LAK Active
VAR Old
LAK Active
VAR Old
LAK Active
Contrast
Birds vs Small Mammals (log ratio)
4
2
0
-2
-4
RAK
LAK
BEK
NOR
VAR Breed
VAR Active
Contrast
Reindeer vs Small Mammals (log ratio)
3
2
1
0
-1
-2
-3
RAK
LAK
BEK
NOR
VAR Breed
VAR Active
Fig. 5 – Contrasts (with 95% c.i.) between and within the study regions in the diet of foxes. Small mammals contents are
expressed as percentage of the total volume of prey remnants, while relative amounts of birds and reindeers are expressed as
log-ratios against small mammals. See Fig. 3 for a description of the interpretation of the contrasts.
Contrast
Skuas
3
2
1
0
-1
-2
0.064
(0.070)
0.82 (0.23)
RAK
LAK
BEK
NOR
VAR Breed
VAR Active
VAR Old
LAK Active
Contrastt
Waders
4
3
2
1
0
-1
-2
-3
2.26
(0.42)
2.81 (0.43)
RAK
LAK
BEK
NOR
VAR Breed
VAR Active
VAR Old
LAK Active
Contrast
Passerines
P
6
4
2
0
-2
-4
6.45
(0.70)
3.35 (0.47)
RAK
LAK
BEK
NOR
VAR Breed
VAR Active
VAR Old
LAK Active
Fig. 6 – Contrast (with 95% c.i.) between and within the study regions in counts of skuas, waders and passerines (number
observed per km transect line). See Fig. 3 for a description of the interpretation of the contrasts.
dens. Waders also tended to have higher abundances in landscape blocks with recent breeding Arctic foxes than the reference blocks.
4.
Discussion
4.1.
Assessing the
MacDonald hypothesis
premises
of
the
Hersteinsson–
In this study, we assessed whether the geographic presenceabsence pattern of Arctic fox in low arctic tundra were asso-
ciated with differences in ecosystem state variables compatible with the climate-induced, trophic cascade proposed by
Hersteinsson and MacDonald (1992). The study area in eastern Finnmark offered a good case for such an assessment
being a relatively homogenous area in terms of topography
and geography and located at the climatic periphery of the
circumpolar tundra biome (Epstein et al., 2004). The den database of the Norwegian Arctic fox monitoring program (Andersen et al., 2004) offered a possibility to strategically design the
study so as to contrast areas (regions and landscape blocks)
with different degrees of recent records of Arctic fox activity.
468
B I O L O G I C A L C O N S E RVAT I O N
Following Hersteinsson and MacDonald (1992) there should
be a higher primary productivity and thus more plant biomass
where Arctic fox breeding has ceased compared to areas where
the Arctic fox are still breeding. Specifically, since warmer climate was predicted to be the ultimate driver of change, we particularly expected to find consistent differences in the biomass
climate sensitive plants. Moreover, for changes in vegetation
to result in a trophic cascade, we expected to find differences
in plants that are important to herbivores.
The results from the comparisons within VARANGER, the
only region with recent breeding records of the Arctic fox,
were quite consistent with these predictions. In VARANGER,
the landscapes surrounding Arctic fox dens without breeding
(active and abandoned dens) had substantially more biomass
of some dominant plant species than landscape blocks with
recent Arctic fox breeding. For instance, bilberry was approximately twice as abundant in blocks with abandoned dens
than in blocks with breeding dens. Similar patterns were evident for dwarf birch and the two graminoids mat grass and
stiff sedge. These four plant species are known to be climate
sensitive. Bilberry is harmed by low winter temperatures and
freeze-drying and are favored by a relatively thick snow cover
(Oksanen and Virtanen, 1995; Virtanen et al., 1999). Bilberry
has thus been predicted to respond under the current climate
trend with milder and snowier winters (Kullman, 2004). Correspondingly, Tømmervik et al. (2004) recently reported that
bilberry was one of the plant species that had increased the
most at permanent plots over a period of 40 years in birch forest in interior Finnmark. Both stiff sedge (Carlsson and Callaghan, 1994) and dwarf birch (Bret-Harte et al., 2001) have
shown strong growth-responses in warming experiments.
Moreover, dwarf birch contributes significantly to the recently
reported increase in the shrubbiness of southern Arctic tundra (Sturm et al., 2001). According to analyses of older data
sets from the same geographic region in Finnmark (Haapasaari, 1988; Virtanen et al., 1999), the mat grass appeared to be
rare compared to our current estimates (Table 2), demonstrating that it is now one of the dominant graminoids. The mat
grass is known to have its strong holds in the oceanic southern alpine areas in Norway (Moen, 1999). Thus it may recently
have increased in the low arctic due to milder and moister
climate.
All these four plant species, that may have shown a climate-induced increase in landscape block with ceased arctic
fox breeding, are reported to be important for some key tundra herbivores. Bilberry is the main forage plant for grey-sided
voles (Hörnfeldt, 2004), while the stiff sedge is a food plant
preferred by many herbivores, including lemmings (Brooker
et al., 2001). Although dwarf birch may not be very palatable
to herbivores it forms a habitat structure, which is important
to the grey-sided vole (Hambäck et al., 1998). The mat grass
appears to be a much-used winter food by alpine small rodents (Austrheim et al., in press), while it is resistant to grazing by large herbivores and may thus also increase due to high
stocking densities of ungulates (e.g. Pakeman, 2004; see
below).
The most abundant heath vegetation plant in Finnmark
tundra is crowberry (Table 2). This strongly non-palatable
evergreen shrub, exhibited a different abundance pattern
than the more palatable vascular plants in VARANGER as it
1 3 5 ( 2 0 0 7 ) 4 5 9 –4 7 2
was least abundant in landscape blocks with active dens.
Interestingly the same pattern was found in LAKSEFJORD.
This could be due to that crowberry probably is more tolerant
to cold soils than bilberry (Oksanen and Virtanen, 1995), and
that it interacts negatively with other plants (including bilberry) (Wardle and Zackrisson, 2005). Based on the biomass
pattern of palatable plants within VARANGER, one could also
expect according to the trophic-cascade scenario of Hersteinsson and MacDonald (1992), higher trophic levels to exhibit an equivalent trend of higher abundance in den blocks
without breeding Arctic foxes. Indeed, landscape blocks with
abandoned dens had the highest counts of insectivorous birds
(passerines and waders). Correspondingly, there were higher
relative proportions of birds in the diet of foxes in these landscape blocks. Counts of skuas were clearly highest in blocks
with active fox dens. The density of fox scats mirrored the
distribution of skuas with highest density in landscapes with
dens classified as active. It is noteworthy that the density of
fox scats in landscape blocks with breeding Arctic foxes was
lower than in den blocks without breeding foxes. A likely
interpretation of this result is that the great majority of fox
scats nowadays found on the tundra in Finnmark stem from
red foxes and that the productive landscape blocks with dens
classified as ‘‘active’’ are overtaken by the increasingly more
abundant red fox. The species origin of recent activity signs
at dens (prey remains, faeces and burrowing activity) without
direct observation of foxes may be uncertain. We, therefore,
suspect that an unknown proportion of dens classified as ‘‘active’’ actually are dens with presence of red fox. Thus the only
unambiguous evidence for Arctic fox activity at dens is provided when Arctic foxes were observed and this happened
most often for those categorized as breeding dens.
Unfortunately we were unable to obtain data that could be
used to investigate whether these landscape level differences
in plant abundance found in region VARANGER, translated
into different abundance and dynamics of voles and lemmings. These small herbivores form the most crucial link between primary producers (i.e. plants) and predators in tundra
ecosystems (Batzli et al., 1980; Krebs et al., 2003; Ims and Fuglei, 2005). One could, however, expect especially based on the
abundance pattern of bilberry and dwarf birch that den blocks
without breeding Arctic foxes would be most suitable for
grey-sided voles. This could be a reason for the generally
higher abundance of fox scats and skuas in these blocks.
The less erratic cyclic dynamics of the grey-sided vole than
the Norwegian lemming (Ekerholm et al., 2001), may have favoured the red fox over the arctic fox since it appears to be
less adapted to strong variation in food resources (Hersteinsson and MacDonald, 1992; Angerbjörn et al., 2004).
The rather consistent patterns both within and among trophic levels in region VARANGER was not present in LAKSEFJORD; i.e. the other region with Arctic fox dens. Within
LAKSEFJORD blocks with active fox dens and the reference
blocks were remarkably similar both in terms of plant variables and variables reflecting higher trophic levels. The generally high and spatially even frequencies of fox scats among
the landscape blocks in LAKSEFJORD, together with the lack
of recent Arctic fox breeding, calls into attention the possibility that this region now is wholly occupied by red foxes. This
suggestion is supported by recent data based snow tracking
B I O L O G I C A L C O N S E RVAT I O N
and photo recording at carcasses in this region (Killengreen
et al., unpublished).
Neither the comparisons at the regional level gave clues to
why the study regions apparently differed in terms of Arctic
fox presence. For instance, although VARANGER and LAKSEFJORD both had many Arctic fox dens they did not share other
ecosystem characteristics that made them distinct from the
three regions without recorded Arctic fox dens (BEKKARFJORD,
NORDKINN and RAKKONJARGA). The latter three regions were
in many respects similar to the reference blocks and blocks
with Arctic fox breeding in VARANGER. For this reason one
may question whether the den database adequately reflects
the status of the regions without recorded fox dens. Surveys
of Arctic fox populations are usually based on mapping of traditional dens (e.g. Angerbjörn et al., 1995, 1999; Roth, 2003). A
problem in this context is that the probability of den detection
(for instance by aerial surveys) is not likely to be uniform
among different study regions. Dens are difficult to detect in
areas where foxes may locate their dens in rugged terrain
among large stones (Prestrud, 1992), whereas they are far more
conspicuous when occurring as large burrow systems in level
terrain. The regions without known Arctic fox dens (NORDKINN, BEKKARFJORD and RAKKONJARGA) had large areas of
boulder fields leading to rejection of sampling areas (see Table
1). This problem was smaller in the regions with known fox
dens (VARANGER and LAKSEFJORD) and no sampling area
was rejected there. For this reason we have higher confidence
in the comparisons made within than between regions.
4.2.
fox
Alternative explanations for the retreat of the Arctic
A different climate change scenario, which could account for
the circumpolar retreat of the Arctic fox from low arctic tundra invokes impacts of climate on the population dynamics of
arctic small rodents such as voles and lemming (Ims and Fuglei, 2005). Inland Arctic foxes and most other predators in tundra rely on cyclic peak abundances of small mammals
(lemming and voles) every 3–5 years to breed successfully (Elton, 1942; Batzli et al., 1980; Angerbjörn et al., 1999; Wiklund
et al., 1999; Loison et al., 2001; Roth, 2003). The spatial pattern
of lemming and voles population dynamics in boreal and Arctic regions indicates that high amplitude population cycles
are ultimately dependent on long and stable cold winters (Elton, 1942; Finerty, 1980; Hansson and Henttonen, 1988). Shorter and less stable winters with frequent thawing and icing
events may act directly on small mammal winter survival
(Aars and Ims, 2002). Long-term trapping series of voles in
Fennoscandia indicate that the amplitude of rodent population cycles (especially with respect to abundance in spring)
has become substantially dampened over the last decades
(Hanski and Henttonen, 1996; Henttonen and Wallgren,
2001; Ekerholm et al., 2001; Yoccoz et al., 2001; Hörnfeldt
et al., 2005). Recent breeding failures and population declines
not only in Arctic foxes (Kaikusalo and Angerbjörn, 1995; Angerbjörn et al., 1995; Tannerfeldt et al., 2002), but also several
other raptors (Kjellén and Roos, 2000; Hörnfeldt et al., 2005),
coincide with these changes in their small rodent prey (Ims
and Fuglei, 2005). In the present paucity of data on the
dynamics of small rodents in the surveyed landscape blocks
1 3 5 ( 2 0 0 7 ) 4 5 9 –4 7 2
469
and regions, we may propose spatially variable relaxation of
small rodent grazing pressure as an alternative explanation
for observed differences in plant biomass. Indeed, experimental exclusion of small rodents from tundra habitats has
shown that plants like bilberry and stiff sedge increase in biomass when released from rodent grazing (Oksanen and Moen,
1994; Virtanen, 2000). Among several arctic rodent species
lemmings appear to be the species with both the largest impact on vegetation (Oksanen and Moen, 1994) and Arctic fox
breeding success (Angerbjörn et al., 1999; Elmhagen et al.,
2000; Tannerfeldt et al., 2002; Roth, 2003; Gauthier et al.,
2004). Could it therefore be that the few remaining Arctic
fox breeding territories on the low arctic tundra now coincide
with a few remaining local lemming ‘‘cold spots’’?
Apart from the ecosystem changes with a climatic origin
and a circumpolar scope discussed above, several alternative
explanations with a more limited reference to the critical situation for the Arctic fox in Fennoscandia have been proposed
(see Hersteinsson et al., 1989; Angerbjörn et al., 1995; Linnell
et al., 1999a). One of these involves overabundance of semidomestic reindeer, which in Finnmark has been claimed to
render an ‘‘ecological disaster’’ (Moen and Danell, 2003). Speculations about cascading effects of reindeer overgrazing ultimately harming the Arctic fox (Angerbjörn, 1998; Elgvin and
Klingsheim, 2002) as well as other predators (Tømmeraas,
1993; Kjellén and Roos, 2000; Ratcliffe, 2005) have been made.
Indeed, a high grazing pressure by reindeer could be thought
of as an alternative to the climatic explanation for the surprisingly high abundance of the grazing resistant mat grass
in landscape blocks with ceased Arctic fox breeding. However,
our analysis of reindeer pellet counts, which is a reliable index of reindeer density (Edenius et al., 2003), gave no indication that differential use of landscape blocks or regions by
reindeers was related to current spatial distribution of the
Arctic fox nor mat grass.
5.
Conclusion
By the present study we have provided a first assessment of
whether changes in ecosystem structure according to a proposed climate change scenario proposed by Hersteinsson
and MacDonald (1992) could underlie the retreat of the Arctic
fox from low arctic tundra. Our analysis relied on data from a
spatially extensive, but short-term, campaign-based study. Of
course such an approach provides only a snap-shot picture of
a highly dynamic system (see Krebs et al., 2003 for a discussion). On the other hand, it represents one of the few means
available for indicating processes taking place at large scales
(Callaghan et al., 2004b; Miller et al., 2004; Hastings et al.,
2005).
We found support for several of the premises of Hersteinson–MacDonald’s hypothesis within VARANGER, which was
the only geographic region where contrast analyses involving
areas with recent breeding of Arctic fox could be made. In
VARANGER landscapes surrounding dens where Arctic fox
breeding has ceased appear nowadays to be more productive
than where the Arctic fox is still breeding. This higher productivity was indicated by state variables at several trophic
levels; i.e. biomass of plant species important to herbivores,
number of insectivorous and predatory birds as well as fre-
470
B I O L O G I C A L C O N S E RVAT I O N
quency of scats likely to stem from red foxes. A climate connection was suggested by the higher biomass of plants favored by warmer climate. However, from our data we
cannot rule out an alternative scenario of relaxed grazing
pressure of lemmings, recently showing dampened population cycles in Fennoscandia. In any case, the process links between climate, herbivore population dynamics and the
abundance of the two fox species on the tundra need to be
elucidated more deeply. Indeed, the fact that we failed to find
patterns at the regional level consistent with those found
within the region VARANGER indicates that large-scale aspects of processes affecting the Arctic fox may have escaped
our study design or the Norwegian Arctic fox monitoring program. In particular, we believe that the spatial pattern of the
temporal change in the dynamics of lemmings, the key food
resource for the Arctic fox in tundra habitats require special
attention together with alternative methods for Arctic fox
monitoring.
Acknowledgements
This project was supported financially by the Norwegian
Directorate of Nature Management and the Research Council
of Norway. Field assistance was provided by Pieter Beck, Tina
Dahl, Ingrid Jensvold, Bjørn Hugo Kristoffersen, Stein Tore
Pedersen, Arne Petter Sarre, Guro Saurdal, Cecilie Steffen
and Alfred Ørjebu. Comments on the manuscript by Eva Fuglei and two anonymous referees are much appreciated.
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