Possible impact of snow depth and ungulate carcasses onred fox (Vulpes vulpes) populations in Norway, 1897–1976

V. Selas & J. O. Vik�

Department of Ecology and Natural Resource Management, Norwegian University of Life Sciences, As, Norway

Keywords

carcasses; rodents; snow; ungulates; Vulpes

vulpes.

Correspondence

Vidar Selas, Department of Ecology and

Natural Resource Management, Norwegian

University of Life Sciences, PO Box 5003,

N-1432 As, Norway.

Email: vidar.selas@umb.no

�Current address: Division of Zoology,

Department of Biology, University of Oslo,

PO Box 1050 Blindern, N-0316 Oslo,

Norway.

Received 9 March 2005; accepted

8 September 2005

doi:10.1111/ j.1469-7998.2006.00048.x

Abstract

During the 1900s, the number of red foxes Vulpes vulpes increased in northern

Europe. At higher altitudes and latitudes, red fox populations are likely to be

limited by thick snow cover, which makes small rodents less available. The

negative effects of snow could, however, be compensated for by high ungulate

numbers, because of increased availability of carcasses in snow-rich winters. In the

period 1897–1932, the number of foxes (mainly red foxes) killed was negatively

related to snow depth indices in 13 of the 17 Norwegian counties. During

1947–1976, after a strong increase in ungulate and red fox numbers, the number

of red foxes killed was negatively related to snow in only one county. The counties

where ungulate density increased the most also had higher increases in the number

of red fox bounties paid. The absence of large predators may at least partly be

responsible for the strong increase in red fox populations, because eradication of

large predators such as wolf Canis lupus in the late 1800s and early 1900s probably

was a necessary condition for the strong increase in ungulate numbers, especially

roe deer Capreolus capreolus.

Introduction

The red fox Vulpes vulpes is a generalist and keystone

predator that in Fennoscandia has a strong impact on the

population level of both prey and competitive predator

species (Marcstrom, Kenward & Engren, 1988; Marcstrom

et al., 1989; Lindstrom et al., 1994, 1995; Selas, 1998a;

Smedshaug et al., 1999). During the 20th century, there was

a strong increase in red fox numbers in northern Europe

(Lund, 1963; Hjeljord, 1980). In this period, the red fox may

have benefited from reduced hunting pressure and reduced

populations of natural enemies. Interspecific killing among

carnivores is common (Palomares & Caro, 1999), and

mesopredator release and trophic cascades after removal of

top predators may be a general phenomenon (Crooks &

Soule, 1999). However, red foxes may have also benefited

from improved carrying capacity. Major changes in carrying

capacity could have been caused by general increases in food

availability due to regional warming (Semb-Johansson,

1988; Hersteinsson & Macdonald, 1992), increased supply

of human garbage due to increased living standards (Lund,

1963; Hjeljord, 1980), increased populations of small ro-

dents due to modern forestry (Christiansen, 1979; Hentto-

nen, 1989) and increased availability of ungulate carcasses

(Smedshaug & Sonerud, 1997; Selas, 1998b). Here we use

hunting indices to evaluate the latter of these (not mutually

exclusive) hypotheses.

At higher altitudes and latitudes, winter food is probably

a limiting factor for red fox populations, not only

by influencing winter survival but also by affecting

fox reproduction, through their body condition in spring.

The red fox is a less efficient hunter of resident medium-

sized prey, such as mountain hare Lepus timidus and

forest grouse, although it may scavenge on prey remains

from predators specialized on these prey, such as goshawk

Accipiter gentilis and eagle owl Buteo buteo. But unless

red foxes can benefit from human garbage, the main

food resources in winter will probably be small rodents

and ungulate carcasses (Lund, 1962; Jedrzejewski &

Jedrzejewska, 1992). In years with deep snow, which

makes small rodents less available (Halpin & Bissonette,

1988; Jedrzejewska & Jedrzejewski, 1998), carcasses may

be of vital importance for both winter survival and

spring condition, and thus the overall reproduction, of red

foxes.

It has commonly been assumed that foxes benefit from

carcass leftovers from wolf Canis lupus and lynx Lynx lynx,

but it should be noted that these predators also kill foxes

(Jedrzejewska & Jedrzejewski, 1998), and that their leftovers

therefore may not be easily available for foxes. In Norway,

both wolf and lynx were almost eradicated during the period

1850–1900 (Johnsen, 1929). As the strongest increase in red

fox numbers occurred several decades later, there is no

Journal of Zoology 269 (2006) 299–308 c� 2006 The Authors. Journal compilation c� 2006 The Zoological Society of London 299

Journal of Zoology. Print ISSN 0952-8369

obvious link between the population level of red fox and

large predators.

Wolf eradication may, however, have had a delayed effect

on red fox populations. If wolves are removed, ungulates

will usually increase in number and eventually reach a

carrying capacity determined by food availability (e.g.

Okarma, 1995; Boertje, Valkenburg & McNay, 1996).

Hunting by man may to some extent compensate for the

lack of natural predation, but humans are in general

less selective with regard to the body condition of their

prey (e.g. Boyd et al., 1994; Solberg et al., 2000). If wolf

extermination results in increasing populations and/or

higher numbers of ungulates in poor condition, we should

expect a higher total number of ungulates to die from

starvation in snow-rich winters (e.g. Okarma et al., 1995).

Their carcasses can then be utilized by foxes with no risk of

being killed by wolves, improving food availability for red

foxes in critical periods.

During the 20th century, the number of moose Alces

alces, red deer Cervus elaphus and reindeer Rangifer taran-

dus increased dramatically in Norway (Jacobsen & Ander-

sen, 1990; Langvatn, 1990; Skogland, 1990). In addition, roe

deer Capreolus capreolus invaded the country, and became a

common ungulate species in large parts of the country

(Østbye & Bjørnson, 1990). The roe deer is probably the

most important species for the red fox, because it suffers

high mortality in snow-rich winters, when it may even be

killed by the red fox (Kjos-Hanssen, 1962; Borg, 1970;

Raiby, 1970; Cederlund & Lindstrom, 1983). The roe deer

is also less regulated by man than the larger cervid species,

and therefore a higher proportion of the population will die

for reasons other than hunting.

Small rodent fluctuations influence the reproduction of

red foxes (Englund, 1970; Lindstrom, 1989), especially in the

north, where the fluctuations are strongest (Hansson &

Henttonen, 1985). According to studies from the late 1900s

(Englund, 1970; Lindstrom, 1989), fox reproduction should

be expected to be influenced mainly by rodent numbers in

the current spring and summer. However, as these studies

were carried out in a period when there probably was a

relatively high availability of carcasses and human leftovers

in winter, they may have missed the possible positive impact

of high rodent numbers before snow-rich winters, as well as

the possible negative impact of deep snow before rodent

peak years.

To document any impact of winter conditions and un-

gulate carcasses on red fox reproduction in Norway, we first

studied the covariation between the number of fox bounties

paid and snow depth measurements within each county

before and after the strong increase in ungulate numbers in

the mid-1900s. Thereafter we used hunting statistics from

the period of ungulate increase to test for relationships

between ungulate and red fox populations. Because the red

fox is difficult to control by hunting (Hewson, 1986),

fluctuations in hunting statistics of this species will usually

reflect fluctuations in the relative population levels (e.g.

Kolb & Hewson, 1980). Because of the general high mortal-

ity and reproduction rate of foxes, we assumed that most

bounties paid referred to juveniles, and thus reflected annual

reproduction.

Methods

Hunting bounties

Bounties were paid for foxes in most Norwegian counties

during 1880–1932 and 1946–1976 (Central Bureau of Statis-

tics of Norway, 1978), referred to as ‘period 1’ and ‘period 2’

below. In Finnmark, bounties were not paid for foxes killed

in winter during 1910–1932, and therefore we omitted this

county from our analyses. Red foxes and arctic foxesAlopex

lagopus were not distinguished in the statistics, but after the

strong decline in the arctic fox populations in 1905–1910

(Johnsen, 1929; Høst, 1935), most bounties paid will refer to

red foxes. Before this decline, Collett (1912) estimated arctic

foxes to constitute c. 20% of the total number of foxes killed

in Norway, although with a much higher proportion in

North Norway (Nordland, Troms and Finnmark) than in

South Norway.

Timing of population indices and covariates

The majority of foxes hunted were probably killed during

winter (Johnsen, 1929) and reported at the end of the winter.

This is confirmed by the data from Finnmark, where the

mean annual number of foxes killed was 1176.3 (� 691.6 SD)

during 1880–1909 and only 33.96 (� 23.2 SD) during

1910–1932, when bounties were paid only in summer. Thus,

to reveal any impact of snow on red fox reproduction, we

compared the red fox index with snow indices of the

previous year. For each county, the red fox index is the

annual number of fox bounties paid, and the snow indices

are the maximum snow depth measured at the selected

meteorological station in March and April. Snow depth

measurements provided by the Norwegian Meteorological

Institute were available from one to two stations per county

from 1896 onwards. Hence, we analysed for relationships

between red fox hunting bags and snow depth in the

previous year for the periods 1897–1932 and 1947–1976.

Meteorological data

For counties with two meteorological stations, we selected

the one situated closest to the coast (Akershus, Telemark,

Vest-Agder, Hordaland, Sogn og Fjordane, Møre and

Romsdal, Sør-Trøndelag) or at the lowest altitude (Hed-

mark, Oppland), based on the assumption that red foxes

were most abundant in coast-near areas and at low altitudes.

For Buskerud, we used a more coast-near station situated in

Telemark, close to the border of Buskerud, rather than any

of the two stations situated at higher altitudes north-west in

Buskerud.

Snow depths

In Norway, the amount of snow left in late winter or spring

will often reflect past winter conditions. We therefore used

Journal of Zoology 269 (2006) 299–308 c� 2006 The Authors. Journal compilation c� 2006 The Zoological Society of London300

Fox numbers, snow depth and ungulate carcasses V. Selas and J. O. Vik

snow depth in March or April as explanatory variables.

During 1896–1932, there was a highly significant correlation

between the two stations, for both March and April snow

depths, for most of the 11 counties with two sets of snow

measurements. The exceptions were the large counties

Hedmark (March: r=0.14, P=0.470), Oppland (March:

r=0.49, P=0.470; April: r=0.29, P=0.207), Sogn og

Fjordane (April: r=0.12, P=0.528) and Troms (March:

r=0.09, P=0.610; April: r=0.09, P=0.609).

North Atlantic Oscillation (NAO)

Because not all snow indices used may be representative for

the whole county, we also used the NAO for December–

March (Hurrell, 1995) as an index to account for year-to-

year variation in winter snow conditions. The NAO is an

alternation in atmospheric pressures over the Atlantic

Ocean. In Norway, there is a positive relationship between

the NAO index on the one hand and winter temperatures

and precipitation on the other (Hurrell, 1995). At lower

altitudes inhabited by red foxes, a high NAO index will

usually be associated with less snow accumulation in late

winter and spring (Mysterud et al., 2000), partly because

much of the precipitation during winter comes as rain and

partly because of an earlier thaw. Although temperature

variability has been better simulated by variations in atmo-

spheric circulation patterns in recent years than for the

period 1900–1924 (Hanssen-Bauer & Førland, 2000), we

found a significant negative correlation between the NAO

index and snow depth in April (Po0.050) during 1896–1932

for seven of the 17 counties (all situated in South Norway).

For three of the remaining counties, there was a significant

negative correlation between NAO and snow depth in May.

During 1946–1976, the NAO index was significantly nega-

tively correlated with snow in April in six counties.

Rodent indices

For period 1, information on rodent numbers (low=0 or

high=1) is given by Wildhagen (1952) for eastern (Østfold,

Vestfold, Akershus, Hedmark, Oppland, Buskerud), south-

ern (Telemark, Aust-Agder, Vest-Agder), western (Roga-

land, Hordaland, Sogn og Fjordane), central (Møre og

Romsdal, Sør-Trøndelag, Nord-Trøndelag) and northern

Norway (Nordland, Troms, Finnmark). Only for Sør-Trøn-

delag there was a significant correlation between the rodent

index and the snow depth index used (snow year t vs.

rodents year t�1; r=�0.34, P=0.046). For period 2,

information on rodent peaks is fromMyrberget (1965, 1982)

and Christiansen (1983). For both periods, the red fox index

was compared with the rodent index of the 2 previous years.

Raptor index

We used the number of goshawks hunted as a covariate to

account for variation that might otherwise obscure any

effects of snow and ungulate carcasses. The goshawk index

may reflect fluctuations in small game, which are important

prey for this species, and also in rodent numbers, which

often fluctuate in synchrony with small game (Hagen, 1952;

Selas, 1997; Selas & Steel, 1998). Additionally, the goshawk

index may reflect changes in hunting effort (Johnsen, 1929;

Myrberget, 1988), which would otherwise be difficult to

account for. Hence, the main purpose of using this index

was to improve the statistical power of the regression

models. However, we did not use the goshawk index for the

counties Sogn og Fjordane, Møre og Romsdal, Sør-Trønde-

lag, Nord-Trøndelag and Nordland for period 1, because of

a highly significant positive correlation with the rodent

index of the previous year. For the remaining counties,

goshawk numbers were not significantly related either to

rodent numbers or to the snow indices used. Because

goshawks also were hunted throughout the year, a time lag

between this species and the red fox should not be expected

unless nestlings or fledglings accounted for the majority of

the hawk bounties paid.

Variable transformation

Hunting indices were converted to annual relative rates of

change by log transformation followed by differencing. In

the fox–snow analyses, we also differenced the explanatory

variables. The transformation improved the statistical prop-

erties of the time series, stabilizing the variance and remov-

ing any exponential trend (i.e. any trend in abundance is

replaced by a nonzero expectation in growth rate).

Regression models of fox versus snow

For each county and each of the two periods, we constructed

a multiple linear regression model with the fox index as

response variable, and snow, rodents and hawks as expla-

natory variables. In a forward procedure, all explanatory

variables with a P-value o0.10 were selected, given that the

sign of the parameter estimate was as expected (negative for

snow, positive for NAO and the rodent/hawk indices). In

the case of serially correlated residuals, we substituted the

response variable with the residuals from an autoregression

model, with autoregressive order corresponding to the lag of

the autocorrelation in the original residuals.

Population growth of fox and cervids

The strongest increase in both red fox and ungulate popula-

tions occurred during the 1930s and 1940s, and before the

strongest increase in human living standard (Fig. 1). In

testing for a possible influence of ungulate population levels

on red fox population growth, we could not use hunting

statistics for the whole period because few bounties were

paid for foxes from 1933 to 1945 (Fig. 1). Instead, we defined

an ‘index of population growth’ for red fox and ungulates.

For each species and county, the index was the average

number killed per year in 1951–1960, divided by the average

for 1921–1930 (data taken from Central Bureau of Statistics

of Norway, 1978). The three counties from North Norway,

with only domestic reindeer, were not used because changes

in reindeer management may have also influenced the

Journal of Zoology 269 (2006) 299–308 c� 2006 The Authors. Journal compilation c� 2006 The Zoological Society of London 301

Fox numbers, snow depth and ungulate carcassesV. Selas and J. O. Vik

availability of carcasses in this region (Skjenneberg &

Slagsvold, 1968).

Moose and reindeer indices

In the analyses we included only counties with at least

150 deer killed during 1921–1930. For moose, this criterion

was fulfilled for the nine eastern and central counties of

Østfold, Vestfold, Akershus, Hedmark, Oppland, Buskerud,

Telemark, Sør-Trøndelag and Nord-Trøndelag. The re-

maining six southern and western counties had less than

75 moose killed, but here there was a sufficient number of

reindeer killed. Also in Oppland, Buskerud and Telemark,

more than 150 reindeer were killed during 1921–1930. Red

deer was not included in the analyses because there were too

few counties with enough kills before 1930.

Roe deer indices

Few roe deer were hunted before 1950, and therefore it was

not possible to compare the increase in bounties paid for red

foxes in each county with a population increase index of roe

deer. During 1930–1950, the roe deer populations probably

reached their highest levels in the counties where the species

first occurred (the species spread from the south-east). We

therefore ranked the South Norwegian counties according

to the first year of continuous annual roe deer hunting

(Central Bureau of Statistics of Norway, 1978). Against this

ranking index we regressed the population-growth index for

red fox.

We assumed that the annual number of ungulates hunted

is an appropriate index of their population levels. However,

because of hunting restrictions given by the game autho-

rities, hunters are not allowed to respond to population

increases of cervids in the same way as for the red fox.

Hence, there will probably be a delay in the increase in the

hunting statistics of ungulates compared with the increase in

their real population levels. This was especially evident for

the moose statistics in some counties in the early 1920s,

where the number of moose killed suddenly increased from a

relatively low to a much higher level. For these counties,

we omitted the first 2 or 3 years of low values when we

calculated the mean annual number of moose hunted during

the 1920s.

Regression models of fox versus cervids

We used linear regression when comparing population-

growth indices of red fox and cervids (n is the number of

counties). The population-growth index for red fox was also

compared with human population densities, because in-

creased living standards in the 1950s, and thus increased

availability of human garbage, may have contributed to the

red fox increase. As, in general, there will be an increase in

winter severity with increasing altitude and latitude, in-

creased availability of cervid carcasses or human leftovers

may have been most important in mountains and in north-

ern counties. We therefore included latitude (measured

midway between the northernmost and southernmost point

in each county) and the proportion of mountains as addi-

tional explanatory variables in models with significant

relationships between fox and cervids.

Results

Red fox indices versus snow depth, rodentsand hawks, 1897–1932

In multiple regression models for period 1 (1897–1932), the

red fox index was significantly related to one of the snow

indices (snow depth inMarch or April, or the NAO index) in

13 of the 17 counties (Table 1, Fig. 2). Additionally, in Sogn

og Fjordane, there was a tendency for a negative relation-

ship with snow depth in April (n=28,R2=0.11,P=0.079).

For the three large counties of Hedmark, Nord-Trøndelag

and Nordland, no relationships with snow or the NAO

index were found. In two other large counties, Oppland

and Hordaland, as well as in the small county Vestfold,

there was a significant relationship only with the NAO

index, and not with March or April snow depths (Table 1).

The NAO index was, however, negatively related to snow

depth in April in both Oppland (n=28, r=�0.37,P=0.043) and Vestfold (n=28, r=�0.64, Po0.001).

In five of the 13 counties with effect of snow on the red fox

index in period 1, there was also a positive relationship

between the fox index and rodent numbers in year t�1 and/

0

1500

3000

4500

6000

Roe

dee

r

0

2500

5000

7500

10 000

Moo

se Roe deer

Moose

0

150 000

300 000

450 000

600 000

GN

P (

mill

ion

kr)

0

10 000

20 000

30 000

40 000R

ed fo

x GNP

Red fox

0

1000

2000

3000

4000

Red

dee

r

0

2500

5000

7500

10 000

Rei

ndee

r

1890 1910 1930 1950 1970Year

Red deer

Reindeer

Figure 1 Number of red fox Vulpes vulpes, moose Alces alces, roe

deer Capreolus capreolus, red deer Cervus elaphus and reindeer

Rangifer tarandus hunted in Norway from 1889 to 1968, and the gross

national product of Norway (in 2000 prices), reflecting human living

standard. Data taken from Central Bureau of Statistics of Norway.

Journal of Zoology 269 (2006) 299–308 c� 2006 The Authors. Journal compilation c� 2006 The Zoological Society of London302

Fox numbers, snow depth and ungulate carcasses V. Selas and J. O. Vik

or t�2 (Table 1). There was a highly significant positive effectof rodents in year t�2 also in Hedmark (n=35, R2=0.27,

P=0.001), and a positive effect of rodents in both year t�1and t�2 in Nord-Trøndelag (n=35, total R2=0.50,

P (t�1)=0.008, P (t�2) o0.001) and Nordland (n=35,

total R2=0.68, P (t�1) o0.001, P (t�2) o0.001). The

goshawk index contributed to explain the red fox index in

seven of the 12 counties where this index was used (Table 1).

Table 1 Results from multiple regression models where the response variable is the first difference of the log-transformed number of red foxes

Vulpes vulpes hunted (or an ar1-model if intercorrelated residuals) in year t during 1897–1932 and 1947–1976, and the explanatory variables are,

respectively, the first difference of a snow index [maximum snow depth (cm) in March or April, or the NAO index], rodent numbers (low=0,

high=1) and the log-transformed number of goshawks hunted

County Explanatory variable Parameter estimate SE d.f. R2 AIC P

1897–1932

ØF (ar1) Intercept 0.032 0.028 1 �105.25

Snow April, t�1 �0.003 0.001 1 0.23 �111.79 o0.001

Hawks hunted, t 0.204 0.079 1 0.38 �116.37 0.016

VF Intercept �0.005 0.053 1 �71.17

Hawks hunted, t 0.322 0.108 1 0.18 �76.27 0.005

NAO, t�1 0.056 0.025 1 0.29 �79.30 0.033

AK Intercept �0.026 0.060 1 �41.55

Hawks hunted, t 0.548 0.158 1 0.44 �53.48 0.002

Snow April, t�1 �0.003 0.001 1 0.54 �56.20 0.045

OP (ar1) Intercept �0.001 0.058 1 �63.30

Rodents, t�2 0.230 0.081 1 0.17 �67.83 0.008

NAO, t�1 0.069 0.028 1 0.30 �71.77 0.021

BU (ar1) Intercept 0.009 0.058 1 �66.21

Snow April, t�1 �0.004 0.001 1 0.22 �72.99 0.004

TE (ar1) Intercept 0.007 0.062 1 �46.39

Rodents, t�1 0.302 0.119 1 0.14 �47.97 0.020

Hawks hunted, t 0.564 0.216 1 0.27 �49.84 0.017

Snow March, t�1 �0.002 0.001 1 0.43 �53.78 0.028

AA (ar1) Intercept �0.011 0.051 1 �72.73

Snow April, t�1 �0.010 0.003 1 0.24 �79.86 0.004

VA (ar1) Intercept �0.003 0.035 1 �100.91

Snow April, t�1 �0.004 0.002 1 0.13 �103.36 0.043

RO Intercept 0.010 0.043 1 �91.90

Snow March, t�1 �0.006 0.003 1 0.12 �94.49 0.039

HO Intercept 0.004 0.047 1 �73.61

Hawks hunted, t 0.619 0.162 1 0.16 �77.56 o0.001

NAO, t�1 0.067 0.024 1 0.28 �81.05 0.009

Rodents, t�1 0.222 0.090 1 0.40 �85.31 0.020

MR Intercept �0.022 0.036 1 �93.00

Snow April, t�1 �0.003 0.001 1 0.22 �99.70 0.001

Rodents, t�1 0.127 0.056 1 0.29 �101.14 0.030

Rodents, t�2 0.122 0.054 1 0.39 �104.44 0.032

ST (ar1) Intercept 0.004 0.076 1 �45.12

Snow March, t�1 �0.004 0.002 1 0.17 �49.74 0.019

Hawks hunted, t�1 0.312 0.135 1 0.29 �53.08 0.028

TR Intercept �0.082 0.084 1 �26.15

Hawks hunted, t 0.425 0.172 1 0.19 �31.34 0.020

Snow April, t�1 �0.006 0.002 1 0.31 �34.91 0.012

Rodents, t�2 0.391 0.124 1 0.39 �37.71 0.004

Rodents, t�1 0.389 0.131 1 0.53 �44.77 0.006

1947–1976

MR Intercept 0.024 0.040 1 �78.97

Snow April, t�1 �0.002 0.001 1 0.21 �83.82 0.021

Rodents, t�1 0.168 0.077 1 0.33 �86.78 0.037

Only counties where snow was found to be significant are listed. The variables are listed in the direction they were obtained in a forward selection

procedure, and cumulative values are given for R2 and AIC. County abbreviations as in Fig. 2.

NAO, North Atlantic Oscillation.

Journal of Zoology 269 (2006) 299–308 c� 2006 The Authors. Journal compilation c� 2006 The Zoological Society of London 303

Fox numbers, snow depth and ungulate carcassesV. Selas and J. O. Vik

Red fox indices versus snow depth, rodentsand hawks, 1947–1976

In period 2 (1947–1976), after the strong increase

in cervid and red fox numbers, only one county (Møre

og Romsdal) showed a negative covariation between

snow depth and red fox index (Table 1). In all counties

except Østfold and Vestfold, there was a significant positive

relationship with the rodent index (Po0.05), usually of

year t�1. Only in the two northern counties of Nordland

and Troms, the fox index was correlated with the rodent

index in year t�2. For Akershus, Hedmark, Buskerud

and Aust-Agder, the goshawk index was also obtained

in the model (Po0.10). For Vestfold, the goshawk index

was the only variable that was selected (R2=0.32,

P=0.005).

Red fox indices versus cervid numbers

Counties with early introduction of roe deer hunting showed

stronger increases in the red fox index from the 1920s to

the 1950s (Table 2, Fig. 3). In a multiple regression

model, there was also a significant positive effect of latitude

(n=15, total R2=0.72, Po0.001 for roe deer, 0.003

for latitude). For the eastern and central counties, there

was a positive relationship between the increase in red

fox and moose indices (Table 2, Fig. 3). Here, there

was a tendency for an additional positive effect of the

TR

NO

NT

ST

HEOP

MR

SF

BU

TE

AAVA

HO

RO

AK

ØFVF

Figure 2 Counties with a relationship between fox bounties and snow

indices of the previous winter during 1897–1932 (shaded areas). The

counties are Østfold (ØF), Vestfold (VF), Akershus (AK), Hedmark

(HE), Oppland (OP), Buskerud (BU), Telemark (TE), Aust-Agder (AA),

Vest-Agder (VA), Rogaland (RO), Hordaland (HO), Sogn og Fjordane

(SF), Møre og Romsdal (MR), Sør-Trøndelag (ST), Nord-Trøndelag

(NT), Nordland (NO) and Troms (TR). P-values are given in Table 1.

Table 2 Results from simple regression models (n is the number of

counties) where the response variable is the increase in the number of

bounties paid for red foxes Vulpes vulpes in each county from

1921–1930 to 1951–1960, and the explanatory variables are, respec-

tively, the increase in the number of moose Alces alces and reindeer

Rangifer tarandus hunted in the same period (positive relationship),

the county’s ranking with regard to the first year of continuous annual

roe deer Capreolus capreolus hunting (negative relationship) and the

human population in 1930

Counties

Moose Reindeer

Roe

deer Humans (km2)

R2 P R2 P R2 P R2 P

East and central,

n=9

0.52 0.029 – – 0.30 0.258 0.09 0.430

South and west,

n=6

– – 0.92 0.003 0.02 0.687 0.05 0.655

All, n=15 – – – – 0.40 0.011 0.01 0.750

Eastern and central counties are ØF, VF, AK, HE, OP, BU, TE, ST, NT.

Southern and western counties are AA, VA, RO, HO, SF, MR. County

abbreviations are as in Fig. 2. ‘–’ is shown where the species in

question is not present.

Roe deer ranking index

r = −0.63

0 2 4 6 8 0 4 8 12 16Moose increase

1920–1950s

r = 0.72

0

1

2

3

4

5

Red

fox

incr

ease

192

0–1

950s

0 5 10 15 20 25Reindeer increase

1920–1950s

r = 0.79

Figure 3 Increase in the number of bounties paid for foxes (mainly red

fox Vulpes vulpes) in each county from 1921–1930 to 1951–1960, in

relation to increase in the number of reindeer Rangifer tarandus and

moose Alces alces hunted in the same period and the county’s

ranking with regard to the first year of continuous annual roe deer

Capreolus capreolus hunting.

Journal of Zoology 269 (2006) 299–308 c� 2006 The Authors. Journal compilation c� 2006 The Zoological Society of London304

Fox numbers, snow depth and ungulate carcasses V. Selas and J. O. Vik

proportion of mountains (n=9, total R2=0.74, P=0.006

for moose, 0.063 for mountains). In the southern

and western counties, red fox and reindeer were positi-

vely correlated (Table 2). The result was also significant

if the three eastern counties with reindeer hunting were

included (n=9, R2=0.62, P=0.012; Fig. 3). There was

no additional effect of latitude or mountains. We found

no relationships between red fox growth and human

density (Table 2).

Discussion

The fox index was significantly related to snow depth indices

in 13 of the 17 counties in period 1, 1897–1932, but in only

one county in period 2, 1947–1976. Hence, the apparent

negative effects of snow on fox population dynamics in

period 1 may have been offset by the increased availability

of carcasses after the strong increase in ungulate numbers

during 1930–1950. Another indication of the stronger im-

pact of snow in period 1 is that rodent numbers in year t�2,i.e. 1 year before fox reproduction, seemed to be more

important than in period 2. This could be because the

positive effect of high rodent numbers on the body condition

of red foxes before a snow-rich winter was more important

for the reproductive effort in the succeeding year when the

availability of ungulate carcasses was low. In period 2,

rodent numbers in year t�1 seemed to be most important, at

least in South Norway, possibly because at that time fox

populations were seldom so depressed after the winter that

they could not respond by increased reproduction in rodent

peak years.

The study supports our hypothesis that in periods with

low availability of carcasses, negative effects of deep snow

on red fox movements (Meia & Weber, 1995; see also

Murray & Lariviere, 2002) and rodent hunting success

(Jedrzejewski & Jedrzejewska, 1992) also influence fox

population levels, through survival or reproduction. The

results are probably robust because errors in hunting statis-

tics are unlikely to correlate with snow conditions in the

previous winter or with rodent peak years. The counties

where we found no relationship with snow during

1897–1932, Hedmark, Nord-Trøndelag and Nordland, are

rather large, so that the snow data used may not have

correlated well with the county as a whole, or the counties

are simply too heterogeneous to be represented by a single

snow index.

As expected, the fox index was positively related to

rodent numbers in several counties in both periods. Regard-

less of the phase of the rodent cycle, a thick snow cover may

positively influence rodent densities in spring, by protecting

the rodents against low temperatures and predation during

winter (Lindstrom & Hornfeldt, 1994). However, any posi-

tive effects of snow on rodent numbers in spring could

apparently not compensate for the negative effect of snow

on red fox numbers in period 1. For some counties also the

number of goshawks rewarded was positively related to the

number of bounties paid for foxes. The goshawk index may

have accounted for variations in hunting effort, but at least

for some counties it may also have been a better predictor

for fluctuations in prey availability than the rodent index. In

Norway, there will usually be a synchronous fluctuation in

population levels of small rodents and small game, and

therefore most predator species feeding on one or both of

these prey groups, such as the red fox and the goshawk,

could be expected to show some similarities in annual

reproduction and survival.

Red foxes are expected to starve in winters with deep

snow if the availability of carcasses is low (Jedrzejewski &

Jedrzejewska, 1992), reducing both the number of reprodu-

cing individuals and mean litter sizes. For arctic foxes in

Sweden, supplemental feeding during winter increased the

number of reproducing individuals in spring (Angerbjorn

et al., 1991). Because the main negative effect of snow is that

small rodents become less available, snow may depress fox

reproduction even when rodents are abundant. In fact,

arctic foxes have failed to reproduce in peak years of

lemming Lemmus lemmus in Finnish Lapland (Kaikusalo &

Angerbjorn, 1995). In snow-rich areas, the most important

effect of high rodent populations is probably increased cub

survival during summer (Tannerfeldt, Angerbjorn & Arvid-

son, 1994; Angerbjorn et al., 1995; Angerbjorn, Tannerfeldt

& Erlinge, 1999; Strand et al., 1999).

The growth in red fox populations during 1921–1950 was

positively associated with the growth in cervid numbers,

supporting our hypothesis that increased carcass availability

because of high ungulate numbers may compensate for the

negative effects of severe winters, and thus increase the

carrying capacity for foxes. It is important that the supply

of carcasses of ungulates died from diseases or starvation

will usually peak in late winter, when the availability of

other food resources is low (Jedrzejewska & Jedrzejewski,

1998). In Norway, populations of forest-living ungulates

increased dramatically from 1940 to 1960, and reached

levels higher than known from any other period in history

(Jacobsen & Andersen, 1990; Langvatn, 1990; Østbye &

Bjørnson, 1990). This was also the period with the strongest

increase in red fox populations.

Even though we found no relationship between the

growth in fox populations and human density, red

foxes may have also benefited from increased supply of

garbage because of improved living standards (e.g.

Panek & Bresinski, 2002), but this factor cannot explain the

regional correlation between red fox and ungulates. An

alternative explanation for the regional correlation between

red fox and moose populations is that both moose and field

vole Microtus agrestis populations increased after the

introduction of modern forestry in the 1950s (e.g. Hansson,

1978; Andersen, 1991), and that the red fox flourished

in response to increases in vole populations. However, the

strongest increase in red fox populations occurred

before any significant landscape changes because of forestry.

Besides, field voles are not likely to benefit red foxes in

snow-rich winters, because this rodent species rarely moves

above the snow cover (Sonerud, 1986; Jacobsen & Sonerud,

1993).

Journal of Zoology 269 (2006) 299–308 c� 2006 The Authors. Journal compilation c� 2006 The Zoological Society of London 305

Fox numbers, snow depth and ungulate carcassesV. Selas and J. O. Vik

Regional warming may have contributed to the strong

red fox increases during 1930–1950, as temperatures in

Scandinavia were above the long-term average in this

period. In Canada, Hersteinsson &Macdonald (1992) found

significant relationships between increased red fox numbers

and climate variables in the same period. A higher frequency

of snow-poor winters may have accelerated the increase in

both red fox and cervid numbers in Norway, resulting in the

observed correlation if both groups increased most in

counties where average snow depths decreased most. How-

ever, the relationship with the roe deer ranking index, which

reflects the geographical spread of roe deer rather than any

climate gradients, demonstrates that cervid numbers were

independently important for the growth in the red fox

populations.

The period of the strongest increase in red fox popula-

tions coincided with the period of the strongest increase and

expansion of roe deer populations in Norway (Østbye &

Bjørnson, 1990). Because the roe deer is vulnerable to

predation by wolf and lynx in snow-rich areas, the absence

of these predators was probably a necessary condition for

the northward spread of roe deer in the 20th century.

Especially the wolf should be able to limit the number of

roe deer in Norway, because this predator commonly also

kills larger cervid species, and will thus (in contrast to lynx

and red fox) be less affected by low roe deer densities.

Hence, if roe deer numbers is an important factor for winter

survival and spring conditions of red foxes in snow-rich

areas, the extermination of the wolf may have helped pave

the way for the subsequent strong increase in red fox

populations in northern Europe during the 20th century.

Acknowledgements

We thank Anders Angerbjorn, Reidar Borgstrøm, Nina E.

Eide, Olav Hjeljord, John Linnell, Anne Loison and Pal

Prestrud for valuable comments on drafts of the manuscript.

References

Andersen, R. (1991). Moose and modern forestry. Fauna 44,

30–40 (in Norwegian, with English abstract).

Angerbjorn, A., Arvidson, B., Noren, E. & Stromgren, L.

(1991). The effect of winter food on reproduction in the

arctic fox, Alopex lagopus: a field experiment. J. Anim.

Ecol. 60, 705–714.

Angerbjorn, A., Tannerfeldt, M., Bjarvall, A., Ericson, M.,

From, J. & Noren, E. (1995). Dynamics of the arctic fox

population in Sweden. Ann. Zool. Fenn. 32, 55–67.

Angerbjorn, A., Tannerfeldt, M. & Erlinge, S. (1999). Pre-

dator–prey relationships: arctic foxes and lemmings.

J. Anim. Ecol. 68, 34–49.

Boertje, R.D., Valkenburg, P. & McNay, M.E. (1996). In-

crease in moose, caribou, and wolves following wolf con-

trol in Alaska. J. Wildl. Mgmt. 60, 474–489.

Borg, K. (1970). On mortality and reproduction of roe

deer in Sweden during the period 1948–1969. Viltrevy 7,

121–149.

Boyd, D.K., Ream, R.R., Pletscher, D.H. & Fairshild, M.W.

(1994). Prey taken by colonizing wolves and hunters in the

Glacier National Park area. J. Wildl. Mgmt. 58, 289–295.

Cederlund, G. & Lindstrom, E. (1983). Effects of severe

winters and fox predation on roe deer mortality. Acta Ther.

28, 129–145.

Central Bureau of Statistics of Norway (1978). Hunting

statistics 1846–1977. Oslo: Central Bureau of Statistics of

Norway.

Christiansen, E. (1979). Skog og jordbruk, smagnagere og rev.

Tidsskr. Skogbruk 87, 115–119 (in Norwegian).

Christiansen, E. (1983). Fluctuations in some small rodent

populations in Norway 1971–1979.Holarct. Ecol. 6, 24–31.

Collett, R. (1912). Norges virveldyr. Bind 1, Norges pattedyr.

Aschehoug: Kristiania (in Norwegian).

Crooks, K.R. & Soule, M. (1999). Mesopredator release and

avifaunal extinctions in a fragmented system. Nature 400,

563–566.

Englund, J. (1970). Some aspects of reproduction and mor-

tality rates in Swedish foxes (Vulpes vulpes), 1961–63 and

1966–69. Viltrevy 8, 1–81.

Hagen, Y. (1952). Rovfuglene og viltpleien. Oslo: Gyldendal

(in Norwegian).

Halpin, M.A. & Bissonette, J.A. (1988). Influence of snow

depth on prey availability and habitat use by red fox. Can.

J. Zool. 66, 587–592.

Hanssen-Bauer, I. & Førland, E. (2000). Temperature and

precipitation variations in Norway 1900–1994 and their

links to atmospheric circulation. Int. J. Climatol. 20,

1693–1708.

Hansson, L. (1978). Small mammal abundance in relation to

environmental variables in three Swedish forest phases.

Stud. Forest. Suec. No. 147. 1–40.

Hansson, L. & Henttonen, H. (1985). Gradients in density

variations of small rodents: the importance of latitude and

snow cover. Oecologia 67, 394–402.

Henttonen, H. (1989). Does an increase in the rodent

and predator densities, resulting from modern

forestry, contribute to the long-term decline in Finnish

tetraonids? Suomen Riista 35, 83–90 (in Finnish with

English summary).

Hersteinsson, P. & Macdonald, D.W. (1992). Interspecific

competition and the geographical distribution of red and

arctic foxes Vulpes vulpes and Alopex lagopus. Oikos 64,

505–515.

Hewson, R. (1986). Distribution and density of fox breeding

dens and the effects of management. J. Appl. Ecol. 23,

531–538.

Hjeljord, O. (1980). Viltbiologi. Oslo: Landbruksforlaget

(in Norwegian).

Høst, P. (1935). Trekk fra dyrelivet pa Hardangervidda.

Norges Jeger- og Fiskerforbunds Tidsskrift 64, 201–211

(in Norwegian).

Journal of Zoology 269 (2006) 299–308 c� 2006 The Authors. Journal compilation c� 2006 The Zoological Society of London306

Fox numbers, snow depth and ungulate carcasses V. Selas and J. O. Vik

Hurrell, J.W. (1995). Decadal trends in the North Atlantic

Oscillation: regional temperatures and precipitation.

Science 269, 676–679.

Jacobsen, B.V. & Sonerud, G.A. (1993). Synchronous switch

in diet and hunting habitat as a response to disappearance

of snow cover in Tengmalm’s owl Aegolius funereus. Ornis

Fenn. 70, 78–88.

Jacobsen, H. & Andersen, R. (1990). Elgen. In Norges Dyr,

Pattedyrene, Vol. 2: 104–127. Semb-Johansson, A. & Fri-

slid, R. (Eds). Oslo: Cappelen (in Norwegian).

Jedrzejewska, B. & Jedrzejewski, W. (1998). Predation in

vertebrate communities. The Bialowieza primeval forest as

a case study. In Ecological studies, Vol. 135: 1–45. Berlin:

Springer.

Jedrzejewski, W. & Jedrzejewska, B. (1992). Foraging and diet

of the red fox Vulpes vulpes in relation to variable food

resources in Bialowieza National Park, Poland. Ecography

15, 212–220.

Johnsen, S. (1929). Rovdyr- og rovfuglstatistikken i Norge.

Bergens Mus. Arbok. Naturvidensk. Rekke 1929, 140 pp. (in

Norwegian).

Kaikusalo, A. & Angerbjorn, A. (1995). The arctic fox

population in Finnish Lapland during 30 years 1964–93.

Ann. Zool. Fenn. 32, 69–77.

Kjos-Hanssen, B. (1962). Rødreven som regulerende faktor i

smaviltbestanden. Jakt, fiske og friluftsliv 91, 501–503, 523

(in Norwegian).

Kolb, H.H. & Hewson, R. (1980). A study of fox populations

in Scotland from 1971–1976. J. Appl. Ecol. 17, 7–19.

Langvatn, R. (1990). Hjorten. In Norges Dyr, Pattedyrene, 2:

81–100. Semb-Johansson, A. & Frislid, R. (Eds). Oslo:

Cappelen (in Norwegian.).

Lindstrom, E. (1989). Food limitation and social regulation in

a red fox population. Holarct. Ecol. 12, 70–79.

Lindstrom, E. &Hornfeldt, B. (1994). Vole cycles, snow depth

and fox predation. Oikos 70, 156–160.

Lindstrom, E.R., Andren, H., Angelstam, P., Cederlund, G.,

Hornfeldt, B., Jaderberg, L., Lemnell, P.-A., Martinsson,

B., Skold, K. & Swenson, J.E. (1994). Disease reveals the

predator: sarcoptic mange, red fox predation, and prey

populations. Ecology 75, 1042–1049.

Lindstrom, E.R., Brainerd, S.M., Helldin, J.O. & Overskaug,

K. (1995). Pine marten–red fox interactions: a case of

intraguild predation? Ann. Zool. Fenn. 32, 123–130.

Lund, H.M.-K. (1962). The red fox in Norway II. The feeding

habits of the red fox in Norway. Papers of the Norwegian

State Game Research Institute, 2. Series, no. 12. Orkanger.

(in Norwegian, with English summary).

Lund, H.M.-K. (1963). Vilt og Viltstell no. 3. Reven.

Smaskrifter utgitt av Viltstyret og Statens Viltundersøkel-

ser (in Norwegian).

Marcstrom, V., Keith, L.B., Engren, E. & Cary, J.R.

(1989). Demographic responses of arctic hares (Lepus

timidus) to experimental reductions of red foxes (Vulpes

vulpes) and martens (Martes martes). Can. J. Zool. 67,

658–668.

Marcstrom, V., Kenward, R.E. & Engren, E. (1988). The

impact of predation on boreal tetraonids during vole

cycles: an experimental study. J. Anim. Ecol. 57, 859–872.

Meia, J.S. & Weber, J.M. (1995). Home ranges and move-

ments of red foxes in central Europe: stability despite

environmental changes. Can. J. Zool. 73, 1960–1966.

Murray, D.L. & Lariviere, S. (2002). The relationship be-

tween foot size of wild canids and regional snow condi-

tions: evidence for selection against a high footload?

J. Zool. (Lond.) 256, 289–299.

Myrberget, S. (1965). Changes in small rodent population levels

in Norway 1946–60. Papers of the Norwegian State Game

Research Institute, 2. Series, no. 19. Orkanger. (in

Norwegian, with English summary).

Myrberget, S. (1982). Population fluctuations in Norwegian

microtines 1932–1971. Fauna 35, 29–32 (in Norwegian,

with English abstract).

Myrberget, S. (1988). Hunting statistics as indicators of game

population size and composition. Stat. J. United Nations

ECE 5, 289–301.

Mysterud, A., Yoccoz, N.G., Stenseth, N.C. & Langvatn, R.

(2000). Relationships between sex ratio, climate and den-

sity in red deer: the importance of spatial scale. J. Anim.

Ecol. 69, 959–974.

Okarma, H. (1995). The trophic ecology of wolves and their

prey predatory role in ungulate communities of forest

ecosystems in Europe. Acta Ther. 40, 335–386.

Okarma, H., Jedrzejewska, B., Jedrzejewski, W., Krasinski,

Z.A. & Milkowski, L. (1995). The roles of predation, snow

cover, acorn crop, and man-related factors on ungulate

mortality in Bialowieza Primeval Forest, Poland. Acta

Ther. 40, 197–217.

Østbye, E. & Bjørnson, B. (1990). Radyret. In Norges Dyr,

Pattedyrene, 2: 128–147. Semb-Johansson, A. & Frislid, R.

(Eds). Oslo: Cappelen (in Norwegian).

Palomares, F. & Caro, T.M. (1999). Interspecific killing

among mammalian carnivores. Am. Nat. 153,

492–508.

Panek, M. & Bresinski, W. (2002). Red fox Vulpes vulpes

density and habitat use in a rural area of western Poland in

the end of 1990s, compared with the turn of 1970s. Acta

Ther. 47, 433–442.

Raiby, M. (1970). Winter mortality rate in roe-deer in relation

to weather conditions. Fauna 23, 284–290 (in Norwegian,

with English summary).

Selas, V. (1997). Cyclic population fluctuations of herbivores

as an effect of cyclic seed cropping of plants: the mast

depression hypothesis. Oikos 80, 257–268.

Selas, V. (1998a). Does food competition from red fox

influence the breeding density of goshawk? Evidence

from a natural experiment. J. Zool. (Lond.) 246,

325–335.

Selas, V. (1998b). Hønsehaukbestanden i tilbakegang – ogsa i

Aust-Agder. Var Fuglefauna 21, 149–154 (in Norwegian).

Selas, V. & Steel, C. (1998). Large brood sizes of pied

flycatcher, sparrowhawk and goshawk in peak microtine

Journal of Zoology 269 (2006) 299–308 c� 2006 The Authors. Journal compilation c� 2006 The Zoological Society of London 307

Fox numbers, snow depth and ungulate carcassesV. Selas and J. O. Vik

years: support for the mast depression hypothesis. Oecolo-

gia 116, 4499–4455.

Semb-Johansson, A. (1988). Faunal changes in Norway in

recent time. Fauna 41, 73–90, 109–132 (in Norwegian, with

English abstract).

Skjenneberg, S. & Slagsvold, L. (1968). Reindriften og dens

naturgrunnlag. Oslo: Universitetsforlaget (in Norwegian).

Skogland, T. (1990). Reinen. In Norges Dyr, Pattedyrene, 2:

148–170. Semb-Johansson, A. & Frislid, R. (Eds). Oslo:

Cappelen (in Norwegian).

Smedshaug, C.A., Selas, V., Lund, S.E. & Sonerud, G.A.

(1999). The effect of a natural reduction of red fox Vulpes

vulpes on small game hunting bags in Norway. Wildl. Biol.

5, 157–166.

Smedshaug, C.A. & Sonerud, G.A. (1997). Can predation on

small game be limited by manipulation of offal? Fauna 50,

146–154 (in Norwegian, with English abstract).

Solberg, E.J., Loison, A., Sæther, B.-E. & Strand, O. (2000).

Age-specific harvest mortality in a Norwegian moose Alces

alces population. Wildl. Biol. 6, 41–52.

Sonerud, G.A. (1986). Effect of snow cover on seasonal

changes in diet, habitat, and regional distribution of

raptors that prey on small mammals in boreal zones of

Fennoscandia. Holarct. Ecol. 9, 33–47.

Strand, O., Linnell, J.D.C., Krogstad, S. & Landa, A.

(1999). Dietary and reproductive responses of arctic

foxes to changes in small rodent abundance. Arctic 52,

272–278.

Tannerfeldt, M., Angerbjorn, A. & Arvidson, B. (1994). The

effect of summer feeding on juvenile arctic fox survival – a

field experiment. Ecography 17, 88–96.

Wildhagen, A. (1952). Fluctuations in small rodent populations

in Norway 1871–1949. Drammen: Statens Viltundersøkel-

ser (in Norwegian, with English summary).

Journal of Zoology 269 (2006) 299–308 c� 2006 The Authors. Journal compilation c� 2006 The Zoological Society of London308

Fox numbers, snow depth and ungulate carcasses V. Selas and J. O. Vik