Journal of Animal
Ecology 2007
76, 873–880
Prolonging the arctic pulse: long-term exploitation of
cached eggs by arctic foxes when lemmings are scarce
Blackwell Publishing Ltd
GUSTAF SAMELIUS*, RAY T. ALISAUSKAS*†, KEITH A. HOBSON*‡ and
SERGE LARIVIÈRE*§
*Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK, S7N 5E2, Canada;
†Environment Canada, Prairie and Northern Wildlife Research Centre, 115 Perimeter Road, Saskatoon, SK, S7N
0X4, Canada; ‡Environment Canada, 11 Innovation Boulevard, Saskatoon, SK, S7N 3H5, Canada; and §Delta
Waterfowl Foundation, R.R.#1, Box 1, Portage La Prairie, MB, R1N 3A1, Canada
Summary
1. Many ecosystems are characterized by pulses of dramatically higher than normal
levels of foods (pulsed resources) to which animals often respond by caching foods for
future use. However, the extent to which animals use cached foods and how this varies
in relation to fluctuations in other foods is poorly understood in most animals.
2. Arctic foxes Alopex lagopus (L.) cache thousands of eggs annually at large goose
colonies where eggs are often superabundant during the nesting period by geese. We
estimated the contribution of cached eggs to arctic fox diets in spring and autumn, when
geese were not present in the study area, by comparing stable isotope ratios (δ13C and
δ15N) of fox tissues with those of their foods using a multisource mixing model in
Program IsoSource.
3. The contribution of cached eggs to arctic fox diets was inversely related to collared
lemming Dicrostonyx groenlandicus (Traill) abundance; the contribution of cached eggs
to overall fox diets increased from < 28% in years when collared lemmings were
abundant to 30–74% in years when collared lemmings were scarce.
4. Further, arctic foxes used cached eggs well into the following spring (almost 1 year
after eggs were acquired) – a pattern that differs from that of carnivores generally
storing foods for only a few days before consumption.
5. This study showed that long-term use of eggs that were cached when geese were
superabundant at the colony in summer varied with fluctuations in collared lemming
abundance (a key component in arctic fox diets throughout most of their range) and
suggests that cached eggs functioned as a buffer when collared lemmings were scarce.
Key-words: food caching, food hoarding, foraging behaviour, foraging ecology, prey
switching, pulsed resources.
Journal of Animal Ecology (2007) 76, 873–880
doi: 10.1111/j.1365-2656.2007.01278.x
Introduction
Many ecosystems are characterized by pulses of
dramatically higher than normal levels of foods (pulsed
resources) that often have large impacts on the trophic
ecology of these systems (Ostfeld & Keesing 2000). For
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society
Correspondence and present address: G. Samelius, Grimsö
Research Station, 730 91 Riddarhyttan, Sweden. E-mail:
[email protected]
Present address: Serge Larivière, Cree Hunters and Trappers
Income Security Board, Edifice Champlain, Bureau 1100,
2700 Blvd Laurier, Sainte-Foy, QC, G1V 4K5, Canada
example, exceptionally large seed crops (mast seeding),
eruptions in plant production following heavy rains
and large influxes of migratory prey provide animals
with pulses of superabundant foods (Willson & Halupka
1995; Ostfeld & Keesing 2000; Holmgren et al. 2001).
The periodic nature of pulsed resources often results in
these foods being more important among animals that
store foods and generalist consumers that switch among
foods (Vander Wall 1990; Ostfeld & Keesing 2000).
Food storage (termed food hoarding or food caching)
is a common response to pulses in food abundance and
may be an adaptive behaviour to avoid food shortages
in stochastic environments; use of stored foods allows
874
G. Samelius et al.
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
873–880
animals to remain in familiar areas and is an alternative
strategy to migration, torpor, hibernation and fat
storage (Smith & Reichman 1984; Vander Wall 1990;
Careau 2006). Food hoarding may also be adaptive to
supplement diets of growing young or to reduce time
spent foraging when other behaviours are more
important (Smith & Reichman 1984; Vander Wall
1990). However, the extent to which animals use stored
foods is unknown for most species (Vander Wall 1990).
This is especially true for members of the order
Carnivora among which many species cache foods but
for whom the actual use of cached foods is unknown
(Vander Wall 1990).
Arctic foxes Alopex lagopus (L.) are generalist
predators and scavengers that rely heavily on lemmings
and voles (small mammals hereafter) throughout most
of their range (Audet, Robbins & Larivière 2002).
However, other foods such as birds and their eggs can
be important in arctic fox diets in some years and
regions of the Arctic (Hersteinsson & MacDonald
1996; Bantle & Alisauskas 1998). Additionally, arctic
foxes commonly cache foods when they are abundant
(Stickney 1991; Samelius & Alisauskas 2000). Caching
of foods appears to be especially common among arctic
foxes at large bird colonies where foxes cache > 1000
eggs per fox each nesting season (Stickney 1991; Samelius
& Alisauskas 2000). Small mammals often fluctuate
over 3–5-year periods, whereas large influxes of migratory
birds and their eggs provide arctic foxes with pulses of
predictable and seasonally superabundant foods. Large
bird colonies therefore provide ideal setting to study
long-term exploitation of pulsed resources and how
this varies in relation to fluctuations in other foods.
The objectives of this study were to examine (1) when
and to what extent arctic foxes at a large goose colony
used cached eggs, and (2) how use of cached eggs varied
with small mammal abundance. Specifically, we examined
arctic fox diets in spring (May) and autumn (September–
November) by comparing stable isotope values (δ13C
and δ15N) of fox tissues with those of their foods. Geese
were not present in the study area in spring or autumn
so stable isotope values of eggs in fox tissues therefore
represented eggs that were cached when geese were
superabundant at the colony in summer. Stable isotope
analyses have been used widely in ecological studies
and are based on the fact that stable isotope values in
animal tissues reflect those of their foods (Hobson
1999; Kelly 2000). We predicted that (1) the proportion
of cached eggs in arctic fox diets would be greater in
autumn than in spring, and (2) arctic foxes would
include cached eggs more frequently in their diets when
small mammals were scarce.
Methods
 
This study was done at the large goose colony at
Karrak Lake (67°14′ N, 100°15′ W) in the Queen Maud
Gulf Bird Sanctuary, Nunavut, Canada, from May to
July in 2000–04. The goose colony at Karrak Lake
consisted of between 700 000 and 1 000 000 nesting
Ross’s Chen rossi (Cassin) and lesser snow geese Chen
caerulescens (L.) in these years (Alisauskas, unpublished data). Geese arrive at Karrak Lake in late May
and depart the colony shortly after hatch in early July
when they disperse throughout the sanctuary (Ryder &
Alisauskas 1995). Average nesting density ranged 22–
34 nests per ha during this study (Alisauskas, unpublished data). Geese migrate south in late August and do
not return to the Arctic until mid to late May the
following year. The colony at Karrak Lake is located
c.60 km south of the Arctic Ocean and the area consists
of gently rolling tundra that is dominated by rock
outcrops, sedge meadows, and marshy areas interrupted
by shallow tundra ponds (Ryder 1972). Spring and
summer diets of arctic foxes at Karrak Lake are
dominated by small mammals, birds and eggs (Bantle
& Alisauskas 1998).
Foods available to arctic foxes in spring and autumn
included collared lemmings Dicrostonyx groenlandicus
(Traill), red-backed voles Clethrionomys rutilus (Pallas),
arctic hares Lepus arcticus (Ross), caribou Rangifer
tarandus (L.), muskoxen Ovibos moschatus (Zimmermann),
ptarmigans Lagopus spp., and cached eggs. Goslings
and geese were not available to foxes in spring and
autumn because they (1) are rarely cached by arctic
foxes during the nesting season of geese (Samelius &
Alisauskas 2000), and (2) departed the colony shortly
after hatch and were rarely seen in or near the colony
thereafter. Further, goslings and geese start to decompose within a few days in summer (Samelius, personal
observation) and therefore would have decomposed
well before temperatures dropped below freezing in
autumn. We therefore did not include goslings and
geese in our analyses on spring and autumn diets. Eggs,
in contrast, store well because the shell, several protective
membranes, and physio-chemical properties of albumen
proteins prevent microbial activity (Freeman & Vince
1974). Arctic hares were rare during this study and are
rarely consumed by arctic foxes at Karrak Lake (Bantle
& Alisauskas 1998) so we did not include arctic hares in
our analyses. Most caribou in the Karrak Lake area are
migratory and are present only in spring and summer,
although some caribou remain in the area throughout
the year (Gunn, Fournier & Nishi 2000). We did not
encounter any brown lemmings Lemmus sibiricus (Kerr)
during this study and therefore did not include them in
our analyses.
   
We collected blood from the cephalic vein and clipped
winter fur from the main trunk of the body of adult
foxes (≥ 1 year old) captured in May and early June (see
Samelius, Larivière & Alisauskas 2003 for capture
procedures). Traps were baited with sardines for 5–10
days prior to capture to improve capture success (see
875
Food pulses and
arctic foxes
inclusion of sardines in diet analyses below). Foxes were
marked with plastic ear tags to distinguish local foxes
from potential immigrants (see below). The metabolic
turnover rate of blood is about 1 month, whereas fur is
metabolically inactive (Hobson 1999); stable isotope values
of blood therefore represented spring diets, whereas
those from winter fur represented diets from the previous autumn when the fur was grown (Roth 2002). Hair
samples were air dried and then stored frozen, whereas
blood samples were stored in 70% ethanol.
Arctic foxes can make considerable long-distance
movements (Audet et al. 2002), although they tend to stay
in an area once they have settled (Tannerfeldt & Angerbjörn 1996; Anthony 1997; Landa, Strand, Linnell &
Skogland 1998). Similarly, arctic foxes marked at Karrak
Lake appeared to use similar areas throughout the year
(Samelius, unpublished data). So, to avoid inclusion of
foxes that may have immigrated from areas where they
may have eaten foods with different isotopic values, we
included only (1) foxes that were ear-tagged in previous
years in analyses of autumn diets, and (2) breeding
foxes and foxes that were ear-tagged in previous years
in analyses of spring diets (foxes started to breed 1–
2 months prior to capture and therefore must have
been resident in our study area for at least that period).
   
We collected goose eggs and muscle samples from
small mammals, caribou, muskoxen and ptarmigans
opportunistically in spring and summer. We had no
muscle samples from autumn, but as diets of small
mammals, caribou, muskoxen and ptarmigans are
similar in spring and autumn (Rodgers & Lewis 1986;
Holder & Montgomerie 1993; Gunn & Adamczewski
2003; Miller 2003), we assumed that isotope values in
muscle of these herbivores were similar within species
in spring and autumn (see Barnett 1994 and Drucker,
Bocherens, Pike-Tay & Mariotti 2001 for similarity of
isotope values of caribou muscle in spring and autumn
and Roth 2002 for similar assumption about small
mammals). We collected fur from three ringed seals
Phoca hispida (Schreber) from the Queen Maud Gulf
to examine whether foxes used marine foods. We also
prepared 10 sardine samples to examine whether consumption of sardines during pre-bating of traps (see
above) influenced stable isotope values of foxes. Egg
and muscle samples from the first 2 years of the study
were stored frozen, whereas they were stored in 70%
ethanol thereafter.
  
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
873–880
We monitored small mammal abundance at three
permanent trap lines established in 1994 following
Shank (1993). Trap lines consisted of 25 trap sites with
one snap-trap placed within 1 m of each trap site. One
trap line was monitored during the second half of June
and the other two were monitored during the second
half of July We monitored small mammal abundance
for 10 consecutive nights and used number of captures
per 100 trap-nights as an index of small mammal
abundance for each year. We subtracted 0·5 trap-nights
for each trap that was snapped without capture to correct
for variation in sampling effort (Beauvais & Buskirk
1999). Trap lines included habitats ranging from wet
lowland areas to dry upland hills.
  
We freeze-dried muscle, blood and egg (homogenized
eggs without the shell) samples to remove water and
used a 2 : 1 chloroform–methanol solution to remove
lipids from muscle and egg samples. Similarly, we removed
surface oil from fur samples by using this solution.
Muscle, blood and egg samples were powdered with a
mortar, whereas fur samples were clipped into fine
pieces of fur. Samples of about 1 mg were weighed
into tin cups and combusted in an Europa 20 : 20 continuous flow ratio mass spectrometer (CFIRMS) at the
Department of Soil Sciences at University of Saskatchewan. We used two laboratory standards (egg albumen
and whale baleen) for every five tissue samples analysed.
Stable isotope ratios were expressed in δ-notation as
parts per thousand (‰) deviations from Pee Dee Belemnite
(δ13C) and atmospheric AIR (δ15N) standards according
to δX = [(Rsample – Rstandard)/Rstandard] × 1000, where X is
13
C or 15N and R is 13C/12C or 15N/14N. Laboratory
measurement error was ±0·1‰ for δ13C and ±0·3‰ for
δ15N.
    

We used Program IsoSource (Phillips & Gregg 2003) to
estimate spring and autumn diets of arctic foxes. This
program uses mass balance mixing models to provide
ranges of possible source contributions when the number
of sources is too large to permit unique solutions from
general mass balance mixing models (Phillips & Gregg
2003). We used source increments of 1% and mass
balance tolerance of ±0·1‰. We performed analyses
on spring and autumn diets separately for each year
(n = 1–9 foxes per year for analyses on spring diets and
4 –7 foxes per year for analyses on autumn diets). Prey
items of arctic foxes were isotopically distinct and did
not vary among years except for values of caribou
muscle that differed among years and overlapped with
muscle values of red-backed voles in 2003 and muskoxen
in 2000, 2002 and 2004 (, F10,270 = 143·45, P < 0·001,
Tukey’s pair-wise test to identify difference among
groups, Fig. 1, Table 1). We suspect that annual variation in isotopic values of caribou muscle was related to
caribou wintering in different areas (see Gunn et al.
2000 for this herd wintering in areas > 300 km apart)
but suggest that caribou values were similar among years
in autumn before caribou moved south. We therefore
used year-specific caribou values in analyses of spring
2·6‰ from δ13C ratios of blood and fur, respectively.
Fox tissues were, thus, normalized to their equivalent
dietary values. Similarly, we corrected fur samples
from seals for isotopic discrimination (i.e. difference in
isotope values between fur and muscle) by using values
calculated for three different species of seals – one of
which was ringed seals (Hobson, Schell, Renouf &
Noseworthy 1996); we subtracted 0·6‰ from δ15N
ratios of fur and 1·5‰ from δ13C ratios of fur. We provide
1st to 99th percentiles of possible source contributions
unless otherwise stated (Phillips & Gregg 2003).
876
G. Samelius et al.
Results
Fig. 1. Stable isotope values of food items included in
analyses of arctic fox diets at Karrak Lake in 2000–04.
diets, whereas we pooled means of caribou values from
all years in analyses of autumn diets. Further, we pooled
means for (1) caribou and red-backed voles in analyses
of spring diets in 2003, and (2) caribou and muskoxen
in analyses of spring diets in 2000, 2002 and 2004. We
did not include seals or sardines in final analyses
because their contributions to fox diets were heavily
skewed towards 0% in preliminary analyses (see
Phillips & Gregg 2003).
We corrected fox samples for isotopic discrimination
(i.e. change in isotope signature from diet to consumer)
by using values calculated for captive red foxes (Roth &
Hobson 2000); we subtracted 2·6‰ and 3·3‰ from
δ15N ratios of blood and fur, respectively, and 0·6‰ and
Small mammal abundance varied considerably among
2
years ( χ( 4 ) = 24·15, P < 0·001, Fig. 2). This variation
was largely caused by collared lemming abundance that
showed great fluctuation among years (Fisher exact test
P = 0·0016); collared lemming abundance peaked in
2000 and was followed by declining and low abundance
during the rest of the study. Red-backed vole abundance,
2
in contrast, was similar among years ( χ( 4 ) = 3·75, P = 0·44).
Further, red-backed vole abundance was greater than
collared lemming abundance from 2000 to 2004 combined
2
( χ(1) = 16·75, P < 0·001).
Arctic fox diets were heavily skewed towards collared
lemmings and cached eggs (Table 2, Fig. 3). Arctic fox
diets also included large proportions of ptarmigans
in the spring of 2000 and 2001. The contribution of
cached eggs to arctic fox diets was inversely related to
collared lemming abundance (Fig. 4). Specifically, the
Table 1. Isotope values of foods included in analyses of arctic fox diets at Karrak Lake in 2000–04 (mean ± SD). Also provided
in the table are isotope values of foods that were not included in analyses of arctic fox diets. The average proportion of C and N
was similar among foods and ranged 47–50% and 13–16%, respectively
Food
Foods included in analyses:
Goose eggs
Collared lemming muscle
Red-backed vole muscle
Caribou muscle 2000*†
Caribou muscle 2001*
Caribou muscle 2002*†
Caribou muscle 2003*†
Caribou muscle 2004*†
Muskox muscle
Ptarmigan muscle
Foods not included in analyses:
Goose muscle (arriving geese)
Gosling muscle (at hatch)
Gosling muscle (at fledging)‡
Ringed seals (muscle)§
Sardines
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
873–880
δ13C, ‰
δ15N, ‰
sample
size
−24·6 ± 0·5
−26·6 ± 0·5
−21·7 ± 0·6
−21·4 ± 0·2
−21·7 ± 0·2
−21·4 ± 0·1
−21·4 ± 0·2
−21·4 ± 0·4
−21·5 ± 1·0
−23·9 ± 0·5
7·0 ± 0·6
4·3 ± 0·8
6·3 ± 0·5
4·3 ± 0·3
3·0 ± 0·7
4·4 ± 1·1
6·4 ± 0·5
4·1 ± 1·3
5·2 ± 0·5
2·2 ± 0·5
97
8
7
6
7
9
2
5
2
5
−23·2 ± 1·3
−24·7 ± 0·7
−26·1 ± 0·5
−20·4 ± 1·9
−18·7 ± 0·5
6·7 ± 0·7
6·8 ± 0·5
3·9 ± 0·4
18·1 ± 1·3
11·5 ± 0·6
57
11
19
3
10
*We used year specific values of caribou muscle in analyses of spring diets whereas we pooled means of caribou muscle from all
years in analyses of autumn diets.
†Caribou values overlapped with red-backed vole values in 2003 and with muskox values in 2000, 2002 and 2004 – we therefore
pooled means for these tissues in analyses of spring diets in those years.
‡Goslings were collected c. 50 km north of the colony as goslings were rarely available in or near the colony after hatch.
§Isotopic values of seal muscle were calculated from fur samples where we used isotopic discrimination between fur and muscle
calculated by Hobson et al. (1996).
877
Food pulses and
arctic foxes
Discussion
Fig. 2. Small mammal abundance at Karrak Lake in 1999–
2004. Brown lemmings were not captured or otherwise
encountered at Karrak Lake during this study.
contribution of cached eggs to overall spring diets increased
from 0–28% in years when collared lemmings were
abundant to 30 –74% in years when collared lemmings
were scarce. Similarly, the contribution of cached eggs
to overall autumn diets increased from 1–19% in years
when collared lemmings were abundant to 44–65% in
years when collared lemmings were scarce. The contribution of collared lemmings to arctic fox diets, in
contrast, was positively related to collared lemming
abundance (Fig. 4). Body mass of arctic foxes in spring
was unrelated to the contribution of cached eggs to
their diets ( on 25-percentiles of possible source
contribution by cached eggs when controlling for sex
and breeding status of foxes, F2,17 = 1·39, P = 0·30). We
did not detect differences in isotope values between
male and female foxes (, F2,15 = 0·59, P = 0·57) or
between breeding and nonbreeding foxes (,
F2,15 = 0·76, P = 0·48) within years.
Food caching is a common response to pulses in
dramatically higher than normal levels of foods
(Vander Wall 1990; Careau 2006). However, the extent
to which animals use cached foods and how this varies
in relation to fluctuations in other foods is poorly
understood in most animals. This study showed that
arctic foxes relied heavily on eggs that were cached
when geese were superabundant at the colony in
summer and that the use of cached eggs varied with
fluctuations in collared lemming abundance. In fact,
the contribution of cached eggs to arctic fox diets was
inversely related to collared lemming abundance, whereas
the contribution of collared lemmings followed that of
their abundance. Further, arctic foxes cached similar
numbers of eggs among years (Samelius 2006) so there
was no indication that foxes used cached eggs in
proportion to the abundance of cached eggs. Arctic
foxes, thus, switched from collared lemmings to cached
eggs in years when collared lemmings were scarce, which,
in turn, suggests that cached eggs functioned as a buffer
when collared lemmings were scarce. Foxes may prefer
collared lemmings over cached eggs because lemmings
may be nutritionally more valuable to foxes or because
large consumption of albumen can result in biotin
deficiency (Klevay 1976). We did not, however, detect
any signs of biotin deficiency (e.g. hair loss or impaired
muscle co-ordination) even when cached eggs contributed
50–60% of their diets, which suggests that arctic foxes
were able to consume large amounts of albumen without
suffering from biotin deficiency. Moreover, spring
body mass of arctic foxes was unrelated to the contribution of cached eggs to their diets, which further
suggests that large consumption of albumen did not impede
body condition of foxes. Arctic foxes at Karrak Lake
Table 2. Ranges of possible source contributions to spring and autumn diets of arctic foxes at Karrak Lake in 2000–04 (1st to 99th
percentiles). Ranges of source contributions were calculated by using Program IsoSource (Phillips & Gregg 2003)
Food
Collared
lemmings, %
Red-backed
voles, %
Caribou
%
Musk
oxen %
Ptarmigans
%
No. of
foxes
Collared lemming
abundance
Spring*
2000
0–28
2001
0–8
2002
30–66
2003
47–74
2004
8–56
24–58
24 – 41
0–27
0–21
9–53
0–21
0–6
0–41
0–30*
0–37
–*
0 –16
–*
–*
–*
0–28*
0–8
0–29*
0–24
0–26*
12–47
43–67
0–20
0–15
0–32
1
9
4
5
4
High
Decreasing
Low
Low
Low–medium
Autumn†‡
2000
1–19
2001
44–59
2002
56–65
2003
51–62
69–85
33 – 46
32– 40
34 – 43
0–12
0–9
0– 4
0–6
0–9
0–6
0–3
0–4
0–10
0–7
0–3
0–5
0–11
0–8
0–4
0–5
7
5
4
4
High
Decreasing
Low
Low
Year
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
873–880
Cached
eggs, %
*We used year specific values of caribou muscle in analyses of spring diets – these overlapped with red-backed vole values in 2003
and with muskox values in 2000, 2002 and 2004 so we pooled red-backed voles and caribou in 2003, and muskoxen and caribou
in 2000, 2002 and 2004.
†We pooled means of caribou muscle from all years in analyses of autumn diets.
‡We have no data on autumn diets in 2004 as winter fur of foxes captured in spring 2004 represented autumn diets in 2003.
878
G. Samelius et al.
Fig. 3. Isotopic values of arctic fox tissues at Karrak Lake in
spring and autumn in 2000 –04 where location in the source
polygon is indicative of diet. Fox values were corrected for
isotopic discrimination by using values calculated for red foxes
(Roth & Hobson 2000). The source polygon differed somewhat
among years in the spring (indicated by dashed lines) because
spring values of caribou muscle differed isotopically among years.
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
873–880
switching to cached eggs when collared lemmings were
scarce was similar to arctic foxes in coastal areas switching
to marine foods in years when lemmings were scarce
(Roth 2002, 2003). However, switching to cached foods
allowed foxes to remain in familiar areas with predictable
food supplies and may be adaptive compared with
dispersing to search for other foods (Samelius &
Alisauskas 2000).
Arctic foxes switching to cached eggs in years when
collared lemmings were scarce may explain why animals
often store more foods than needed. Specifically, arctic
foxes may cache eggs independently of small mammal
abundance to compensate for unpredictable changes in
future lemming abundance. In fact, arctic foxes cached
similar numbers of eggs among years (Samelius 2006),
although they rarely fed on these eggs in years when
collared lemmings were abundant. This pattern follows
that of carnivores often appearing to cache as much
food as possible when foods are abundant (Vander
Wall 1990), which, in turn, may be an adaptive strategy
in stochastic environments where foods are easy to
obtain and acquired at low risk of injury (Samelius &
Alisauskas 2006). Animals may also store more foods
than needed to compensate for losses to competitors
and failure to locate caches (Vander Wall 1990).
Fig. 4. Contribution of cached eggs and collared lemmings to
arctic fox diets at Karrak Lake in relation to collared lemming
abundance. Brackets indicate 1st to 99th percentiles of source
contributions for each year. Autumn diets are indicated by
solid brackets and spring diets by dashed brackets. Dashed
lines connect midpoints of possible source contributions at
high and low lemming densities and should be used as guides
for general trends rather than exact relationships.
Arctic foxes used cached eggs well into the following
spring (almost 1 year after foods were acquired), which
differs greatly from that of carnivores generally storing
foods for only a few days (Vander Wall 1990). Carnivores in northern climates may, however, store
foods for several months (e.g. Stickney 1991; Bantle
& Alisauskas 1998) because decomposition rates are
much lower than in more temperate or tropical
environments (Vander Wall 1990). The duration of
storage may also vary among food types depending
on how well they preserve. For example, eggs preserve
better than other foods because the shell, several
protective membranes, and physiochemical properties
of albumen proteins prevent microbial activity (Freeman
& Vince 1974). In fact, eggs preserve for > 1 year if
properly cached (Stickney 1991; Bantle & Alisauskas
1998). Our estimates of cached eggs contributing up to
about 60% of arctic fox diets may therefore be on the
extreme end of how much carnivores rely on cached
foods as there may be few other situations where
879
Food pulses and
arctic foxes
carnivores have access to foods that are equally suited
for long-term storage. Nevertheless, this study showed
that carnivores can rely heavily on cached foods in
some situations.
Arctic foxes rarely fed on red-backed voles, although
they were more abundant than collared lemmings on
which foxes frequently fed. This may largely have been
the result of differences in habitat use between these
species and how this affected exposure to arctic fox
predation. Specifically, collared lemmings use hummocky
lowland areas (Banfield 1974) where they are easy for
foxes to capture through the snow (Samelius, personal
observation). Red-backed voles, in contrast, use rocky
upland areas (Banfield 1974) where they may be more
difficult for foxes to capture through the snow. Differences
in consumption rate of collared lemmings and red-backed
voles may also have resulted from a preference by foxes
for collared lemmings over red-backed voles, although
this seems unlikely given the opportunistic nature of
arctic foxes (Audet et al. 2002).
In summary, many ecosystems are characterized by
pulses of food abundance to which animals often respond
by caching foods for future use (Vander Wall 1990;
Ostfeld & Keesing 2000). This study showed that
long-term use of eggs that were cached when geese were
superabundant at the colony in summer varied with
fluctuations in collared lemming abundance – a key
component in arctic fox diets throughout most of their
range (Audet et al. 2002). This study also illustrates the
linkage between arctic environments and wintering
areas by geese thousands of kilometres to the south
(Ryder & Alisauskas 1995). In fact, few ecosystems
occur in isolation and transfer of resources between
ecosystems appears to be the norm rather than the
exception (Polis & Strong 1996).
Acknowledgements
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
873–880
We thank J. Aitaok, J. Bantle, C. Bergman, R. de Carle,
C. Hendrickson, W. Kurz, A. Lusignan, K. Phipps, J.
Pitt, D. Stern and N. Wiebe for assistance in the field,
D. Kellett and F. Moore for logistical support, M.
Stocki for stable isotope analyses, V. Careau for insightful
discussions on his work on pulsed resources and food
caching by arctic foxes on Bylot Island, D. Berteaux,
M. Humphries, K. McCann, J. Pitt, and an anonymous
reviewer for comments that helped improve this manuscript, and J. Aitaok, B. Eyegetok, and D. Stern for
help and hospitality in Cambridge Bay. This study was
supported by California Department of Fish and
Game, Canadian Wildlife Service, Delta Waterfowl
Foundation, Ducks Unlimited Inc., Jennifer Robinson
Memorial Scholarship, Polar Continental Shelf
Project, Sweden-America Foundation, and University
of Saskatchewan. This research adhered to institutional guidelines; capture and handling procedures
were approved by the University of Saskatchewan
Animal Care Committee (UCACS protocol number
19990029).
References
Anthony, R.M. (1997) Home range and movements of arctic
fox (Alopex lagopus) in Western Alaska. Arctic, 50, 147–157.
Audet, A.M., Robbins, C.B. & Larivière, S. (2002) Alopex
lagopus. Mammalian Species, 713, 1–10.
Banfield, A.W.F. (1974) The Mammals of Canada. National
Museum of Natural Sciences, National Museums of
Canada, Ottawa.
Bantle, J.L. & Alisauskas, R.T. (1998) Spatial and temporal
patterns in arctic fox diets at a large goose colony. Arctic,
51, 231–236.
Barnett, B.A. (1994) Carbon and nitrogen isotope ratios of
caribou tissues, vascular plants, and lichens. MSc Thesis.
University of Alaska, Fairbanks, USA.
Beauvais, G.P. & Buskirk, S.W. (1999) Modifying estimates of
sampling effort to account for sprung traps. Wildlife Society
Bulletin, 27, 39 – 43.
Careau, V. (2006) Arctic Fox Hoarding Behaviour in a Snow
Goose Colony at Bylot Island, Nunavut (In English with
French introduction and summary). MSc Thesis. Université
du Québec à Montéal, Canada.
Drucker, D., Bocherens, H., Pike-Tay, A. & Mariotti, A.
(2001) Isotopic tracking of seasonal dietary change in
dentine collagen: preliminary data from modern caribou.
Earth and Planetary Sciences, 333, 303 –309.
Freeman, B.M. & Vince, M.A. (1974) Development of the
Avian Embryo. Chapman & Hall, London.
Gunn, A. & Adamczewski, J. (2003) Muskox – Ovibos moschatus.
Wild Mammals of North America: Biology, Management, and
Conservation (eds G.A. Feldhamer, B.C. Thompson & J.A.
Chapman), pp. 1076 –1094. The John Hopkins University
Press, Baltimore, MD.
Gunn, A., Fournier, B. & Nishi, J. (2000) Abundance and
Distribution of the Queen Maud Gulf Caribou Herd, 1986 –1998.
File Report No. 126. Department of Resources, Wildlife
and Economic Development, Government of the Northwest
Territories, Yellowknife, NWT.
Hersteinsson, P. & MacDonald, D.W. (1996) Diet of arctic fox
(Alopex lagopus) in Iceland. Journal of Zoology, 240, 457–
474.
Hobson, K.A. (1999) Tracing origins and migration of
wildlife using stable isotopes: a review. Oecologia, 120,
3 1 4 –326.
Hobson, K.A., Schell, D.M., Renouf, D. & Noseworthy, E.
(1996) Stable carbon and nitrogen isotopic fractionation
between diet and tissues of captive seals: implications for
dietary reconstructions. Canadian Journal of Fish and
Aquatic Sciences, 53, 528 –533.
Holder, K. & Montgomerie, R. (1993) Rock ptarmigan
(Lagopus mutus). The Birds of North America, No. 51. The
American Ornithologists’ Union, Philadelphia, PA.
Holmgren, M., Scheffer, M., Ezcurra, E., Gutierrez, J.R. &
Mohren, G.M.J. (2001) El Nino effects on the dynamics of
terrestrial ecosystems. Trends in Ecology and Evolution, 16,
89–94.
Kelly, J.F. (2000) Stable isotopes of carbon and nitrogen in the
study of avian and mammalian trophic ecology. Canadian
Journal of Zoology, 78, 1–27.
Klevay, L.M. (1976) The biotin requirements of rats fed 20%
egg white. Journal of Nutrition, 106, 1643 –1646.
Landa, A., Strand, O., Linnell, J.D.C. & Skogland, T. (1998)
Home-range sizes and altitude selection for arctic foxes and
wolverines in alpine environment. Canadian Journal of
Zoology, 76, 448 – 457.
Miller, F.L. (2003) Caribou – Rangifer tarandus. Wild Mammals
of North America: Biology, Management, and Conservation
(eds G.A. Feldhamer, B.C. Thompson & J.A. Chapman),
pp. 965 –997. The Johns Hopkins University Press,
Baltimore, MD.
880
G. Samelius et al.
© 2007 The Authors.
Journal compilation
© 2007 British
Ecological Society,
Journal of Animal
Ecology, 76,
873–880
Ostfeld, R.S. & Keesing, F. (2000) Pulsed resources and
community dynamics of consumers in terrestrial ecosystems.
Trends in Ecology and Evolution, 15, 232–237.
Phillips, D.L. & Gregg, J.W. (2003) Source partitioning using
stable isotopes: coping with to many sources. Oecologia,
136, 261–269.
Polis, G.A. & Strong, D.R. (1996) Food web complexity
and community dynamics. American Naturalist, 147,
813–846.
Rodgers, A.R. & Lewis, M.C. (1986) Diet selection in arctic
lemmings (Lemmus sibiricus and Dicrostonyx groenlandicus):
demography, home range, and habitat use. Canadian
Journal of Zoology, 64, 2717–2727.
Roth, J.D. (2002) Temporal variability in arctic fox diets as
reflected in stable-carbon isotopes; the importance of sea
ice. Oecologia, 133, 70 –77.
Roth, J.D. (2003) Variability in marine resources affects arctic
fox population dynamics. Journal of Animal Ecology, 72,
668 –676.
Roth, J.D. & Hobson, K.A. (2000) Stable carbon and nitrogen
isotopic fractionation between diet and tissue of captive red
fox: implications for dietary reconstruction. Canadian
Journal of Zoology, 78, 848 – 852.
Ryder, J.P. (1972) Biology of nesting Ross’s geese. Ardea, 60,
185–215.
Ryder, J.P. & Alisauskas, R.T. (1995) Ross’s Goose (Chen
rossii). The Birds of North America, No. 162 (eds A. Poole &
F. Gill). The Academy of Natural Sciences, Philadelphia,
and the American Ornithologists’ Union, Washington,
DC.
Samelius, G. (2006) Foraging behaviours and population dynamics
of arctic foxes. PhD Thesis. University of Saskatchewan,
Saskatoon, Canada.
Samelius, G. & Alisauskas, R.T. (2000) Foraging patterns of
arctic foxes at a large arctic goose colony. Arctic, 53, 279–
288.
Samelius, G. & Alisauskas, R.T. (2006) Sex-biased costs in
nest defence by lesser snow geese (Chen caerulescens):
consequences of parental roles? Behavioral Ecology and
Sociobiology, 59, 805 –810.
Samelius, G., Larivière, S. & Alisauskas, R.T. (2003)
Immobilization of arctic foxes with tiletamine hydrochloride
and zolazepam hydrochloride (Zoletil®). Wildlife Society
Bulletin, 31, 192–196.
Shank, C.C. (1993) The Northwest Territories Small Mammal
Survey: 1990–1992. Manuscript Report No. 72. Department
of Renewable Resources, Government of Northwest
Territories, Yellowknife, NWT.
Smith, C.C. & Reichman, O.J. (1984) The evolution of food
caching by birds and mammals. Annual Review of Ecology
and Systematics, 15, 329 –351.
Stickney, A. (1991) Seasonal patterns of prey availability and
foraging behaviour of arctic foxes (Alopex lagopus) in a
waterfowl nesting area. Canadian Journal of Zoology, 69,
2853 –2859.
Tannerfeldt, M. & Angerbjörn, A. (1996) Life history
strategies in fluctuating environment: establishment and
reproductive success in the arctic fox. Ecography, 19, 209–220.
Vander Wall, S.B. (1990) Food Hoarding in Animals. University
of Chicago Press, Chicago, IL.
Willson, M.F. & Halupka, K.C. (1995) Anadromous fish as
keystone specis in vertebrate communities. Conservation
Biology, 9, 489– 497.
Received 6 January 2007; accepted 25 May 2007
Handling Editor: Murray Humphries