Feast
to famine: sympatric predators respond differently to seasonal prey
scarcity on the low-Arctic tundra
Chloé Warret Rodrigues* and James D. Roth
Department of Biological Sciences, University of Manitoba, 50 Sifton
Road, Winnipeg, Manitoba R3T 2N2, Canada
*corresponding author:
warretrc@myumanitoba.ca
Abstract
Resource fluctuation is a major driver of animal movement, influencing
strategic choices such as residency vs nomadism, or social dynamics. The
Arctic tundra is characterized by strong seasonality: resources are
abundant during the short summers but scarce in winters. Therefore,
expansion of boreal-forest species onto the tundra raises questions on
how they cope with winter-resource scarcity. We examined a recent
incursion by red foxes (Vulpes vulpes ) onto the coastal tundra of
western Hudson Bay, an area historically occupied by Arctic foxes
(Vulpes lagopus ) that lacks access to anthropogenic foods, and
compared seasonal shifts in space use of the two species. We used 4
years of telemetry data following 8 red foxes and 11 Arctic foxes to
test the hypothesis that the movement strategies of both species are
primarily driven by temporal variability of resources. We also predicted
that the harsh tundra conditions in winter affect red foxes more than
Arctic foxes, which are adapted to this environment. Dispersal was the
most frequent winter movement strategy in both fox species, despite its
association with high mortality (winter mortality was 9.4 times higher
in dispersers than residents). Red foxes consistently dispersed towards
the boreal forest, whereas Arctic foxes primarily used sea ice to
disperse. Home range size of red and Arctic foxes did not differ in
summer, but resident red foxes substantially increased their home range
size in winter, whereas home range size of resident Arctic foxes did not
change seasonally. As climate changes, abiotic constraints on some
species may relax, but associated declines in prey communities may lead
to local extirpation of many predators, notably by favoring dispersal
during resource scarcity.
Key-words: climate change, movement ecology, seasonality,
resource fluctuation, range expansion, telemetry
Introduction
Species’ range expansions rank among the preeminent ecological
consequences of Arctic warming and anthropogenic pressure (McCarty
2001). For example, species that primarily inhabit the boreal forest
have settled onto the tundra due to milder winters, longer productive
periods, and increased availability of anthropogenic subsidies
(Hersteinsson and Macdonald 1992; Tape et al. 2016; Gallant et al.
2020). However, at the edge of its distribution, a species also reaches
the limits of its environmental tolerances (biotic and abiotic). Scarce
patches of preferred habitat, lower resource availability, and harsh
winters may challenge the survival of peripheral individuals and force
them to adjust their behavior, including ranging behavior (e.g.,
Niedzielski and Bowman 2016; Linnell et al. 2021).
Movement strategies are driven by ecological, social, and
morpho-physiological factors acting in synergy, such as resource
availability, body size, seasonality, or the distribution of prey or
competitors (Macdonald and Johnson 2015). Although most individuals
restrict their ranging behavior to familiar areas to meet their needs
efficiently, some can emigrate or become nomadic if the cost of staying
exceeds the benefits (e.g., Avgar et al. 2014). Individuals usually
favor residency when they find abundant and predictable resources and
can avoid competitors or predators (Jonzén et al. 2011; Marneweck et al.
2019). Residents’ successive maintenance movements (sensu Roshier
and Reid 2003), as measured over short time periods, typically occur
over relatively short distances and do not produce a net displacement
along a movement vector over a longer time period. The succession of
these maintenance movements thus perpetuates a home range (or a
territory if actively defended) (e.g., Powell 2000). In contrast,
individuals may engage in long-range movements when they cannot predict
resource availability, nor avoid adverse weather conditions or
competitors (or predators) (Jonzén et al. 2011; Hsiung et al. 2018).
Long-range movements occur on a continuum. Unlike migrations, nomadic
movements lack directionality and regular timing: the animal leaves its
former range permanently, and may wander over long time periods (Roshier
and Reid 2003). Although carnivores typically exhibit residency, they
may engage in long-range movements to reproduce or settle in more
suitable habitat, resulting in dispersal (Roshier and Reid 2003).
Resources influence not only movement strategy and ranging behavior (and
hence home range sizes), but also the degree to which competitors
tolerate each other (Maher and Lott 2000; Mcloughlin et al. 2000; Eide
et al. 2004). The resource dispersion hypothesis predicts that home
range size increases with increased resource dispersion, while
territoriality decreases with increased food abundance: when resources
are highly unpredictable, an individual (or breeding pair) will likely
maintain a home range large enough to meet its needs during times of
scarcity (MacDonald 1983). Furthermore, Maher and Lott (2000)
hypothesized that as resource predictability decreases, so does the net
benefit of territoriality, except in food-caching species, which still
benefit from being territorial. This territorial benefit was empirically
corroborated in fieldfares (Turdus pilaris ), which defend stored
food in anticipation of food scarcity, and in Arctic foxes (Vulpes
lagopus ), which defend food caches and exhibit the lowest home range
overlap in areas where prey are unpredictable (Maher and Lott 2000; Eide
et al. 2004).
Arctic ecosystems are characterized by marked seasonality and
interannual resource fluctuation (Korpimäki and Hongell 1986; Jonzén et
al. 2011). Low availability of resources in winter contrasts with a
summer resource burst; geese, seabirds, and shorebirds reproduce every
summer in the Arctic, offering an abundant and predictable food source
to predators, if only for a limited period (Tannerfeldt et al. 1998;
Eide et al. 2004; McDonald et al. 2017). Many Arctic predators primarily
rely on arvicoline rodents (lemmings and voles) that are present
year-round but whose fluctuating populations peak every 3-4 years (Krebs
et al. 2002; Fauteux et al. 2015). Together, rodent-abundance
fluctuations and the relatively short lifespan of mammalian predators
make rodents an unpredictable resource (Tannerfeldt et al. 1998; Krebs
et al. 2002; Bilodeau et al. 2013).
Predators may thus migrate or disperse, either to track their preferred
prey (Korpimäki and Hongell 1986; Jonzén et al. 2011) or because peaks
of rodent abundance have favored a higher consumer density, which
reduces per capita energy intake (Mysterud et al. 2011) when
rodent abundance decreases again (Avgar et al. 2014; Robillard et al.
2016). In that context, long-range movement may be an adaptive strategy
to reduce competition between consumers or alleviate the negative
effects of food scarcity on survival and reproduction. However, such
movements are often associated with high rates of mortality because
individuals lack familiarity with or adaptation to the landscapes
crossed (Korpimäki and Hongell 1986; Roth 2003; Powell and Mitchell
2012). Therefore, terrestrial predators typically favor residency over
nomadism (Powell 2012; Lai et al. 2017), and develop strategies to cope
with prey scarcity while retaining their home ranges. Examples of such
strategies include demographic lability (Barraquand and Benhamou 2008),
food caching (Sklepkovych and Montevecchi 1996), larger home range
maintenance to cope with prey scarcity (Eide et al. 2004), or increased
frequency of short extraterritorial trips (excursions) to exploit
alternative resources (Messier 1985; Lai et al. 2017).
The harsh Arctic conditions historically limited the northern
distribution of red foxes (Vulpes vulpes ) (Hersteinsson and
Macdonald 1992; Bartoń and Zalewski 2007; Gallant et al. 2020), but
during the 20th century, red foxes considerably extended their range
into the Arctic due to increased availability of anthropogenic subsidies
that buffered winter-food scarcity in many Arctic areas (Gallant et al.
2020). Both fox species are ecologically similar: they use dens to
reproduce and raise their young, beginning shortly before migratory
birds arrive, and although they depend strongly on arvicoline rodents,
they forage opportunistically and cache food (Roth 2002; Careau et al.
2007a; McDonald et al. 2017). However, red foxes are larger than Arctic
foxes, which increases their food requirements (Hersteinsson and
Macdonald 1992), and are less adapted than Arctic foxes to prey scarcity
during the harsh Arctic winters (Fuglesteg et al. 2006; Careau et al.
2007b).
We examined movement strategies and space use of red and Arctic foxes on
the low Arctic tundra in northern Manitoba, where red foxes recently
expanded from the adjacent boreal forest and now reproduce in sympatry
with Arctic foxes (Moizan 2019, Zhao et al. submitted). We hypothesized
that seasonal variability of resources primarily drives movement
strategies in both red and Arctic foxes, but winter conditions are more
limiting to red foxes. Specifically, red foxes lack adaptations to
exploit the sea ice, and their increased energetic requirements during
winter constrain their ranging behavior. We thus predicted that
long-range movements are primarily initiated during winter (P1), red
foxes are more likely to disperse in search of better conditions instead
of commuting to the sea ice and back like Arctic foxes (P2), red foxes
always maintain larger home ranges than Arctic foxes (P3), and
extra-territorial excursions are more frequent for resident red foxes
than Arctic foxes, and more frequent in winter in both species (P4).
Methods
Study area and species. – Our study area near Churchill,
Manitoba (Fig. 1; 58°N, 94°W), is part of the Hudson Bay Lowlands, a
uniformly flat (<200m elevation) wetland bordering the
south-western shore of Hudson Bay (Brook and Kenkel 2002). This wet
tundra ecosystem lies between the boreal forest to the south and west,
and the marine ecosystem to the north and east. The three biomes thus
transition in our study area. In fall, this part of Hudson Bay freezes
as early as the first week of November, and the ice along the northern
and western coasts of the Bay is typically consolidated by December 2,
providing a platform for fox movements and opportunities to forage on
marine resources. Sea ice in the area breaks up around mid-June, and the
area is typically free of ice by the first week of July (Hochheim et al.
2010), thus limiting access to marine resources on the sea ice until the
ocean freezes again. We consider that the sea ice starts at the low
tideline (Ponomarenko et al. 2014).
Lemmings are available year-round, but their abundance has dramatically
damped throughout the Arctic (e.g., Bilodeau et al. 2013), particularly
low Arctic populations sympatric with voles (Ehrich et al. 2020).
Abundant populations of Canada geese (Branta canadensis ) and
lesser snow geese (Anser caerulescens ) nest each year in the
study area, providing an important food source to predators (McDonald et
al. 2017). Canada goose nests are distributed throughout the entire area
along with some snow goose nests, and two major snow goose colonies
(>20,000 nesting pairs) occur near the coast (Fig. 1)
(Andersen et al. 2010; McDonald et al. 2017). Peak arrival of snow geese
occurs during the first week of May (Cargill and Jefferies 1984) and
>95% of Canada goose nests are initiated before the last
week of May, with a median hatch date during the 3rdweek of June (Andersen et al. 2010). Geese remain abundant throughout
fall and may be present until late October—the latest recovery for the
2017-2019 period was on October 16 (Celis-Murillo et al. 2020).
Capture and satellite telemetry. – Between 2017 and 2019 we
captured 10 red foxes and 13 Arctic foxes using Tomahawk (Model 208,
Tomahawk Live Trap Co., WI) and padded leghold traps (Softcatch # 1.5,
Oneida Victor Ltd, USA). Traps were placed on active dens or by
protruding features (e.g., driftwood or spruce islets) and remained open
continuously for up to one week. We checked the traps every 4-6 hours
and closed them during extreme weather conditions (e.g., blizzard or
temperatures below -25°C). We captured adult foxes from March to May
when snow still covers the ground and facilitates travel over large
distances, except two adult foxes caught near our field camps in June
2018. Foxes were first wrapped in a blanket and released from the traps,
then we assessed sex and body condition, deployed an Iridium satellite
collar (#4170 or 4270, Telonics, Mesa, Arizona, USA;
~100g, i.e., 2-4% of a fox body mass), and released
them at the site of capture. All handling procedures were approved by
the University of Manitoba Animal Care Committee (Protocol F17-012), and
the research was conducted under Parks Canada Research and Collection
Permits WAP-2017-25781 and WAP-2018-27938, and Manitoba Wildlife
Scientific Permits WB20226 and WB21856.
Movement analysis. – Our GPS collars used different schedules
throughout the year (see Table S1), so we thinned all the tracks by
randomly selecting 1 location per day (the lowest fix frequency) to
obtain independent successive locations. We defined two relevant
contrasting periods based on goose phenology. The season of abundant
resources (hereafter summer) thus extended from May 15, the approximate
date of nest initiation, to the end of October, the last month during
which geese can be considered alternative prey for the foxes of this
area (Andersen et al. 2010; McDonald et al. 2017). The resource-scarcity
period (hereafter winter) extended from November 1 to May 14, when geese
are absent and foxes mostly rely on arvicoline rodents.
We plotted all fox tracks in ArcGIS 10.3 (ESRI 2017, Redland, CA, USA)
to remove possible major erroneous locations and identify movement
strategies: residency and long-range movements. We labelled a fox as a
resident only if it maintained a home range from the start of a given
season until the end of that season or until its death (i.e., we did not
include the season of capture in movement strategy and home range
comparisons). All foxes that underwent long-range movements (hereafter
dispersals) were considered dispersers, since none of the foxes returned
to its departure area, but these dispersal events were not natal
dispersal because we only captured adults.
For each dispersal we calculated the cumulative distance travelled
(i.e., sum of straight-line distances between successive daily
relocations), the duration (starting with the last position within the
home range boundaries), the cumulative to straight-line distance ratio
(a proxy for fox behavior during dispersal), the cardinal direction (the
angle of the vector between first and last locations, degrees from due
North), the main substrate used for movement (sea ice or land), and the
average daily speed. We considered that the dispersal started with the
last location in a home range prior to dispersal initiation, or at the
point of capture if a fox did not exhibit residency prior to dispersal
(and thus was likely captured while already dispersing), and ended with
the first location associated with a settlement of >7 days
in a new delimited ranging area (on land, not ice) or with the death of
the fox. Although foxes can exhibit staged dispersal, exploring
delimited areas for a temporary period from a few days up to a few weeks
(e.g., Walton et al. 2018), we never observed clear staging behavior.
We estimated residents’ home ranges and core areas, defined as the 95%
and 50% utilization distribution isopleths, respectively, with local
convex hulls (LoCoH) using the package T-LoCoH v.1.40.07 in R (Lyons et
al. 2013). LoCoH are nonparametric estimates of utilization
distributions and perform better than parametric kernel methods to
identify boundaries (such as coastlines) and unused areas (Getz et al.
2007; Stark et al. 2017). Due to heterogeneous location densities, we
used the adaptive method (a-LoCoH). However, we still excluded locations
(or clusters of consecutive locations) > 20 km from the
mean center of all locations, because including them distorted some home
ranges.
To estimate seasonal home-range shifts in each fox, we measured summer
and winter home range overlaps using the package T-LoCoH.dev v.
1.34.00/r12 and the distance between their centroids estimated in ArcGIS
10.3 (ESRI, 2017). Using a subset of 16 individuals with 111 to 187
locations each, we determined that home range areas reached an asymptote
with 38 locations on average. All our resident foxes exceeded this
threshold with at least 61 locations.
Many residents undertook short-distance and short-duration trips outside
the boundaries of their home range, either on land or on the sea ice. We
defined excursions as any exploratory movement <7 days away
from the current home range followed by a return to the home range.
Because we estimated home ranges as a 95% utilization distribution, we
differentiated excursions from movements near the home range border,
based on the distribution of the distances between a location and the
centroid of the estimated home range. Locations that appeared to be
outliers using a one-sided Hampel filter (upper bound = median
(Tukey-transformed distance) + 3 median absolute deviations) were
considered excursions. If a trip outside the boundaries of the LoCoH
home range estimate consisted of multiple consecutive locations, we used
the farthest away of the consecutive locations to determine if that trip
was an excursion. Finally, we called “commuting trip” any excursion on
the sea ice (Lai et al. 2017).
Statistical analyses. – We performed all statistical analyses in
R software (R Core Team, 2020). To compare the proportion of dispersal
events (P1, P2) and home-range size (P3) between species and between
seasons, we ran generalized linear mixed-effect models (GLMM) using the
lme4 package v.1.1-25 (Bates et al. 2015). We included species, season
and their interaction term, and controlled for fox ID as a random
effect. Two of the collared red foxes were a mated pair and like fox
pairs elsewhere in the Arctic (Rioux et al. 2017, Lai et al. 2022),
their home range sizes were similar (paired permutation t-tests, home
range: t = 9.78, P = 0.25; core area: t = 11.00,P = 0.25, n = 3). We reviewed 3 potential outlier foxes with
leverage higher than 0.5 (Cooks’ distance) individually to decide
whether they should be removed. Two red foxes settled in forest habitat
after dispersing and therefore were excluded. We found no valid
ecological or methodological reason to remove the outlying Arctic fox,
and thus retained that estimate in the data set.
We assessed if dispersal track
parameters differed between species using two-sided permutation tests
based on the t statistics (nperm = 9999) in library
RVAideMemoire v. 0.9-79 (Hervé 2021). We assessed the impact of
dispersing on winter survival and annual survival using a right-censored
Cox mixed effect model from the coxme library (Therneau 2020),
controlling for fox ID as a random effect, and with time-to-event as the
number of days since the start of a given winter (1 November). We used
Fisher’s exact test to test if commuting trips were more frequent in
Arctic foxes (P2). We then tested if land excursions by resident foxes
were more likely in winter and in red foxes (P4) using GLMMs to control
for fox ID as a random effect: we transformed the raw number of
excursions into a frequency of excursions per week, due to substantial
inter-individual variation in tracking period length. All summary
statistics are presented as mean ± SE and/or mean [range] unless
stated otherwise. Given our low sample size and individual heterogeneity
in spatial behavior, we used an alpha threshold at 0.1 to lower the risk
of evidence minimization (e.g., Knaub 1987; Altman and Bland 1995).
Results
We tracked 13 Arctic foxes and 10 red foxes between May 2017 and August
2020 (see Table S2 for capture details), which yielded a total of 6159
locations after thinning their tracks to one daily location, but 10
Arctic and 7 red foxes yielded enough data to perform home-range
analyses and assess the seasonal shift in space use. Since we followed 7
individuals for more than one year, we obtained 8 Arctic and 9 red fox
home ranges over 3 winters, and 13 Arctic and 12 red fox home ranges
over 4 summers.
Dispersal events. – We recorded 14 dispersal events
overall: 9 by Arctic foxes (8 individuals, since one fox dispersed
twice) and 5 by red foxes (see Tables S2 and S4). One Arctic fox and one
red fox were captured while dispersing (i.e., they were not using a home
range at the time of capture) and 11 of the other 12 dispersals were
initiated during winter (specifically between November 14 and May 10),
while one was initiated on September 30. Foxes settled in a new area (at
least temporarily) after 10 of the dispersal events, but 7 died 11 days
to 4 months after dispersing (at least one was caught by a fur trapper).
Of the four foxes that died while dispersing, at least two were caught
by fur trappers, but we have no information on the cause of death for
the other two.
All red foxes dispersed towards forested areas, and all but one in a
southwestern direction, whereas Arctic foxes moved towards other tundra
habitats, 8 to the northeast and northwest, and 1 to the southeast (but
still in the Hudson Bay Lowlands) (Fig. 2). Of the 9 Arctic foxes that
dispersed, 3 used sea ice exclusively until they died or reached a new
delimited ranging area, 3 navigated between sea ice and land, and 3
exclusively used land. No red foxes dispersed using the sea ice. The
mean length, duration, speed and cumulative-distance to straight-line
ratio of dispersal tracks were all smaller in red foxes, indicating they
dispersed a shorter distance (perm. test, nArctic = 9,
nred = 5, t = 1.44, P = 0.002), over less time (t
= 1.55, P = 0.036), with a slower speed (t = 1.78, P =
0.043), and more directly (t = 1.08, P = 0.020) than Arctic foxes
(Table 1).
Of the 16 fox observations over 3 winters, 56% dispersed (5/9 red foxes
and 5/7 Arctic foxes), but red foxes did not disperse more often than
Arctic foxes (GLMM: Z = -1.06, P = 0.29, n = 16). Dispersals were
associated with higher mortality than residency: mortality risk was 9.4
times higher for dispersing foxes in the short-term (i.e., during the
same winter: z = -1.99, P = 0.046; ndisperse = 14,
nresident = 7) and 6.5 times higher in the long-term
(i.e., within a year of dispersing: z = -1.95, P = 0.051).
However, mortality risk did not differ by species in that winter (z =
1.29, P = 0.20; nred = 10,
nArctic = 11) or the following year (z = 0.42, P= 0.67).
Seasonal home range. – Resident fox space-use patterns
differed between species (Table 2). While summer home ranges and core
areas of red foxes and Arctic foxes were similar, red foxes drastically
increased the size of their home range in winter (Fig. 3; GLMM:
tseason = 0.72, P = 0.48, nsummer= 24, nwinter = 12; tspecies = 0.14,P = 0.89, nred = 19, nArctic =
17; tspecies*season = 3.06, P = 0.006,
ntotal = 36). Winter home range and core areas of red
foxes were 1.9 and 2.7 times larger than their summer home ranges and
core areas, respectively. Table S3 provides all parameters from all
GLMMs.
Individuals’ summer and winter home ranges overlapped moderately in both
species, although the seasonal change was small for some (red foxes:
55.8±11.9% [33.2-70.7%], n = 7; Arctic foxes: 62.3±12.3%
[45.9-75.4%], n = 4). The distance between winter and summer home
range centroids was also relatively short (red foxes: 0.9±0.6 km
[0.4-2.0 km], n = 7; Arctic foxes: 0.8±0.4km [0.3-1.1km], n =
4). Core areas, however, generally overlapped only slightly to
moderately between seasons (red foxes: 21.4±20.2% [0-55.7%], n =
7; Arctic foxes: 29.9±29.3% [1.5-70.7%], n = 4), and so the
seasonal shift of core area centroids was often sizeable (red foxes:
3.5±2.2 km [0.6-7.4 km], n = 7; Arctic foxes: 1.6±1.1 km [0.4-3.3
km], n = 4).
Excursions and commuting trips. — In winter, all resident
Arctic foxes used the sea ice, commuting at least once and up to 7
times, although their commuting trips never lasted more than three days.
However, no red foxes commuted to the sea ice (Fisher’s exact test:P = 0.001, nArctic = 5, nred =
7). We found no overall difference in land excursion frequency between
seasons or species (GLMM: tspecies = -0.859, P =
0.397; tseason = -0.539, P = 0.593;
tseason*species = 1.650, P = 0.109, n = 36).
Weekly frequency of land excursion in red foxes increased from 0.05
[0-0.25] in summer to 0.13 [0-0.32] in winter, while Arctic fox
land excursion frequency was 0.08 [0-0.21] in summer and 0.06
[0-0.13] in winter. Pooling together excursions and commuting trips,
we found that these extraterritorial exploratory trips were more
frequent in winter (GLMM: tseason = 3.113, P =
0.004, n = 36) but occurred at a similar frequency in both species
(tspecies = -1.547, P = 0.131).
Discussion
Both red and Arctic foxes showed mixed movement strategies in our study
area, some remaining resident and others engaging in long-range
movements, which denotes flexibility in both species’ spatial behavior.
However, although resident red foxes used space similarly to resident
Arctic foxes during summer, their winter strategy differed markedly and
likely reflected their lack of adaptation to prey scarcity and the harsh
conditions of the tundra during winter.
As predicted (P1), foxes did not disperse in summer while prey was
abundant. The high dispersal rate in winter contrasted with the usually
low proportion of dispersing adults found in both red and Arctic fox
populations elsewhere (e.g., Storm et al. 1976; Lai et al. 2017; Walton
et al. 2018), and other carnivores in general (e.g., Ferreras et al.
2004), suggesting that overwinter survival near treeline was
particularly difficult for both species. The higher dispersal rate in
our study area could be due to low rodent densities compared to
elsewhere, notably the Canadian high Arctic (Ehrich et al. 2020; Lai et
al. 2022), and scarce access to anthropogenic subsidies unlike other
areas of sympatry (Killengreen et al. 2011; Rød-Eriksen et al. 2020),
which could further indicate that Churchill foxes were less likely than
other populations (such as Bylot Arctic foxes living near the large snow
goose colony) to capitalize on summer-abundant resources, caching items
to survive winters as residents (Rioux et al. 2017).
Dispersal can incur high fitness costs, with higher mortality or missed
opportunities to reproduce following dispersal (e.g., Ferreras et al.
2004; Soulsbury et al. 2008; Lai et al. 2017). As expected, the survival
cost of dispersal was high in our population, with 11 of 13 dispersers
suffering mortality within 4 months of starting dispersal. Mortality
during dispersal may occur because dispersers must cross unfamiliar
areas (e.g., Storm et al. 1976; Ferreras et al. 2004) and in leaving our
remote study area may come into greater contact with humans (e.g.,
Ferreras et al. 2004). The cost of dispersal on reproduction was also
likely high, as only three of our 13 dispersed foxes survived long
enough through the subsequent breeding season to have successfully
raised pups, whereas all but one residents (11 of 12) survived long
enough to raise pups successfully. However, remaining resident during
prey scarcity may compromise reproduction too, as resources may be
allocated to overwinter survival at the cost of next-season reproduction
(Löfgren et al. 1986). Although each strategy may have a cost, our
results suggest that dispersing is risky for both red and Arctic foxes,
and may be a desperate strategy to cope with local prey scarcity.
Arctic foxes are well-known for their long-range movements, specifically
using the sea ice (Lai et al. 2017; Fuglei and Tarroux 2019). When
rodent abundance is low, they respond numerically to marine resources,
suggesting that exploiting the sea ice in winter is a well-established
strategy for responding to prey scarcity (Roth 2003). Two-thirds of our
Arctic foxes indeed dispersed using the sea ice as a platform, whereas
red foxes never did, likely denoting their lack of adaptation to exploit
marine resources. The dispersal distances of red foxes, despite being
shorter than those of Arctic foxes, were particularly large for this
species; only two studies have reported similar dispersal distances, in
Sweden and the Canadian high Arctic (Walton et al. 2018; Lai et al.
2022), but unlike in Sweden, they dispersed towards the boreal forest.
The low cumulative to straight-line dispersal distance ratio of these
red foxes suggests straight relocation until finding suitable habitat,
unlike Arctic foxes, which seemed more prone to exploration during
dispersal, suggesting they primarily use the sea ice for foraging (as
suggested by diet studies; Roth 2003), and not just as a dispersal
platform.
Red foxes’ difficulty overwintering on the tundra is further reflected
in the seasonal change in home-range size of residents. While home-range
or core-area sizes did not differ between species during summer, when
food is plentiful and the climate mild, red foxes substantially
increased their ranging behavior in winter, whereas Arctic foxes did
not. The Obstinate Strategy hypothesis states that animals may not
adjust their ranging behavior to the fluctuation of resources because
fighting competitors to expand a home range is costly (von Schantz
1984). Our red fox population instead behaved as flexible strategists,
unlike many other carnivore populations (Meia and Weber 1995; Eide et
al. 2004; López-Bao et al. 2019). Winter home ranges of these red foxes
averaged ~35 km2 (up to 56
km2), among the largest reported for this species
(Goszczyński 2002; Walton et al. 2017; Lai et al. 2022). Large home
ranges suggest a low fox density in our area (Trewhella et al. 1988),
which may decrease the cost of expanding the home range in winter,
compared to maintaining such a large home range during summer.
Anecdotally, one red fox captured on the tundra relocated to the boreal
forest long enough during winter to calculate two core areas and home
ranges (tundra and forest): her
forest home range was 25% the size of her tundra home range (only 14%
for core areas), suggesting that forest habitat was much higher quality
than the tundra.
We found low seasonal overlap of individual core areas and large
distances between core-area centroids, indicating relatively low site
fidelity, and thus quite high spatial flexibility in both species. The
flexible and the obstinate strategies are two ends of a continuum that
depend on the amplitude of resource fluctuation and the life span
relative to the periodicity of resource fluctuation. In the Canadian
High Arctic, Arctic foxes behaved as flexible strategists, unlike in the
European Arctic (e.g., Eide et al. 2004), adjusting the size of their
home range yearly to lemming density (Tarroux 2011). Hyenas have also
shown mixed strategies at the species level, some clans behaving as
obstinate and other clans as flexible strategists in response to
resource fluctuation (Maude et al. 2019). That behavioral plasticity in
carnivores may allow them to adapt to future changes in prey abundance
and distribution linked to climate change (Nater et al. 2021).
In partial agreement with P3, all Arctic foxes commuted to the sea ice
(one Arctic fox even had 76.7% of her winter home range on the sea ice,
yet still took five exploratory trips farther onto the sea ice; Fig.
S1), whereas our red foxes did not. Red foxes are opportunistic feeders
(e.g., Kidawa and Kowalczyk 2011) and may occasionally feed on beached
marine carrion (Andriashek et al. 1985; Killengreen et al. 2011).
Although sea ice may offer alternative resources when terrestrial prey
is scarce, our red fox population did not exploit this habitat, likely
due to their lack of adaptation to that environment. Yet red foxes did
not engage more often in dispersal or excursions than Arctic foxes, nor
did their excursion rate increase in winter. Expanding their home range
during winter may have been sufficient to obtain enough prey. This
winter expansion may originate from both a decrease in prey abundance
and an increase of red foxes’ energetic requirements. Arctic foxes adapt
to the harsh winter climate with a low resting metabolic rate (likely to
conserve energy) and exceptional insulation (Prestrud 1991; Fuglei and
Øritsland 1999; Fuglesteg et al. 2006). They also show metabolic
depression (i.e., a significant decrease in the resting metabolic rate)
in response to starvation, indicating an adaptation to food scarcity
(Fuglei and Øritsland 1999). Red foxes in the Arctic compensate for
their poorer insulation with a higher basal metabolic rate, which
benefits them by expanding their thermoneutral zone (Careau et al.
2007b), but at the same time increases their energetic requirements
(Fuglesteg et al. 2006).
Our study generally supports the idea that movement strategies in both
red and Arctic foxes are mostly driven by seasonal fluctuations of
resources, and that both species are highly flexible. The high
proportion of adult red and Arctic foxes that disperse in winter may
indicate that winter food is even scarcer in our area than elsewhere
(e.g., Lai et al. 2017; Walton et al. 2018), or sea ice may be more
productive for Arctic foxes than elsewhere. Although current conditions
of food scarcity during winter may limit red fox density (Gallant et al.
2012, 2020), resident red foxes were able to overwinter without relying
on anthropogenic subsidies and they did not engage in risky dispersal
more often than their congeners. The hindrance to overwinter survival
imposed by their lack of adaptation to food scarcity and the harsh
conditions of the tundra seem therefore limited at treeline, where they
may be able to use sparse forest patches to buffer the low food
availability on the tundra.
The changes occurring on the tundra associated with Arctic warming will
likely lower the constraints on boreal-forest species’ persistence in
this environment (Callaghan et al. 2004). For example, increased winter
temperatures will lower the costs associated with thermoregulation
(Pálsson et al. 2016; Nater et al. 2021), and changing tundra-biotic
communities will provide expanding species with increased foraging
opportunities (Post et al. 2009; Tape et al. 2016). Meanwhile, Arctic
foxes seemed to rely quite heavily on the sea ice instead of expanding
their home ranges, but this habitat will be negatively affected as the
Arctic warms, and tundra species that rely on their ability to exploit
those alternative resources may thus lose opportunities to cope with
terrestrial food scarcity.
The species interaction-abiotic stress hypothesis proposes that abiotic
stress mostly limits a species’ distribution in areas where climate
imposes stressful conditions (e.g., cold edge of a species’ range),
while interactions with heterospecific competitors likely limits species
distributions in milder areas (e.g., Louthan et al. 2015). However, in
areas particularly vulnerable to the effects of climate change, edge
populations may also become directly limited by climate-induced declines
in resource availability. Declines in some crucial prey may trigger
important dispersal in highly mobile predators, or prevent newcomers
from becoming established, which could lead to local extirpation of
predator species.