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Food-caching animals can gain nutritional advantages by buffering seasonality in food availability, especially during times of scarcity. The wolverine (Gulo gulo) is a facultative predator that occupies environments of low productivity. As an adaptation to fluctuating food availability, wolverines cache perishable food in snow, boulders, and bogs for short- and long-term storage. We studied caching behavior of 38 GPS-collared wolverines in four study areas in Scandinavia. By investigating clusters of GPS locations, we identified a total of 303 food caches from 17 male and 21 female wolverines. Wolverines cached food all year around, from both scavenging and predation events, and spaced their caches widely within their home range. Wolverines cached food items on average 1.1 km from the food source and made between 1 and 6 caches per source. Wolverines cached closer to the source when scavenging carcasses killed by other large carnivores; this might be a strategy to optimize food gain when under pressure of interspecific competition. When caching, wolverines selected for steep and rugged terrain in unproductive habitat types or in forest, indicating a preference for less-exposed sites that can provide cold storage and/or protection against pilferage. The observed year-round investment in caching by wolverines underlines the importance of food predictability for survival and reproductive success in this species. Increasing temperatures as a consequence of climate change may provide new challenges for wolverines by negatively affecting the preservation of cached food and by increasing competition from pilferers that benefit from a warmer climate. It is however still not fully understood which consequences this may have for the demography and behavior of the wolverine. Significance statement Food caching is a behavioral strategy used by a wide range of animals to store food for future use. Choosing appropriate caching sites appears important for slowing down decomposition rates and minimizes competition. In this study, we demonstrate that the wolverine, an opportunistic predator and scavenger, utilizes available carrion to create caches all year around. By following wolverines with GPS collars, we registered that they carried food far away to cache it in secluded and cold places, which are often located on steep slopes or in forest. However, when scavenging other carnivores’ prey, they move food in shorter distances, possibly to be able to quickly return for more. The observed efficiency in wolverine caching behavior is likely vital for their survival and reproductive success in the harsh and highly seasonal environment in which they live.
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ORIGINAL ARTICLE
Refrigeration or anti-theft? Food-caching behavior of wolverines
(Gulo gulo) in Scandinavia
Bert van der Veen
1,2
&Jenny Mattisson
3
&Barbara Zimmermann
1
&John Odden
4
&Jens Persson
5
Received: 21 October 2019 / Revised: 23 February 2020 / Accepted: 3 March 2020 / Published online: 15 April 2020
#
Abstract
Food-caching animals can gain nutritional advantages by buffering seasonality in food availability, especially during times of scarcity.
The wolverine (Gulo gulo) is a facultative predator that occupies environments of low productivity. As an adaptation to fluctuating food
availability, wolverines cache perishable food in snow, boulders, and bogs for short- and long-term storage. We studied caching
behavior of 38 GPS-collared wolverines in four study areas in Scandinavia. By investigating clusters of GPS locations, we identified
a total of 303 food caches from 17 male and 21 female wolverines. Wolverines cached food all year around, from both scavenging and
predation events, and spaced their caches widely within their home range. Wolverines cached food items on average 1.1 km from the
food source and made between 1 and 6 caches per source. Wolverines cached closer to the source when scavenging carcasses killed by
other large carnivores; this might be a strategy to optimize food gain when under pressure of interspecific competition. When caching,
wolverines selected for steep and rugged terrain in unproductive habitat types or in forest, indicating a preference for less-exposed sites
that can provide cold storage and/or protection against pilferage. The observed year-round investment in caching by wolverines
underlines the importance of food predictability for survival and reproductive success in this species. Increasing temperatures as a
consequence of climate change may provide new challenges for wolverines by negatively affecting the preservation of cached food and
by increasing competition from pilferers that benefit from a warmer climate. It is however still not fully understood which consequences
this may have for the demography and behavior of the wolverine.
Significance statement
Food caching is a behavioral strategy used by a wide range of animals to store food for future use.Choosing appropriate caching
sites appears important for slowing down decomposition rates and minimizes competition. In this study, we demonstrate that the
wolverine, an opportunistic predator and scavenger, utilizes available carrion to create caches all year around. By following
wolverines with GPS collars, we registered that they carried food far away to cache it in secluded and cold places, which are often
located on steep slopes or in forest. However, when scavenging other carnivoresprey, they move food in shorter distances,
possibly to be able to quickly return for more. The observed efficiency in wolverine caching behavior is likely vital for their
survival and reproductive success in the harsh and highly seasonal environment in which they live.
Bert van der Veen and Jenny Mattisson contributed equally to this work.
Communicated by C. Soulsbury
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s00265-020-2823-4) contains supplementary
material, which is available to authorized users.
*Jenny Mattisson
jenny.mattisson@nina.no
1
Faculty of Applied Ecology, Agricultural Sciences and
Biotechnology, Inland Norway University of Applied Sciences
(INN), NO-2480 Koppang, Norway
2
Norwegian Institute of Bioeconomy Research (NIBIO),
NO-7031 Trondheim, Norway
3
Norwegian Institute for Nature Research (NINA),
NO-7485 Trondheim, Norway
4
Norwegian Institute for Nature Research (NINA),
NO-0349 Oslo, Norway
5
Grimsö Wildlife Research Station, Department of Ecology, Swedish
University of Agricultural Science, SE-730 91 Riddarhyttan, Sweden
Behavioral Ecology and Sociobiology (2020) 74: 52
https://doi.org/10.1007/s00265-020-2823-4
The Author(s) 2020
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
Keywords Carnivore .Climate change .Mustelid .Resource selection .Scatter hoarding .Seasonality
Introduction
Food caching is a widespread behavior in mammals, birds, and
arthropods (Vander Wall 1990; Sutton et al. 2016). Food-caching
animals can gain a nutritional or energetic advantage through this
behavior, as it can buffer seasonality in food availability and
increase the spatial distribution of their food supply in times of
scarcity (Vander Wall 1990). Access to cached food may be
crucial, especially during periods of high energy demands, such
as lactation and the rearing of young (Gittleman and Thompson
1988;Persson2005; Inman et al. 2012a; Derbyshire et al. 2015).
Food-caching behavior involves the following: (1) the storage of
food before consumption, through transport, placement, and con-
cealment; and (2) the recovery and consumption of the cache
food (Vander Wall 1990).
For caching behavior to be advantageous, the gain from
storage and recovery should outweigh the cost of caching
(Andersson and Krebs 1978; Alpern et al. 2012). Animals
have evolved several strategies to maximize the benefits of
caching, such as preventing or minimizing competition
through cache placement, concealment, and dispersion, by
optimizing transport distance (Stapanian and Smith 1978;
Rong et al. 2013), and through varying recovery strategies.
Recovery can occur through olfactory or visual senses, spatial
memory, or in opportunistic manner (Kamil and Balda 1985;
Vander Wall 1990; Phillips et al. 1991; Vander Wall and
Jenkins 2003). Food items can be either stored closely togeth-
er (larder hoarding; Jenkins and Breck 1998)orasdispersed
caches (scatter hoarding; Brodin 2010), and for short-term
(hours to days) or long-term periods (weeks to months,
Vander Wall 1990; or even years, Smith 1968). Long-term
caching of seeds and nuts is a common behavior of several
bird species (Clayton and Krebs 1995) and rodents (Aleksiuk
1970; Wauters et al. 1995). Short-term caching has been ob-
served in several large northern predators such as bears (Ursus
spp.; Elgmork 1982) and the Eurasian lynx (Lynx lynx;
Jedrzejewski et al. 1993vrum2000), who cover their prey
with snow, earth, or plant material when temporarily leaving
the carcass (Vander Wall 1990).
Many mustelid species are known to cache food, e.g., the
least weasel (Mustela nivalis; Criddle 1947), the Eurasian ot-
ter (Lutra lutra; Lanszki et al. 2006), the American mink
(Neovision vision; Yeager 1943), the American marten
(Martes americana; Henry et al. 1990), the Tayra (Eira
barbara; Soley and Alvarado-Díaz 2011), and the American
badger (Taxidae taxus;Michener2000). The worlds largest
terrestrial mustelid, the wolverine (Gulo gulo), inhabits unpro-
ductive and highly seasonal environments in boreal forests
and alpine tundra in the northern hemisphere (Inman et al.
2012a). As a facultative predator and scavenger, the wolverine
benefits from an opportunistic food acquisition strategy
(Lofroth et al. 2007; Van Dijk et al. 2008; Inman et al.
2012a; Mattisson et al. 2016). Morphologically and behavior-
ally, the wolverine is well adapted to roam large areas in
search of carcasses (Banci 1994). Ungulates are an important
part of the wolverines diet in most areas, although diet com-
position shifts according to available resources (Van Dijk et al.
2008; Dalerum et al. 2009; Mattisson et al. 2016). While it is
generally accepted that wolverines cache food for later con-
sumption (Krott 1960;Haglund1966; Inman et al. 2012a),
few studies have described their food-caching behavior (but
see Magoun 1987; Samelius et al. 2002; Wright and Ernst
2004). Caching facilitates the occupancy of unproductive hab-
itat by improving food predictability and by allowing wolver-
ines to take advantage of sudden food bonanzas (Vander Wall
1990; Inman et al. 2012a). Wolverine food caches are mostly
located in secluded and cold microhabitats (e.g., snow,
swamps, and cavities under boulders), referred to as natural
refrigeratorsin the literature (Haglund 1966;Bevanger1992;
Inman et al. 2012a). Food degradation by insects and bacteria
can be slowed down by caching food in cold and dark envi-
ronments (Sutton et al. 2016). As wolverines cache highly
perishable food (i.e., meat) for long-term storage, the wolver-
ine is predicted to be one of the caching vertebrates most
susceptible to climate change (Sutton et al. 2016). Caching
structures that function as natural refrigerators can also reduce
competition from other scavengers (Hopewell et al. 2008)by
decreasing pilfering (Vander Wall and Jenkins 2003). The
cache site can protect food from degradation and from pil-
ferers that rely on visual or olfactory senses. Wolverine cach-
ing behavior can thus fit two, in literature proposed, hypothe-
ses: the habitat structure hypothesis (i.e., careful cache
placement in specific habitat, to decrease the probability of
losing large quantities of food to pilferers; Steele et al. 2013)
and the refrigeration hypothesis (i.e., storage in caches that
preserve food well; Inman et al. 2012a), but these might be
difficult to disentangle in practice.
The goal of this study was to describe different spatial
components of the wolverines caching behavior. We discuss
our findings in the perspective of the habitat structure hypoth-
esis and the refrigeration hypothesis. First, we aimed to assess
whether wolverines are scatter hoarders or larder hoarders.
Spreading caches across space can reduce the risk of pilferage
(Vander Wall 1990) but requires more sophisticated spatial
cognition for cache recovery. Scattered hoarding fits well
within the territorial defense behavior displayed by wolverines
(Mattisson et al. 2011b). Secondly, we investigated selection
of caching locations by wolverines. We expected wolverines
to select locations with favorable conditions for both preser-
vation of food (i.e., cold, dark places) and protection from
52 Page 2 of 13 Behav Ecol Sociobiol (2020) 74: 52
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chemically and visually orientated pilferers. In winter, snow
coverage provides plentiful opportunities for caching. For
long-term storage (after snowmelt), we expected underlying
structures (e.g., secluded cavities in-between boulders) to be
important. Boulder structures are most common in steep and
rugged terrain, offering many potential microhabitat structures
suitable for caching year around. North- and east-facing
slopes retain snow longer in spring and remain cooler in sum-
mer due to shorter sun exposure and can therefore be expected
to preserve cached food longer. Selection of specific locations
for caching may be more critical in summer than in winter
because of the lack of snow in summer. Thirdly, we estimated
the distance at which wolverines transported food items from
a food source to a caching site. It has been suggested that
caching should occur quickly and in close proximity to the
source (Clarkson et al. 1986), as caching at long distances
reduces the available time for removing food at the source,
especially if other competitors are present (Hopewell et al.
2008). Long distances will also increase traveling costs but
might, on the other hand, offer better caching habitat for long-
term storage, as well as better food dispersion within a terri-
tory. To maximize food gain under competition pressure, we
expect wolverines to transport food shorter distances when
scavenging from ungulate carcasses that were killed by anoth-
er carnivore than if killed by the wolverine itself. Similar,
when scavenging on ungulates that died of natural causes,
competition is excepted to be high as other scavengers most
likely are present before, or at the same time as the wolverine.
Additionally, wolverines might cache at far distances when
competition is low to optimize suitability of caching site hab-
itat or to increase resource dispersion.
Materials and methods
Study area
The study was carried out in four areas on the Scandinavian
Peninsula Finnmark (70°10N, 24°70E), Troms (69°00N,
19°90E), and Nord-Trøndelag (64°30N, 12°50E) counties
in Norway, and the Sarek region (67°00N, 17°40E) in
Sweden (Fig. 1). The climate in Nord-Trøndelag and Sarek
is continental while Troms and Finnmark have a coastal alpine
climate. All areas are generally covered with snow from
November to May. Sarek, Troms, and Finnmark are dominat-
ed by alpine tundra, where mountain birch forest (Betula
pubescens) forms the treeline. Patches of pine forest (Pinus
sylvestris) can be found in Finnmark and Troms, while north-
ern boreal forest, dominated by conifer (Pinus sylvestris,
Picea abies), interspersed with bogs and mires, is common
in Nord-Trøndelag and at lower elevations in Sarek. Sarek
and Troms are characterized by steep alpine topography with
peaks up to ~ 2000 m.a.s.l. The topography in Finnmark and
Nord-Trøndelag is more open and gentler than in Sarek and
Troms, and with elevations ranging up to ~ 1100 and
1500 m.a.s.l. Free-ranging semi-domestic reindeer (Rangifer
tarandus) and moose (Alces alces) are the main sources of
carrion in all areas. In the Norwegian areas, free-ranging do-
mestic sheep (Ovis aries) are also a potential source of carrion
during summer in most areas. Other large carnivores present at
varying densities in the study areas were Eurasian lynx and
brown bears (Ursus arctos).
Study animals
Between 2008 and 2014, wolverines were anesthetized by
darting from helicopter and equipped with either a GSM or
UHF communication type GPS collar (GPS plus mini,
Vectronic Aerospace GmbH, Berlin, Germany). Capture and
handling followed existing protocols (Arnemo et al. 2012).
GPS collars were originally programmed to take one to eight
locations per day. Collars were reprogrammed to take between
19 and 48 locations per day in the Norwegian areas, and 38
and 96 locations per day in the Sarek area, during pre-set
intensive periods of three to 8 weeks, with the aim to study
diet and predation by wolverines (see Mattisson et al. 2016).
Due to collar failure, some periods were shorter than planned
(minimum 1 week). Age (subadult 12 years or adult
2 years), sex and reproductive status (male, single female, or
female with cubs) of the wolverine, whether the wolverine had
established a territory (stationary) or not (dispersing),and sea-
son (winter, OctoberApril; summer, MaySeptember) were
assigned to each intensive monitoring period. Wolverine es-
tablishment was determined by visually studying all available
Fig. 1 The four study areas in Scandinavia. NT Nord-Trøndelag, S Sarek,
T Troms, and F Finnmark
Behav Ecol Sociobiol (2020) 74: 52 Page 3 of 13 52
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
GPS locations for each individual. If the GPS locations indi-
cated a steady home range with no long-range movements, we
considered the wolverine as stationary.
Detecting food caches and food sources
Diet studies were carried out on 38 wolverines, including
2090 monitoring days spread out over 33 intensive monitoring
periods in summer and 33 periods in winter (14 per individ-
ual). During the intensive periods, clusters of GPS locations,
defined as two locations within 100 m of each other, were
identified and investigated in the field (see Mattisson et al.
2016). Initially, we visited all clusters that were possible to
reach, but as our experience grew, clusters with patterns char-
acteristic of daybeds (i.e., 2 daytime-only consecutive loca-
tions within a very limited area, with no revisits) were given
less priority. In winter, avalanche risk sometimes prohibited
visits to clusters in steep terrain. Although the primary objec-
tive was to document predation events, we registered findings
at all clusters. A cluster was classified as a food cache when
only parts of a carcass (e.g., a leg or a head) were found, which
had clearly been carried away from the site where the ungulate
had died, and which had been stored by the wolverine. Holes
with signs of digging, interpreted as an attempt to store or
retrieve food, were also identified as food caches. We assumed
that signs of caching or digging, observed at the site of the
GPS locations in a cluster, were caused by the focal wolverine.
A cluster was defined as a food source when we found a
relatively complete carcass (from predation, natural, or un-
known cause of death) or an anthropogenic food deposit such
as bait stations and slaughter remains. The cause of death for
ungulate carcasses was determined following the
methodology in Mattisson et al. (2016) appendix S1. When
we only found food remains (chewed bones and hairs) with no
indication that anything had been hidden, the cluster was de-
fined as a feeding place and thus separated from caches.
The definition of a food cache was consistent throughout
the study, but the focus on caches specifically developed over
time. Therefore, the registration of caches intensified in later
years. It is likely that we have underestimated the number of
caches by wolverines in the beginning of the study.
Additionally, when a cluster was registered as a cache, we
did not always register details such as microhabitat (e.g., boul-
der cavities, bogs, or snow) or species of the stored food item.
It was also harder to document caches in winter, as we did not
want to cause unnecessary disturbance by digging out holes
found in the snow to document potential food items.
Additionally, we may have failed to detectwell-hidden caches
with no signs of activity, for example, in bogs, or during win-
ter when the wind in combination with snowfall can rapidly
cover signs of food caching. Consequently, we were unable to
analyze seasonal and individual differences in the number of
created and utilized caches.
When possible, food caches were linked with a food source
using wolverine GPS locations. Wolverines often displayed a
repeated track between the food source and various cache
locations (Supplementary material Fig. S1,S2). This linkage
was occasionally confirmed in the field by snow tracking or
by linking the species and age of cached food to the source.
We often found prey items of very different age at the same
caching site indicating that the caching site had been reused by
the wolverine. This makes it difficult to determine whether a
cache that could not be linked to a food source was newly
created when discovered (i.e., the wolverine just moved a food
item there) or utilized (i.e., the wolverine visited the cache to
either eat, control, or restock it). If a wolverine only passed a
carcass to take a single food item and did not stop or return, no
cluster would have been formed (2 GPS locations), and we
would not have detected the food source.
It was not possible to record data blindly because our study
only involved focal animals in the field.
Cache dispersion
We visualized the cache dispersion pattern per intensive peri-
od for wolverines with 10 food caches, including six inten-
sive periods (summer only) from five wolverines
(Supplementary material Table S1). Two dispersing individ-
uals with sufficient sample sizes were excluded, as they did
not maintain a home range, and the lack of a territory is likely
to influence cache dispersion.
We created separate 100% minimum convex polygons
(MCPs) for the areas utilized by the wolverines during each
of the intensive periods, and plotted these together with the
associated caches and food sources, to illustrate the spatial
spreading of the caches and whether the location of the cache
was influenced by the location of the source. Additionally, to
compare how the utilized area and caching pattern related to
individual home ranges, we estimated and plotted home
ranges (100% MCP) based on all available GPS locations
for each wolverine. The duration of periods used to estimate
individual home ranges differed between individuals
(Supplementary material Table S1). However, wolverines
use > 75% of their entire multi-year home range within a
month (Inman et al. 2012b); thus, home ranges calculated
for short-term periods (3 months) should still give a represen-
tative reflection of their complete home range. We additional-
ly calculated the Euclidean distance between all caches per
stationary individual as an attempt to further describe the spac-
ing of caches.
Selection of habitat for caching sites
Selection of habitat for caching sites occurs when the cache is
created, i.e., when a food item is moved there. Therefore, to
characterize habitats that were chosen as caching sites by
52 Page 4 of 13 Behav Ecol Sociobiol (2020) 74: 52
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wolverines, we only included caches that we could link to a
food source (86 in summer and 42 in winter). By doing this,
we could safely assume that food was cached at these sites
when the cluster of GPS locations was formed (and not during
a recovery attempt). To determine habitat availability near the
food source, we created 20 random locations inside a buffer
zone around the source, with a radius equal to the 90th per-
centile of the distance between sources and caches in this
study (2638 m).
As the microhabitat at food caches was only registered in
the field for 46% of the caches, and was not available for
random locations, we used environmental maps to retrieve
the habitat for all locations. These maps poorly represent the
microhabitat used by wolverines for caching, but rather reflect
the generalhabitat at the caching site. We intersected the cache
and random locations with the following environmental raster
maps: vegetation (Swedish Corine land cover map
Lantmäteriet, 25 × 25 m merged with Northern Research
Institutes vegetation map, Norway, 30 × 30 m into a 25 ×
25 m raster), elevation, slope, aspect, and ruggedness, all de-
rived from DEM 50 × 50 m (Norge digital Statens kartverk,
Geographical data Sweden, Lantmäteriet). Ruggedness was
calculated from the elevation map as vector ruggedness mea-
sure index (Sappington et al. 2007) with neighborhood size
three (to include all neighboring cells) in GRASS GIS 7
(GRASS Development Team 2017). Due to the relatively
small sample size of caches, we grouped the original vegeta-
tion classes into four classes: barren areas, forest, open areas
with vegetation, and snow-patch vegetation (Supplementary
material Table S2). However, a very low sample size in barren
areas in winter forced us to pool this class with snow-patch
vegetationin winter. One cache was excluded as it was located
outside available environmental maps. All spatial analyses
were performed in R 3.1.1 (R Development Core Team
2017) with the packages sp (Pebesma and Bivand 2005)and
raster (Hijmans 2016), or in QGIS 2.14-Essen (QGIS
Development Team 2016).
We applied a conditional logistic regression to analyze selec-
tion of habitat for caching, because it allows each cache to be
linked with its random locations (thus conditioning use on avail-
ability) by including a stratum. Additionally, we included animal
ID in the models as a cluster term to account for autocorrelation
issues. To detect potential seasonal differences, we performed
this analysis separately for summer and winter. To account for
circularity in aspect, we converted degrees to radians and includ-
ed the aspect as both eastness (sine) and northness (cosine) trans-
formation. We used a pairwise Pearson rank correlation to test for
collinearity among the explanatory variables (r> 0.60), though
none of the variables was collinear. We performed model selec-
tion with the use of Akaikes information criterion corrected for
small sample sizes (AIC
c
) and considered models to fit the data
equally well if ΔAIC
c
were smaller than or equal to two
(Burnham and Anderson 2002). All continuous explanatory
variables were initially evaluated to determine if a non-linear
second order polynomial generated a better fit, according to
AIC
c
, than a linear. Only the best fit of the two was kept for
further model selection. Ruggedness was transformed by taking
its natural logarithm before entering the models, to limit the
influence of outliers.
Caching distance
To study the mechanisms influencing transport distance between
a food source and a cache, we calculated the Euclidean distance
between linked caches and food sources. Because some caches
were linked to two or three sources, our sample size was greater
than in the habitat selection analysis. It was possible to identify
149 linked food sources and caches, 70 by females (n
ind.
=16)
and79bymales(n
ind.
= 16). To test if the habitat quality for
caching was an important motivator for wolverines to cache far
away from the source, we created a Δhabitat variable where we
estimated the differences in habitat quality between the cache and
its source. Habitat quality was estimated by predicting the odds
ratio using the top-ranked habitat selection model from above. A
positive Δhabitat indicates that the wolverine moved to a better
habitat for caching than the one available at the food source (and
theconverseforanegativeΔhabitat). In addition, we tested if the
distance was related to the habitat quality at the caching site
directly, i.e., unrelated to the habitat at the source. Transport
distance may also be influenced by potential competition at the
food source. To test for this, we grouped the food sources into (1)
ungulates killed by the focal wolverine (n= 56), (2) ungulates
killed by other carnivores (n= 27), or (3) ungulates dying from
other causes or from anthropogenic sources (n= 46). Among the
wolverine-killed ungulates, interpretation of GPS data suggested
seven ungulates to have been communally killed by two (female,
male) or three (female, male, yearling male) GPS-collared wol-
verines. These were treated similar as when only one GPS-
collared wolverine had been involved in the killing. We excluded
two caches made by a GPS-collared wolverine that were linked
to an ungulate killed by an uncollared wolverine. The transport
distance might, in these two cases, be different as the caching
wolverine was not first on site. Caching distance will be restricted
by home range size (which is larger for males than for females;
Mattisson et al. 2011b) and can potentially be influenced by the
presence of cubs; thus, we also tested for sex and reproductive
status in the models.
Caching distance was analyzed using linear models. As the
response variable was right-skewed, we log transformed the
variable before entering it to the model. To correct for poten-
tial autocorrelation of data from the same wolverine and/or
study area, we first fitted a full linear mixed-effects model
(LMER) with individual wolverine and study area (combined
and separately) as random factors. However, as very little of
the variance were explained by the random effects (i.e., no
evidence of pseudo replication), we continued with a simpler
Behav Ecol Sociobiol (2020) 74: 52 Page 5 of 13 52
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model excluding random factors (LM). Model selection was
performed using AIC
c
. All continuous explanatory variables
were initially included as both linear and quadratic terms, but
only the term generating the model with the lowest AIC
c
value
was kept in further model selection. As the variable Δhabitat
was derived using the variable habitat quality at the caching
site, these could not be combined in the same model.
Similarly, reproductive status could not be combined with
sex as only females fit the family category. Therefore, we first
set up competing models with these variables as single pre-
dictors. We continued the model selection including the vari-
ables Δhabitat and sex as they performed better than models
with habitat quality at the caching site and reproductive status,
according to AIC
c
. Vegetation type was not available for either
the cache or the source for five-linked caches and food
sources; thus, we excluded these from the analysis. All statis-
tical analyses were done in R 3.1.1 with the package lme4
(Bates et al. 2015).
Results
We identified 303 food caches, 146 by males (n
ind.
= 17), 117 by
single females (n
ind
= 16), and 40 by females with cubs (n
ind
=8),
of which 215 were found in summer and 88 in winter. The most
common microhabitats of caching sites in summer were boulder
cavities (n= 72), excavated holes in bogs (n= 14), and in
persistent snow patches (n= 9). Some caches were covered un-
derneath moss or vegetation (n= 7) or completely submerged
under water (n= 1). In winter, the ground was mostly covered
with snow, and for 20 caches, we only found holes in the snow,
but for an additional 14 snow-covered caches, we detected boul-
der cavities as the underlying microhabitat structure. For two
caches, vegetation or soil was found around the holes in the
snow, indicating caching below the snow cover. One cache was
submerged under non-frozenwater. Example photos of cach-
ing sites are shown in Fig. 2and in supplementary material Fig.
S3. For 72% of all caches, it was possible to identify the species
of the food item. Reindeer was by far the most cached prey
(84%; n= 177). Other identified species were moose (n=25),
sheep (n= 5), unknown ungulate (n=2),andredfox(n=2).
On average, we found 0.16 caches per wolverine monitoring
day, ranging from none to 0.96 caches/day among all wolverine
individuals. This should be regarded as a minimum estimate of
caching as we did not register all caches (see methods).
In total, we found 460 food sources during the study, of
which 161 were wolverine-killed ungulates (157 reindeer and
4 sheep). Othercarnivores provided an additional140 sources,
mostly reindeer (n= 129), where lynx was the primary preda-
tor (n= 121). The remaining 159 sources were either ungu-
lates that died from natural or unknown causes (106 reindeer,
33 moose, and 1 sheep), or of anthropogenic origin (11
slaughter remains and 8 bait stations). We could link 149 of
all food sources to caches (32%). These food sources were
Photo: Jenny Masson
Photo: Zea Walton
Photo: John Ivar Larsen Photo: Jenny Masson Photo: Jenny Masson Photo: Jenny Masson
abdc
Photo: Geir Rune Rauset
Photo: Zea Walton
efghi
Photo: Jenny Masson
Fig. 2 Photos of caching sites in winter and late spring (ad)andin
summer (ei). aA hole in the snow with hair of a reindeer spread
around. bParts of a reindeer found in a cavity between the snow and a
cliff. c,dRemains of a reindeer becoming visible after the beginning of
the snowmelt in late spring. The holes continue deep down into the
remaining snow. eA hoof of a moose buried into vegetation (the hole
has been exposed by us). fPart of a reindeer skull found in a hole in a high
alpine mire. gA cache in a bog. hWell-reused caching site in boulders
containing prey remains of different ages. Note the dark green moss
indicating a cold and dark micro-environment. iA reindeer skull found
hidden in a boulder field (now exposed)
52 Page 6 of 13 Behav Ecol Sociobiol (2020) 74: 52
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
ungulates killed by wolverines (n= 63), by other carnivores
(n= 35, including 25 known lynx-killed reindeer), or by other
causes (n=51).
In 14 caches, wolverines had gathered food items from
more than one food source (12 caches had 2 sources and 4
had 3 sources). Furthermore, 11% of the linked food sources
were the origin of more than one-documented cache (10
sources with 2 caches, 3 with 3 caches, 1 with 4 caches, and
2 with 6 caches). We documented that 21% of the food sources
were visited by more than one wolverine.
Cache dispersion
Both caches and food sources were distributed across wolver-
ine home ranges (Fig. 3), and caches were often spatially
clustered around the food sources. The median distance be-
tween caches for 16 stationary females was 7.1 km (n=446,
mean = 7.2 km, SD = 5.98) and 10.9 km for 8 stationary males
(n= 192, mean = 13.9 km, SD = 7.83). This approaches the
approximate radius of an average home range size (females
7.9 km, males 15.3 km; Mattisson et al. 2011b).
Selection of habitat for caching sites
The best model for habitat selection for caching sites in both
summer and winter included the polynomial term of slope and
ruggedness (Table 1, Supplementary material Table S3,S4). In
summer, the best model additionally included vegetation type. In
both seasons, wolverines selected habitat with slopes steeper than
approximately 9° for caching (Fig. 4a), indicating low seasonal
differentiation. Flat terrain was avoided by caching wolverines in
both summer and winter, while highly rugged terrain was select-
ed stronger in summer than in winter (Fig. 4b). In summer,
wolverines selected for forest habitat and against open areas with
vegetation when caching (Fig. 4c).
In summer, there were no other models within two AIC
c
units (Supplementary material Table S3). In winter, the sepa-
rate addition of northness, eastness, or elevation to the top
model increased AIC
c
by 1.2, 1.7, and 1.7, respectively
(Supplementary material Table S4). However, the estimates
for elevation and eastness had larger standard errors than their
estimates. Northness explained some variation, indicating that
wolverines selected for more south-facing slopes.
Fig. 3 Plots of home ranges
(dashed black lines), with food
caches (o) and food sources (x)
documented during periods of in-
tensive monitoring of wolverines
in summer. Area use restricted to
the intensive period is shown as
solid gray lines. Durations of the
intensive periods and the home
ranges differ between individuals
(see Supplementary material
Table S1). Plots cand fbelong to
the same male individual that ex-
panded his home range during the
study due to the death of a neigh-
boring male wolverine. The fe-
male in plot ehad dependent
cubs. Values on xand yaxis rep-
resent coordinates in meters,
displayed in Universal Transverse
Mercator (UTM) zone 33N. Note
that the scale is different for dif-
ferent plots
Behav Ecol Sociobiol (2020) 74: 52 Page 7 of 13 52
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
Caching distance
The median distance between food sources and food caches
was 499 m (mean = 1120 m, SD = 1673 m, range = 35
9329 m, n= 149). Of all distances, 90% were shorter than
2500 m (Supplementary material Fig. S4). The longest dis-
tance was 9.3 km. Based on model selection, distances be-
tween caches and sources were best explained by the origin
of the food source and Δhabitat (Supplementary material
Table S5). Wolverines cached food items closer to the source
if the ungulate was killed by another carnivore than if it was
killed by a wolverine (Fig. 5a,β= 0.59, CI 95% = 0.11
1.108) or if the ungulate died from other causes (Fig. 5a,
β= 0.49, CI 95% = 0.0050.99). Distance between the cache
and the source increased when Δhabitat increased, suggesting
that wolverines transported food further away from the source
to find more suitable habitat (Fig. 5b,β= 0.16, CI 95% =
0.060.25). In 98 cases (68%), the habitat at the cache was
superior to that at the source; in 45 cases (31%), it was worse,
and for one the same. However, the best model only explained
about 12% of the observed variation (R
2
= 0.12), and five
other models were within two ΔAIC
c
(Supplementary
material Table S5). All these models included Δhabitat but
with different combinations of the variable food source origin,
sex, and season. Sex, included in the second, fourth, and sixth
ranked models, showed slightly longer caching distances for
males than for females in all models where it was included
(2nd model β= 0.22, CI 95% = 0.150.59). Season, includ-
ed in the third, fourth, fifth, and sixth ranked models, showed
shorter caching distance in winter than in summer (3rd model
β=0.22, CI 95% = 0.620.18).
Discussion
Wolverines visited food caches at a rate of at least one per
6 days in both winter and summer, suggesting that cached
food is an important part of wolverine foraging behavior
throughout the whole year. Wolverines generally inhabit un-
productive and highly seasonal environments and are there-
fore likely to take advantage of any abundance of food re-
sources regardless of whether it occurs in winter or in summer
(Magoun 1987; Mattisson et al. 2016). Sudden food bonanzas,
such as ungulates killed by avalanches, and predictable
Table 1 Estimates from the best
ranked conditional logistic
regression models, for habitat
selection at caching sites by
wolverines (based on 86 food-
caching sites in summer and 42 in
winter) in Scandinavia
Summer Winter
β
a
CI 2.5% CI 97.5% β
a
CI 2.5% CI 97.5%
Vegetation type - forest
b
0.38 0.47 1.22
Vegetation type - open
b
0.74 1.50 0.03
Vegetation type - snow-patch
b
0.11 0.61 0.83
Slope 34.26 14.86 53.65 16.63 3.12 30.15
Slope
2
8.62 18.05 7.26 4.04 12.03 3.95
ln(ruggedness) 27.76 10.69 44.84 35.61 14.30 56.92
ln(ruggedness)
2
5.40 18.05 7.26 20.40 31.34 9.45
a
βis on the logit-scale
b
The reference category is barren areas
abc
Fig. 4 Predicted log-odds with 95% confidence intervals (shaded area
and error bars) for informative variables included in the model that best
explain habitat selection of wolverines for caching in Scandinavia in
summer (top row) and in winter (bottom row). Slope (a), ruggedness
(b), and vegetation type in summer (c; B barren areas, F forest, O open
areas with vegetation, S snow-patch vegetation). The dashed line indi-
cates a threshold where log-odds below the line show avoidance and
above it show selection
52 Page 8 of 13 Behav Ecol Sociobiol (2020) 74: 52
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
seasonal occurrences, such as ungulate calving periods, pro-
vide opportunities for caching that can buffer against periods
of food shortage. Food shortage is expected to be most com-
mon in winter (Inman et al. 2012a), but as wolverines in
northern Scandinavia largely rely on migratory semi-
domestic reindeer (Mattisson et al. 2016), food shortage may
occur also during summer, as wolverines do not follow rein-
deer on their migration (Walton 2015). Most of the intensive
periods included in this study were conducted during the sea-
sons when the focal wolverine overlapped with the grazing
areas of semi-domestic reindeer (Mattisson et al. 2016), but
not all wolverines had access to reindeer year around (Walton
2015). The overall pattern that wolverines cache food across
seasons presumably facilitates optimal exploitation of tempo-
rary availability of reindeer.
The distance between caches found in this study suggests
that wolverines spread food caches across their home range.
The observed cache dispersion pattern suggests that the wol-
verine is a scatter hoarder (Vander Wall 1990). This seems to
be an efficient cache defense strategy that combines well with
the overall high activity pattern (Mattisson et al. 2010;Inman
et al. 2012b) and territoriality (Persson et al. 2010; Mattisson
et al. 2011b) of wolverines. The defense of a territory reduces
the risk of conspecifics consuming resources or robbing
caches (Vander Wall 1990), thus increasing the benefits from
food caching (Alpern et al. 2012). The spatial pattern we ob-
served is likely a result of food caches being linked to where
the food item becomes available and the distance the wolver-
ine is willing to transport a food item. Scattering caches de-
creases the likelihood of losing large quantities of food to
pilfering (Stapanian and Smith 1978; Vander Wall 2000;
Leaver 2004), but increases the cost related to caching
(Alpern et al. 2012) through handling, re-caching, and even-
tual recovery of numerous food items. As territory holders,
wolverines need an extensive spatial memory of their range,
aiding cache placement and recovery (Sherry 1984).
On some occasions, we observed more than one wolverine
using the same caching site at the same time, or at different
times. Whether these interactions at caches between overlap-
ping territory holders (Mattisson et al. 2011b) suggest com-
munal caching or pilferage is not known. Sharing resources
may be a beneficial strategy among breeding adults with com-
mon offspring, or between parents and offspring, while unre-
lated individuals are mostly excluded by territorial behavior.
However, young dispersing conspecifics may take the risk
involved in pilfering when food is scarce.
Wolverines selected caching sites in steep and rugged ter-
rain and preferred to cache in forest vegetation in summer,
when available. However, in areas with limited forest cover,
wolverines also cached in open alpine habitat with boulder
structures or bogs. These habitats possibly provide a larger
quantity of secluded, cold, and dark microhabitat structures
that may be better suited for preserving and disguise food
items when compared with flat open areas, rich in low alpine
vegetation. In addition, selectionof steep and rugged terrain is
in accordance with general habitat selections of wolverines
(Rauset et al. 2013). Contrary to our expectations, caching
wolverines did not select for shaded slopes, i.e., north- or
east-facing slopes. This may, however, be less important for
cached food preservation when the microhabitat (i.e., snow,
boulder cavities, or bogs) shields food items from the sun.
Caching under forest cover and other visually occludedplaces
might prevent avian scavengers from locating the caches.
Corvid and eagle species (Aquila chrysaetos,Haliaeetus
albicilla) are common in our study areas and are important
competitors of wolverines at carcasses (Mattisson et al. 2011a;
a
200
400
600
800
Carnivore Other Wolverine
Food source origin
Distance (meters)
b
500
1000
1500
2000
2500
−2 0 2 4 6
Delta habitat
Distance (meters)
Fig. 5 Mean distance between food sources and wolverine caching sites
dependingon(a) the origin of the food source: ungulates killed by the
wolverine (n= 60), ungulates killed by another carnivore species (n=33,
of which 23 were known to be killed by lynx), or ungulates that died from
other causes (n=55);and(b) increasing habitat quality from the source to
the cache location (Δhabitat). Estimates are obtained from the highest
ranked GLMM model and are shown with 95% confidence intervals
Behav Ecol Sociobiol (2020) 74: 52 Page 9 of 13 52
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
Henden et al. 2014;Gomoetal.2017), and at least, corvids
have the potential to be pilferers of wolverine caches. For
example, ravens (Corvus corax)havebeenobservedrobbing
caches of arctic foxes (Vulpes lagopus; Careau et al. 2007b).
Caching in bogs and water can be an efficient strategy to
disguise food smells from potential terrestrial pilferers, such
as the red fox which is one of the most common terrestrial
competitors in our study system.
Contrary to our expectations, we did not find a clear sea-
sonal difference in habitat selection for caching sites. The lack
of a seasonal selection pattern may be due to the relatively
small sample size of caching sites in winter, in combination
with the use of coarse-scale environmental maps that may not
sufficiently describe microhabitat. In both seasons, we docu-
mented cached food items in boulder cavities, snow, water,
and bogs. These structures provide cold and secluded environ-
ments that can act as natural refrigerators that delay decompo-
sition rates of cached food by bacteria and insects (Kruuk
1972; DeVault et al. 2004; Parmenter and MacMahon 2009)
and/or protect caches by masking visual and chemical clues
that can attract pilferers. In winter, when microhabitat struc-
tures are covered by snow, wolverines likely rely on their
spatial memory to locate suitable caching locations under-
neath the snow. Persistent snow cover offers ample opportu-
nities to cache food, and selecting caching locations in snow-
bed habitat with late spring snow cover could prove important
forfoodpredictabilityduringspringandearliersummer.A
study that mimicked caching by cougar (Puma concolor;
Bischoff-Mattson and Mattson 2009) showed that caching
served to reduce competition from arthropods and mi-
crobes, in addition to lowering detection rates of other
scavenging carnivores. Wolverines are known to cache
in trees (Krott 1960;Haglund1966), which does not de-
lay decomposition of cached food, but may allow for
short-term storage in areas where terrestrial scavengers
form the main source of competition.
Food sources (e.g., a large ungulate carcass) used by wol-
verines usually contain more food than a wolverine can trans-
port and cache in a single trip, and thus provide opportunities
to cache multiple items. Caching close to the source mini-
mizes costs associated with transport and allows wolverines
to secure as much food as possible before the arrival of com-
petitors. It is common for wolverines to scavenge from car-
casses killed by other carnivores, such as lynx (Mattisson et al.
2011a), wolves (Van Dijk et al. 2008), and brown bears
(Mattisson et al. 2016). However, this may involve a risk if
the other carnivore defends its kill (Inman et al. 2007; Kortello
et al. 2007; Jimenez et al. 2008). Wolverines reduce this risk
by mainly utilizing lynx-killed carcasses after they were aban-
doned by the lynx (Mattisson et al. 2011a), or while the lynx
was temporarily away (López-Bao et al. 2016). If we assume
that wolverines are not able to know when, or if, the predator
is coming back to a carcass, the shorter transport distance we
observed at kills from other carnivores is a favorable strategy
to quickly secure as much food as possible. However, caching
in close vicinity to the carcass may increase the risk of cache
pilferage (Tamura et al. 1999); also, the habitat near the car-
cass might not be optimal for long-term storage. When cach-
ing close to a carcass, wolverines may move caches to a more
suitable site at a later time, as observed in arctic foxes whilst
caching goose eggs (Careau et al. 2007a) and for other species
including rodents (Waite and Reeve 1992;Rongetal.2013)
and birds (Moore et al. 2007). We found indications that wol-
verines cached food further away from the carcass to find
more preferred habitat than the one available at the carcass.
Habitat has been shown to be an important motivator to hoard
further away from the source in various rodent species, likely
because preferred habitat decrease cache pilferage (Wang and
Corlett 2017). It is likely that other scavengers may detect
carcasses prior to the wolverine, which will increase compe-
tition at the food source (Selva and Fortuna 2007;Gomoetal.
2017). High numbers of birds can consume large quantities of
animal biomass over short periods of time (Selva 2004;
Wikenros et al. 2013). We found that wolverines transported
food items further distances when the food source was a
wolverine-killed ungulate. Presumably, the wolverine was
first on site and consequently had more time to find suitable
caching sites and spread them further away from the carcass.
The potential influence of climate change on various as-
pects of wolverine ecology (e.g., denning and caching) has
received increasing attention in recent years (Aubry et al.
2007;Schwartzetal.2009; Copeland et al. 2010;McKelvey
et al. 2011; Peacock 2011; Inman et al. 2012a;Webbetal.
2016;AronssonandPersson2017;Magounetal.2017).
Inman et al. (2012a)proposedarefrigeration-zonehypoth-
esis as a food and competition-based explanation for the ob-
served correlation between wolverine distribution and the area
encompassed by persistent spring snow cover (Copeland et al.
2010). Accordingly, the wolverine is suggested to be more
susceptible to climate change than most caching vertebrates
(Sutton et al. 2016). In this study, we confirm that caching is
common in wolverines of both sexes all year round and that
they seem to invest considerably in finding suitable caching
sites. Caching in steep and rugged terrain in unproductive
habitat types indicates a preference for less exposed sites that
can function as natural refrigerators and minimize pilfering.
The effort wolverines put into improving food predictability
and increasing their food supplies underlines the importance
of caching behavior for their survival and reproduction (Inman
et al. 2012a). Increasing temperatures as a consequence of
climate change may provide new challenges for wolverines
as it affects both the preservation of cached food (Sutton et al.
2016) and may increase occurrence of potential pilferers such
as the red fox (Elmhagen et al. 2015). It is however still not
fully understood which consequences this may have for the
demography and behavior of the wolverines.
52 Page 10 of 13 Behav Ecol Sociobiol (2020) 74: 52
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
Acknowledgments We thank P. Segerström, E. Segerström, T.
Strømseth, and J. M. Arnemo for capturing and collaring the wolverines,
and the State Nature Inspectorate, reindeer herders, and all additional
people that have contributed to captures and data collection in the field.
A special thanks to P. Segerström and G. R. Rauset for their support and
expertise, and to Z. Walton, A. Ordiz, and anonymous reviewers for
fruitful comments on earlier drafts. This MS is a continuation of a master
thesis by Bert van der Veen (https://brage.inn.no/inn-xmlui/bitstream/
handle/11250/2445533/vanderveen.pdf?sequence=1&isAllowed=y).
Funding information Open Access funding provided by Norwegian in-
stitute for nature research. This work was supported by the Swedish
Environmental Protection Agency, the Norwegian Environment
Agency, the Research Council of Norway (Project 212919), the
European Association for Zoo and Aquaria, the World Wide Fund for
Nature (Sweden), the Swedish Research Council for Environment,
Agricultural Sciences and Spatial Planning (Formas), the private founda-
tions Olle och Signhild Engkvists Stiftelser,and Marie-Claire
Cronstedts Stiftelse.The County administrations in Nord-Trøndelag,
Troms, and Finnmark, the Carnivore Management Boards in regions 6
and 8, and the Reindeer Development Fund in Norway also provided
considerable financial assistance.
Data availability The datasets analyzed during the current study are avail-
able at https://osf.io/8phf6(caching distance) and https://osf.io/5f46d
(habitat selection).
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
Ethical approval All applicable international, national, and/or institu-
tional guidelines for the care and use of animals were followed. All
procedures performed in studies involving animals were in accordance
with the ethical standards of the institution or practice at which the studies
were conducted. Capture and handling followed existing protocols
(Arnemo et al. 2012) and were approved by the Swedish Animal Ethics
Committee in Umeå (A11-12) and the Norwegian Experimental Animal
Ethics Committee (FOTS ID2826, FOTS ID5699, FOTS ID7017).
Open Access This article is licensed under a Creative Commons
Attribution 4.0 International License, which permits use, sharing,
adaptation, distribution and reproduction in any medium or format, as
long as you give appropriate credit to the original author(s) and the
source, provide a link to the Creative Commons licence, and indicate if
changes were made. The images or other third party material in this article
are included in the article's Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in the
article's Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
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... Slaktrester från älgjakten tillförs dock endast under en begränsad tid på året, i samband med älgjakten 5 . Men järven är en art anpassad till oförutsägbar födotillgång eftersom den lagrar mat i så kallade matgömmor 15 . Därför kan järven ha nytta av slaktrester även under en längre period på året än bara under jaktsäsongen och kan därmed ha stor betydelse för järvens mattillgång 2 . ...
... Att järvar är ensamlevande och revirhävdande med stora revir 2 , samt att stora delar av vårt studieområde ligger i den absolut sydligaste delen av järvens utbredningsområde, gör att tätheten generellt blir låg. Därför är det inte förvånande med en låg sannolikhet för besök av järv vid de olika födokällorna, trots att järven är en asätare som också lagrar mat 15 . När det gäller lagring av mat kan vi förvänta oss fler och korta besök vid de vargdödade kadavren, där det troligtvis finns mer biomassa att hämta och lagra. ...
Technical Report
Järven har under senare tid etablerat sig i Inre Skandinaviens skogsområden vilket även är vargens huvudsakliga utbredningsområde i Skandinavien. Det finns lite kunskap om järvens matvanor i detta område då mycket av den befintliga kunskapen om järven kommer från studier i fjälltrakterna. Järvar som lever i vargrevir har tillgång till föda från vargdödade klövdjur året om. Andelen tillgänglig mat från vargarnas byten varierar med deras storlek, då vargarna förtär en större andel av de ätliga delarna på mindre bytesdjur. Hur mycket vargarna lämnar efter sig varierar också med tid på året, då det t.ex., blir mindre mat över till asätande arter under sommaren. Människan bidrar också med stora mängder slaktrester under älgjakten och denna födoresurs nyttjas av olika asätare inklusive järv och varg. Slaktrester från älgjakten är dock sannolikt tillgängligt under en mer begränsad del av året jämfört med rester som vargar lämnat efter sig.
... Food caching (e.g. [23][24][25]) is one such sequence, as observed in many canids, which are active hunting predators storing food for later consumption [26]. Canid caching behaviour generally follows a distinctive sequence of food carrying, digging with forepaws, tamping with muzzle to press food into the soil, and head scooping to cover food with substrate [27]. ...
... Furthermore, as arctic foxes are territorial and tend to avoid territory borders [40], their territoriality could lead to non-random distribution of specific behaviours. For example, caches could be preferentially located away from territory edges to reduce pilferage, as observed in wolverines (Gulo gulo) that tend to cache food in sites less exposed to competitors [25]. Another interesting avenue would be to directly assess arctic fox tendencies to do cache pilfering in neighbour territories or along overlapping areas. ...
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Background Biologging now allows detailed recording of animal movement, thus informing behavioural ecology in ways unthinkable just a few years ago. In particular, combining GPS and accelerometry allows spatially explicit tracking of various behaviours, including predation events in large terrestrial mammalian predators. Specifically, identification of location clusters resulting from prey handling allows efficient location of killing events. For small predators with short prey handling times, however, identifying predation events through technology remains unresolved. We propose that a promising avenue emerges when specific foraging behaviours generate diagnostic acceleration patterns. One such example is the caching behaviour of the arctic fox ( Vulpes lagopus ), an active hunting predator strongly relying on food storage when living in proximity to bird colonies. Methods We equipped 16 Arctic foxes from Bylot Island (Nunavut, Canada) with GPS and accelerometers, yielding 23 fox-summers of movement data. Accelerometers recorded tri-axial acceleration at 50 Hz while we obtained a sample of simultaneous video recordings of fox behaviour. Multiple supervised machine learning algorithms were tested to classify accelerometry data into 4 behaviours: motionless, running, walking and digging, the latter being associated with food caching. Finally, we assessed the spatio-temporal concordance of fox digging and greater snow goose ( Anser caerulescens antlanticus ) nesting, to test the ecological relevance of our behavioural classification in a well-known study system dominated by top-down trophic interactions. Results The random forest model yielded the best behavioural classification, with accuracies for each behaviour over 96%. Overall, arctic foxes spent 49% of the time motionless, 34% running, 9% walking, and 8% digging. The probability of digging increased with goose nest density and this result held during both goose egg incubation and brooding periods. Conclusions Accelerometry combined with GPS allowed us to track across space and time a critical foraging behaviour from a small active hunting predator, informing on spatio-temporal distribution of predation risk in an Arctic vertebrate community. Our study opens new possibilities for assessing the foraging behaviour of terrestrial predators, a key step to disentangle the subtle mechanisms structuring many predator–prey interactions and trophic networks.
... RF results supported the hypothesis that distance to high-elevation talus and snow water equivalent would be the most important variables for wolverine habitat selection. Talus is an important habitat structure (Copeland 1996;May et al. 2012;Inman et al. 2013), and there is evidence that wolverines use talus and boulder fields extensively for food caching, denning, microrefugia from warm temperatures during summer, and hunting (Kortello et al. 2019;van der Veen et al. 2020). Given the broad range of physical habitat structure used for various wolverine behaviors, including reproductive behavior, the importance of talus is logical for both sexes. ...
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Article
In the conterminous United States, wolverines (Gulo gulo) occupy semi-isolated patches of subalpine habitats at naturally low densities. Determining how to model wolverine habitat, particularly across multiple scales, can contribute greatly to wolverine conservation efforts. We used the machine-learning algorithm random forest to determine how a novel analysis approach compared to the existing literature for future wolverine conservation efforts. We also determined how well a small suite of variables explained wolverine habitat use patterns at the second- and third-order selection scale by sex. We found that the importance of habitat covariates differed slightly by sex and selection scales. Snow water equivalent, distance to high-elevation talus, and latitude-adjusted elevation were the driving selective forces for wolverines across the Greater Yellowstone Ecosystem at both selection orders but performed better at the second order. Overall, our results indicate that wolverine habitat selection is, in large part, broadly explained by high-elevation structural features, and this confirms existing data. Our results suggest that for third-order analyses, additional fine-scale habitat data are necessary.
... There are also species which have several den sites during a denning season. Wolves (Canis lupus) make use of one natal den site and some maternal den sites (up to 3), before they switch to using rendezvous sites (Theuerkauf et al., 2003;Alfredéen, 2006;Sidorovich et al., 2017). Arctic foxes (Alopex lagopus) can use several den sites simultaneously within one denning season, and they may also reuse these den sites over many years (Eberhardt et al., 1983). ...
... In my study area, reindeer are the main food resource for wolverines. Wolverines are also known for their food caching capabilities (van der Veen et al., 2020). Therefore, they can buffer for low resource Figure 7: The hazard ratio estimations for the temperature during the day when denning in forest habitat (light blue = 95% confidence intervals; grey = amount of data). ...
... På grunn av at feltpersonell i noen tilfeller kom sent på klusterne kan også dette ha ført til en underestimering av drapsraten fordi en da ikke kunne avgjøre om reinsdyret var drept av den GPS-merkede bjørnen eller ikke. I tillegg kan åtselsetere som jerv, rødrev og ravn (Corvus corax) spise opp kadavre i løpet av kort tid (Selva et al., 2003;van der Veen et al., 2020). ...
... For three decades no wolverine signs have been observed in the Altai Mountains (Sinkiang, northwestern China) likely due to habitat loss, food limitation, and poaching (Zhang et al., 2007). The paucity of Russian and Asian research in this review could be an English-language, western-science indexing bias (Konno et al., 2020;Trisos et al., 2021), or reflect real differences in researchers' interests, national conservation priorities, and available funding for research. ...
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Wolverines are vulnerable to multiple, widespread, increasing forms of human activity so have become an indicator of conservation success or failure for northern ecosystems. Logistically difficult to research, the last two decades have seen marked changes in technology yielding new insights. We reviewed and synthesized this recent research and asked: what are the known drivers of wolverine populations and distribution, is there consensus on mechanisms for populations dynamics, and how can this knowledge inform wolverine conservation? From 156 peer-reviewed papers we observed wolverine research varies geographically in volume, and especially in focus. Most papers arose from Canada and the USA, whereas Scandinavia led Palearctic efforts; large gaps exist outside that region. DNA and telemetry are the most common modes of inquiry, with camera traps increasing recently. In Scandinavia coordinated long-term monitoring programs have yielded substantial information; the Nearctic relied on stand-alone research until the recent USA multi-state monitoring project, and Canada lacks such coordination. Globally, protected areas are important for wolverine conservation, but effective landscape and population management in the working land base is vital. The dual drivers of climate and landscape change manifest across wolverines’ range, but past and current correlation between them remains a confound. Coordinated continental-scale analyses across gradients of development and climate change are needed to parse apart drivers of declines at macroecological scales, to inform effective conservation decisions.
Article
Full-text available
Being the first to discover a resource can provide a competitive advantage (priority effect), even for an animal that is inferior in aggressive contests. Nicrophorus spp. (burying beetles) are known for caching a small vertebrate carcass as provision for their young, reducing volatile cues available to rivals by burying the carcass (vertical movement) and by altering the microbial community. A decomposing carcass, however, can leave cues (residues of decay) on soil and leaf litter that a burying beetle has less opportunity to neutralize. I investigated whether horizontal movement of the carcass by burying beetles, separating the carcass from soil at the site of death, might reduce competition from congeners. When fresh carcasses were placed in the field on top of soil with residues of decay, akin to no horizontal displacement, carcasses were discovered within 24 h by free-flying competitors more frequently (58.2%) than when the carcass was placed 1 m from treated soil (8.3%). In a second experiment, carcasses were more likely to be discovered by burying beetles when a chemical attractant (methyl thiocyanate) was placed near a carcass (0.03 and 0.25 m) than when it was placed more distant (1 and 5 m) or for controls (no attractant). The results suggest that horizontal displacement of a carcass after discovery serves not only to locate a suitable spot for burial but also to reduce information available to rivals searching for the resource.
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Being the first to discover a resource can provide a competitive advantage (priority effect), even for an animal that is inferior in aggressive contests. Nicrophorus spp. (burying beetles) are known for caching a small vertebrate carcass as provision for their young, reducing volatile cues available to rivals by burying the carcass (vertical movement) and by altering the microbial community. A decomposing carcass, however, can leave cues (residues of decay) on soil and leaf litter that a burying beetle has less opportunity to neutralize. I investigated whether horizontal movement of the carcass by burying beetles, separating the carcass from soil at the site of death, might reduce competition from congeners. When carcasses were placed in the field along with soil of decay, akin to no horizontal displacement, carcasses were discovered within 24 h by free-flying competitors more frequently (58.2%) than when the carcass was placed 1 m from treated soil (8.3%). In a second experiment, carcasses were more likely to be discovered by burying beetles when a chemical attractant (methyl thiocyanate) was placed near a carcass (0.05 and 0.25 m) than when it was placed more distant (1 and 5 m) or for controls (no attractant). The age of the carcass had no effect on discovery. The results suggest that horizontal displacement of a carcass after discovery serves not only to locate a suitable spot for burial but also to reduce information available to rivals searching for the resource.
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After centuries of intense persecution, several large carnivore species in Europe and North America have experienced a rebound. Today's spatial configuration of large carnivore populations has likely arisen from the interplay between their ecological traits and current environmental conditions, but also from their history of persecution and protection. Yet, due to the challenge of studying population-level phenomena, we are rarely able to disentangle and quantify the influence of past and present factors driving the spatial distribution and density of these controversial species. Using spatial capture-recapture models and a data set of 742 genetically identified wolverines Gulo gulo collected over 1/2 million km^2 across their entire range in Norway and Sweden, we identify landscape-level factors explaining the current population density of wolverines in the Scandinavian Peninsula. Distance from the relic range along the Swedish-Norwegian border, where the wolverine population survived a long history of persecution, remains a key determinant of wolverine density today. However, regional differences in management and environmental conditions also played an important role in shaping spatial patterns in present-day wolverine density. Specifically, we found evidence of slower recolonization in areas that had set lower wolverine population goals in terms of the desired number of annual reproductions. Management of transboundary large carnivore populations at biologically relevant scales may be inhibited by administrative fragmentation. Yet, as our study shows, population-level monitoring is an achievable prerequisite for a comprehensive understanding of the distribution and density of large carnivores across an increasingly anthropogenic landscape.
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We report a chromosomal-level genome assembly of a male North American wolverine (Gulo gulo luscus) from the Kugluktuk region of Nunavut, Canada. The genome was assembled directly from long-reads, comprising: 758 contigs with a contig N50 of 36.6 Mb; contig L50 of 20; base count of 2.39 Gb; and a near complete representation (99.98%) of the BUSCO 5.2.2 set of 9,226 genes. A presumptive chromosomal-level assembly was generated by scaffolding against two chromosomal-level Mustelidae reference genomes, the ermine and the Eurasian river otter, to derive a final scaffold N50 of 144.0 Mb and a scaffold L50 of 7. We annotated a comprehensive set of genes that have been associated with models of aggressive behaviour, a trait for which the wolverine is purported to have in the popular literature. To support an integrated, genomics-based wildlife management strategy at a time of environmental disruption from climate change, we also annotated the principal genes of the innate immune system to provide a resource to study the wolverine's susceptibility to new infectious and parasitic diseases. As an illustrative example, we annotated genes involved in the modality of infection by the coronaviruses, an important class of viral pathogens of growing concern as shown by the recent spillover infections by severe acute respiratory syndrome coronavirus-2 to naïve wildlife. Tabulation of heterozygous single nucleotide variants in our specimen revealed a heterozygosity level of 0.065%, indicating a relatively diverse genetic pool that would serve as a baseline for the genomics-based conservation of the wolverine, a rare cold-adapted carnivore now under threat.
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Caching of animal remains is common among carnivorous species of all sizes, yet the effects of caching on larger prey are unstudied. We conducted a summer field experiment designed to test the effects of simulated mountain lion (Puma concolor) caching on mass loss, relative temperature, and odor dissemination of 9 prey-like carcasses. We deployed all but one of the carcasses in pairs, with one of each pair exposed and the other shaded and shallowly buried (cached). Caching substantially reduced wastage during dry and hot (drought) but not wet and cool (monsoon) periods, and it also reduced temperature and discernable odor to some degree during both seasons. These results are consistent with the hypotheses that caching serves to both reduce competition from arthropods and microbes and reduce odds of detection by larger vertebrates such as bears (Ursus spp.), wolves (Canis lupus), or other lions.
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Background Human food subsidies can provide predictable food sources in large quantities for wildlife species worldwide. In the boreal forest of Fennoscandia, gut piles from moose (Alces alces) harvest provide a potentially important food source for a range of opportunistically scavenging predators. Increased populations of predators can negatively affect threatened or important game species. As a response to this, restrictions on field dressing of moose are under consideration in parts of Norway. However, there is a lack of research to how this resource is utilized. In this study, we used camera-trap data from 50 gut piles during 1043 monitoring days. We estimated depletion of gut piles separately for parts with high and low energy content, and used these results to scale up gut pile density in the study area. We identified scavenger species and analyzed the influences of gut pile quality and density on scavenging behavior of mammals and corvids (family Corvidae). Results Main scavengers were corvids and red fox (Vulpes vulpes). Parts with high energy content were rapidly consumed, mainly by corvids that were present at all gut piles shortly after the remains were left at the kill site. Corvid presence declined with days since harvest, reflecting reduction in gut pile quality over time independent of gut pile density. Mammals arrived 7–8 days later at the gut piles than corvids, and their presence depended only on gut pile density with a peak at intermediate densities. The decline at high gut pile densities suggest a saturation effect, which could explain accumulation of gut pile parts with low energy content. Conclusions This study shows that remains from moose harvest can potentially be an important food resource for scavengers, as it was utilized to a high degree by many species. This study gives novel insight into how energy content and density of resources affect scavenging patterns among functional groups of scavengers.
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The relationship of wolverines (Gulo gulo) to persistent spring snow (PSS) may be obligate at the den-site scale but this relationship has yet to be examined at this scale. Our objective was to detect snow at the den-site scale in late May using low-altitude aerial photography in wolverine denning habitat both in the Rocky Mountains of western United States and northwestern Alaska, USA. In the Rocky Mountains, we detected snow on 31 May 2016 in low to heavy categories in 82% of 40 transect segments flown through home ranges of 4 reproductive female wolverines that had denned in Idaho and Montana, USA, prior to our study. In the Alaska study area, we detected snow on 29 May 2016 at 4 den sites of reproductive female wolverines that denned in 2016. By then, snow remained only in occasional, widely scattered patches. Remnant snowdrifts remained at all 4 den sites. High-latitude tundra habitats in Alaska may lose PSS sooner than montane habitats at the southern extent of wolverine distribution. To manage wolverines and their habitat and incorporate PSS in models of future wolverine habitat, we must understand the relationship of wolverines to snow and measure PSS at an appropriate resolution and scale that is biologically meaningful for the species.
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Seed caching by scatter-hoarding rodents is an important dispersal mechanism for many plant species, and the microhabitat of the caching site influences the quality and effectiveness of this dispersal. Shrub vegetation is a major determinant of microhabitat heterogeneity in the forest understory and influences both rodent activity and foraging behavior, and seed germination and seedling establishment. However, very few studies have investigated how shrubs affect this important mutualistic plant–animal interaction and how this is influenced by seed traits. In this study, we monitored rodent choices of caching microhabitat for 3564 artificial seeds that varied in size, nutrient content, and tannin content. By analyzing 1333 primary caches and 209 secondary caches, we showed that rodents selected different caching microhabitats for seeds with different traits. Larger and more nutritious seeds were cached in shrubs more frequently than in the open, while tannin content had no effects on the probability of seeds being cached in shrubs. Furthermore, shrub cover significantly increased the distance which seeds were transported by rodents. If these caching differences apply to natural seeds and persist through seedling establishment and subsequent growth, they could play an important role in the spatial pattern of forest regeneration.
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Food caching is a behavioural strategy used by a wide range of animals to store food for future use. When food is stored, it is susceptible to environmental conditions that can lead to spoilage via microbial proliferation or physical and chemical processes. Given that the nutrition gained from consuming cached food will almost always be less than consuming it immediately upon capture, the degree of degradation will play a central role in determining the ecological threshold at which caching is no longer profitable. Our framework proposes that the degree of susceptibility among caching species is based primarily on the duration of storage, and the perishability of stored food. We first summarize the degree of susceptibility of 203 vertebrate caching species. Thirty-eight percent (38%) of these species are long-term cachers (>10 days) but only 2% are both long-term cachers and store highly perishable food. We then integrate insights from the fields of applied food science and plant biology to outline potential mechanisms by which climate change may influence food-caching species. Four climatic factors (temperature, number of freeze-thaw events, deep-freeze events and humidity) have been shown to affect the degradation of food consumed by humans and are also expected to influence the quality of perishable food cached in the wild. Temperature and moisture are likely important factors influencing seemingly nonperishable seeds. Although we are able to provide broad classifications for caching species at risk of climate change, an improved understanding of how environmental conditions affect the quality and persistence of cached food may allow us to better predict the impact of changing climatic conditions on the fitness of food-caching animals.
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The interaction between predators and their prey is a key factor driving population dynamics and shaping wildlife communities. Most predators will scavenge in addition to killing their own prey, which alters predation effects and implies that one cannot treat these as independent processes. However, the relative importance of predation vs. scavenging and the mechanisms driving variation of such are relatively unstudied in ecological research on predator–prey relationships. Foraging decisions in facultative predators are likely to respond to environmental conditions (e.g., seasonality) and inter- or intraspecific interactions (e.g., prey availability, presence of top predators, scavenging competition). Using data on 41 GPS-collared wolverines (Gulo gulo) during 2401 monitoring days, in four study sites in Scandinavia, we studied variation in diet and feeding strategies (predation vs. scavenging), along a gradient of environmental productivity, seasonality, density, and body mass of their main prey, semidomestic reindeer (Rangifer tarandus). The most important factor affecting the relative extent of predation and scavenging was mean prey body mass. Predation was more pronounced in summer, when vulnerable reindeer calves are abundant, and individual kill rates were negatively related to local reindeer body mass. This relationship was absent in winter. The probability of scavenging was higher in winter and increased with decreasing local reindeer body mass, likely as a response to increased carrion supply. Wolverine feeding strategy was further influenced by predictable anthropogenic food resources (e.g., slaughter remains from hunted ungulates) and the presence of a top predator, Eurasian lynx (Lynx lynx), which provided a continuous carrion supply promoting scavenging. Our results suggest that wolverine feeding strategies are flexible and strongly influenced by seasonally dependent responses to prey body condition in combination with carrion supply. This study demonstrates that large-scale environmental variation can result in contrasting predator feeding strategies, strongly affecting trophic interactions and potentially shaping the dynamics of ecological communities.
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Wolverines (Gulo gulo) in the contiguous United States have been considered for protection under the Endangered Species Act, most recently based on the value of deep snow for the duration of the wolverine's denning season. We examined evidence for an obligate relationship between wolverines and spring snow cover using camera traps and long-term fur harvests in Alberta. The proportion of traplines that harvested ≥1 wolverine was highest in the northwest Boreal Forest (0.3), where mean wolverine harvest density increased by 75% from the 1990s to 2000s. There was no difference in percent spring snow cover on traplines with a female (n = 81) or no female (n = 416) wolverine harvest in the Boreal Forest. Further, all female wolverines (n = 8) positively identified from camera traps in the Boreal Forest, including 5 lactating females, were located within townships predicted to have no spring snow cover. Long-term harvests and evidence of reproduction in areas with low amounts of spring snow cover in the Boreal Forest of northern Alberta suggest that wolverines may be more flexible in their distribution than previously assumed.
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Efficient conservation of wide-ranging carnivores requires that adaptive management consider the varying ecological and societal conditions within the entire range of a population. In northern Europe, large carnivore management has to balance carnivore conservation and maintaining the indigenous reindeer-herding culture. Wolverine Gulo gulo monitoring and management in Sweden is currently focused on alpine reindeer husbandry areas where wolverine abundance and associated depredation conflicts have been highest. However, this focus ignores a potential southwards population expansion because current monitoring relies on snow-based tracking methods that are not applicable outside northern alpine areas. Thus, in this study we: (1) used available monitoring data from 1996 to 2014 in Sweden to assess wolverine distribution trends in relation to national management goals, and (2) evaluate the current monitoring protocol against the use of camera stations as an alternative, snow-independent, method for detecting wolverine presence at the southern periphery of its distribution. We show that the wolverine population in Sweden has expanded considerably into the boreal forest landscape, and colonized areas without reindeer husbandry and persistent spring snow cover. The latter indicates a less strict relationship between wolverine distribution and snow cover than previously hypothesized. Current management continues to use a monitoring protocol that is only adapted to high-conflict alpine areas, and is not adapting to changing conditions in the population range, which creates a problematic scale mismatch. Consequently, national management decisions are currently based on incomplete population information, as roughly a third of wolverine's range is not included in official population estimates, which could have detrimental consequences for conflict mitigation and conservation efforts. This illustrates that an important key to successful carnivore conservation is flexible management that considers the entire range of conditions at the appropriate regional and temporal scales under which carnivores, environment and people interact.