Spatio–temporal hotspots of satellite–tracked arctic foxes reveal a large detection range in a mammalian predator

(a) Attraction to hotspots and detection range

Satellite–tracked arctic foxes converged at specific areas on the sea ice of the Canadian
Arctic. Individuals joining a hotspot usually left their inland home range to do so,
and traveled back to it when they left the hotspot. These foxes remained mainly inland
during winter (80 % of the time), with some foxes present at identified hotspots
during a relatively high proportion of the days they spent on the sea ice. In addition
to the use of the sea ice by foxes being relatively low and often associated with
visits to hotspots, four individuals left their inland home range for the first time
of the winter to go to a hotspot. These results may indicate that foxes did not forage
on the sea ice routinely during that winter, but rather used this habitat opportunistically,
when the availability of carrion was detected, possibly from the home range. On these
occasions, foxes traveled long distances to reach sea ice hotspots, often more than
10 km and up to 40 km. Altogether, the above suggests that foxes may be attracted
to carrion from a relatively long distance. Note that although some fox trips on the
sea ice appeared unrelated to any hotspot, not all foxes were collared in the area,
and these trips could thus have led to undetected hotspots.

The dark and cold conditions prevailing during the study prevented us from sampling
food sources on the sea ice, yet we can assume that food of marine origin was present.
In addition, since all hotspots were detected from December–February, before seal
pups were born, this food must have been carrion. Whereas all species of arctic whales
leave the area before winter 47], ringed seals remain abundant all year round. They are fed upon by polar bears, which
sometimes act as surplus killers in addition to often eating seals only partially
48]–50]. Hunters from Pond Inlet, the closest Inuit community, also hunt seals, but they
usually do not leave remains on the ice (C.–A. Gagnon, personal communication). A
likely, testable hypothesis is therefore that hotspots occurred around ringed seal
carrion left by polar bears. The size (several km
²
) of hotspots may be explained by a combination of 1– polar bears leaving clusters
of carcasses rather than single carcasses, 2– foxes moving in the vicinity of carcasses
between meals, and 3– Argos location error.

An alternative, non–mutually exclusive hypothesis may explain the specific case of
Hotspot–3 (Fig. 2c). A few days before this hotspot was formed, Pond Inlet hunters transported by sledge,
some bowhead whale meat that had been retrieved from a cache set up the previous summer;
some meat may have been inadvertently lost on the ice (A. Maher, Parks Canada agency,
personal communication).

(b) Mechanisms involved in long–range food detection

The concurrent visit of the same areas by several individuals may indicate that they
are guided by the same cues. Mammalian scavengers rely mostly on olfaction to find
carcasses 18], 20], thus a logical hypothesis is that arctic foxes used long–range olfactory detection
to detect carrion on the sea ice. The good olfactory capability of arctic foxes is
well known as they can detect frozen lemmings under 46–77 cm of packed snow 27] or a subnivean seal lair (the excavated snow cavity made by a seal above a breathing
hole) through snow depths of over 150 cm 28]. Our study may provide, however, the first estimates of long–range food detection
for this species. It is noteworthy that marine mammal carcasses are very smelly and
scent sources are rare on the sea ice, so that any new carrion may be readily detected.
In addition, prevailing winter winds in Pond Inlet, located 60 km from our study area,
are from the south and southwest 51], and could thus carry scents from the sea ice to fox territories (Fig. 1). On the other hand, the cold winter temperatures might hamper the generation and
propagation of odors.

Among other arctic mammals, polar bears are notorious for their excellent sense of
smell 49], 52]. Their scent detection distances vary from 2 to 3 km for a seal to 16 km for a large
carcass 53] and even 60 km according to a popular publication 54], although the evidence is unclear in this last case. Unfortunately, olfaction–based
detection distances have rarely been studied experimentally in mammals, and the few
distances obtained through experiments 55], 56] are well below those reported here. Interestingly, however, observers following scent
detection dogs (Canis familiaris) tracking seal lair or excavation 28], 57] or whale scats at sea 13] reported scent detection distances of up to 2–3 km. Some telemetry studies report
higher distances, but with some caveats. For example, cattle carcass pits attracted
resident and transient coyotes (Canis latrans) from 12.2 km and 20.5 km, respectively 58], but it is unclear whether coyotes detected carcasses remotely or were just revisiting
productive sites. To our knowledge, the only strong evidence for a detection distance
approaching estimates provided by our study is that of Nevitt et al.16] who found through GPS tracking that the wandering albatross (Diomedea exulans) is capable of olfactory detection from over 20 km.

Other foraging tactics could be involved, such as the following of cues left by polar
bears in the same way coyotes, ravens and red foxes (Vulpes vulpes) track wolf trails in the snow to find their kills 59]–62], conspecific cueing mediated through chemical communication such as scent marks or
scent trails as suggested for black bear (Ursus americanus) 63], coarse–level local enhancement 64] or inter–guild social information 65]. Until the nature of the items attracting foxes is clearly identified, some uncertainty
remains about the method of detection and the exact activities of foxes on the sea
ice, thus requiring further investigation. Moreover, some fox trips to the sea ice
appeared unrelated to any hotspot. Foxes may thus also move onto the sea ice without
a priori knowledge of food location. All of these hypotheses regarding long–range detection
need testing and the arctic fox study system could offer productive avenues for experimental
research, especially in late winter when light and temperature constraints are released
in the Arctic. In particular, the experimental use of seal carcasses, coupled with
Argos telemetry and camera traps 66], could yield new evidence. The use of tracking devices with finer spatial and temporal
resolutions than Argos, such as GPS, would also allow a more precise estimation of
detection distances, through e.g. detailed analysis of movement paths 16].

(c) Behavioral and ecological implications of long–distance detection range

Because of the patchiness and unpredictability of marine resources, foraging on the
sea ice is usually considered to be more risky for foxes than foraging on land 25], 67]. Our finding that marine resources may be detected from within the fox territories
may challenge this view, at least when local conditions (distance of territories from
the coast, presence of seal carcasses on the sea ice, direction of prevailing winds)
make our results transferable. The large detection range of foxes may allow them to
adopt a dual habitat selection strategy; they defend the inland territory that is
essential for breeding and summer feeding, while occasionally traveling on the sea
ice to feed upon marine resources when detected. Foxes closer to a hotspot were not
more likely to move out of their ranges to feed on the sea ice than foxes located
further away, indicating that some foxes may choose to remain on the land even if
carrion is available. Foraging on the sea ice may indeed present other constraints,
such as the competition with conspecifics at the carcass, the risks of interacting
with a dominant species such as the polar bear, or simply the energetic costs of traveling.
In addition, the prolonged absence of a territory holder may increase the risk of
intruders settling in the territory, as seen in birds 68], 69]. In red foxes, territory takeover can occur from 3 to 8 days after the death of its
owner 70]–72]. The attachment to the home range of arctic foxes was also highlighted by the fact
that individuals joining successive hotspots returned to their inland home ranges
in between, instead of remaining on the sea ice. The distance of foxes to the coast
also did not influence the probability to join a hotspot, showing that foxes with
home ranges not located directly on the coast are also able to detect carrion. Hotspots
lasted about 1–2 weeks. Foxes coming from further away from the hotspot did not stay
longer than the ones from a closer range, but the last foxes arriving spent less time
there than did the first ones arriving, indicating that while the resource found may
offset the costs of travel, it was depleted relatively rapidly. Additional knowledge
on the nature and availability of winter carcasses in the study area, as well as on
potential scavenger competitors, is needed to untangle the costs and benefits of alternative
winter foraging strategies.

In general, the lack of information on resource detection abilities could lead to
erroneous conclusions in animal movement research. For example, a straight–line movement
of an animal towards a resource can result either from goal–oriented navigation based
on a cognitive map or from a discovery made using long–range detection. Distinguishing
between these alternatives requires measuring detection distances for specific resources
7]. Our results also suggest that detection ranges may be underestimated for some mammalian
scavengers, with implications regarding the appropriate spatial scale at which study
results should be interpreted. Furthermore, a better knowledge of the detection ranges
of various scavenger species would help to understand the sequence of exploitation
of carrion by different competitor species, and hence the potential effect of such
resource pulses on community ecology. Finally, fox hotspots also represent locations
where many individuals are close to each other, thereby increasing the risks of transmission
of diseases such as rabies 73]. Rabies is a contact disease whose epidemiology with arctic foxes is still largely
unknown 74]. Knowing from how far away foxes in a population can be coming into contact can help
in modeling the spatial spread of epidemic outbreaks.