DISCUSSION
In this study, we assessed how the combined influences of top-down and
bottom-up factors affected the interactions among mesocarnivores in
Norway in two different seasons. In general, bottom-up factors were
stronger predictors of dominant mesocarnivores’ encounter rates (red fox
and badger) than top-down factors. Contrary to what we expected, large
carnivores apparently had a positive effect on mesocarnivores, with a
positive association between lynx and badger and between wolf and red
fox in summer (although weak for the last pair). Previous studies also
found positive effects of large predators on mesopredators. For
instance, Sivy et al. (2017) found a local-scale positive association
between wolves and non-apex predators in Canada, which they attributed
to carrion facilitation. In Sweden, Wikenros et al. (2017) found a
positive effect of lynx on red foxes, which contrasted with previous
studies (Pasanen-Mortensen et al., 2013, Pasanen-Mortensen and Elmhagen,
2015). They suggested that this might be caused by a behavioral response
of foxes to lynx abundance, where foxes would be using olfatory cues
from lynx to increase their possibility to access carrion from prey
killed by lynx. Carcasses left by apex predators are known to be an
important food supply for smaller predators (Wikenros et al., 2014,
Selva et al., 2005, Prugh and Sivy, 2020). These remains can be an
important food source during winter, when other food sources are scarce
(Carricondo-Sánchez et al., 2016, Helldin and Danielsson, 2007, Needham
et al., 2014, Willebrand et al., 2017), or during spring, when animals
are usually reproducing (Wikenros et al., 2014). The slight positive
effect of wolf on red foxes in summer (which also includes spring months
April and May in our analysis) could be related to food provisioning
during reproduction time. Regarding the association between lynx and
badgers, their positive relationship in summer could be related to their
preference for productive environments during that season (Figure 3).
There are also no reports of aggressive interactions between these two
carnivores (Neal and Chesseman 1996, as cited in Fedriani et al., 1999),
and there are several studies documenting a predisposition of badgers to
coexist with other apex predators (Fedriani et al., 1999, Garrote and
Perez de ayala, 2019, Palomares et al., 1996).
Both red fox and badger were stronger predictors of pine marten
encounter rates than land cover variables in winter. Indeed, the three
mesocarnivores (red fox, badger and pine marten), showed positive
associations among each other, which were stronger in winter. Food
scarcity and challenging winter conditions may force species to use the
same resources and areas. Previous studies have found positive
associations among competing predators during times of food scarcity in
Scandinavia. For instance, Cano-Martínez et al. (2021) found a positive
association between red fox, pine marten and weasels (Mustela
nivalis ) during periods of low rodent abundance. Similarly, Stoessel et
al. (2018) found a positive association between arctic fox (Vulpes
lagopus ) and red fox during the low rodent phase. However, there is
evidence that red foxes kill pine martens (Lindström et al., 1995),
which is probably one of the reasons why pine martens avoid open areas
(Storch et al., 1990). Pine martens are often described as being more
habitat specialists in Scandinavia as compared to other mesocarnivores.
Also, pine martens are primarily associated with spruce-dominated
forests with large trees at fine spatial scales (Brainerd and Rolstad,
2002), which enables them to avoid predation by climbing trees (Storch
et al., 1990). However, at the lanscape scale, pine martens seem to be
able to live in a mixed landscape of old forest and other habitat types
in Noway (Angoh et al., 2023), sharing that landscape with other
mesopredators. Pine martens might use small-scale spatiotemporal
mechanisms, i.e. avoiding sites only when there is a high risk of
encountering a potential enemy, in order to minimize interactions with
larger predators and facilitate coexistence (Zalewska et al., 2021).
Furthermore, the density of both red fox and pine marten seems to be
correlated in Finland, which indicates that the possible effects of
interspecific competition do not determine the spatial abundance of pine
martens at either a regional or a landscape level (Kurki et al., 1998).
This is in opposition to an increase in pine marten density reported by
Storch et al. (1990) following a decrease in red fox density during an
epizootic of sarcoptic mange (Sarcoptes scabiei ) in Sweden.
Regarding the positive association between badgers and red foxes,
Macdonald et al. (2004) recorded a series of non-aggressive interactions
between the two mesocarnivores where foxes seemed to seek the company of
badgers at setts. They argued for the possibility that foxes might
receive interspecific information from badgers, for example to find good
feedings spots. Also, red foxes and badgers are known to share
setts/dens (Macdonald 1987 as cited in Macdonald et al., 2004), which
indicates some kind of facilitative relationship. Positive associations
between competing species may be faciliated by landscape heterogeneity
and by mechanisms of niche separation such as temporal partitioning
(Bischof et al., 2014, Lesmeister et al., 2015, Viota, 2012). Badgers
are considered strictly nocturnal, while red foxes and pine martens are
considered facultative nocturnal, since they are more flexible in their
use of time (Torretta et al., 2016, Monterroso et al., 2014, Zalewska et
al., 2021).
Based on our predictions, we expected environmental productivity to have
a stronger positive effect on carnivore encounter rates in winter
because of food scarcity (Elmhagen and Rushton, 2007). However, we found
a positive association between EVI and some of the carnivores (lynx, red
fox and badger) only in summer. Nevertheless, even if the seasonal
effect of productivity was not as expected, mesocarnivores in Norway
seem to be more influenced by bottom-up rather than by top-down
mechanisms, as the effect of large carnivores was weak compared to the
effect of land cover. Wikenros et al. (2017) also found that bottom-up
processes were more influential on red fox abundance in Sweden than the
top-down effect of lynx and wolves, although they emphasized the
importance of considering spatial scale. Large carnivores in Norway may
occur at too low densities to have an effect on the encounter rates of
mesocarnivores at a large scale. The Scandinavian wolf population
declined strongly during the 19th century and was
declared functionally extinct in 1966 (Wabakken et al., 2001). The
population started to recover in the early 1980s in south-central
Scandinavia and it has increased in number and geographical distribution
since then (Wabakken et al., 2001). However, of the 540 (95% CI =
427-702) individuals estimated during the winter 2021/2022 in
Scandinavia, only 88-91 were counted in Norway (Wabakken, 2022).
Furthermore, the “wolf zone” only represents 5% of the national
territory and is limited to southeastern Norway, and outside this area,
wolves are excluded via culling. Lynx numbers are also actively managed
through quota regulated hunting to limit their population densiy and
constrict their distribution (Linnell et al., 2010). A reduced predator
population exposed to hunting may not be able to play its full
ecological role, limiting both direct and indirect effects on other
predators and prey (Ordiz et al., 2013). In this kind of system, it is
predicted that bottom-up influence will be stronger than top-down
control of mesocarnivores (Pasanen-Mortensen and Elmhagen, 2015). This
implies that the abundance of smaller carnivores would be dependent on
prey availability, which ultimately is related to bioclimatic factors
such as environmental productivity and land use (Pasanen-Mortensen and
Elmhagen, 2015).
The proportion of agricultural land also had an important effect on all
carnivores, except for red foxes. Actually, agricultural fields in
Norway have been found to sustain the lowest abundance of small mammals
(Panzacchi et al., 2010), which would explain the lack of effect of this
type of landscape on red fox encounter rates. On the other hand, the
negative effect of agricultural land found on lynx, wolf and pine marten
was expected given that these are predominantly forest species. This
negative effect of agriculture was weaker in winter. Agricultural fields
vary in usage level by humans over the year, with high activity during
late spring and summer, and less activity occurring during autumn and
winter (Bunnefeld et al., 2006). This might explain the observed
seasonal variation and the strong negative effect of agriculture fields
in summer for lynx and wolf. Furthermore, this seasonal variation could
also be related to seasonal movements of prey. Moose (Alces
alces ) and roe deer (Capreolus capreolus ) migrate to areas of
lower elevation during winter, in search of higher food availability
provided by lower snow depth and artificial feeding sites (Bunnefeld et
al., 2006, Singh et al., 2012, Mysterud, 1999). The migration of moose
and roe deer to areas of lower elevation during winter could relax the
negative effect of fields on lynx and wolf in winter.
Regarding the effect of human disturbance, humans were positively
associated with the two dominant mesocarnivores (red fox and badger) in
summer. Previous studies have documented positive relationships between
red fox abundance and human settlements (e.g., Jahren et al., 2020,
Panek and Bresiński, 2002), although they tend to avoid highly urbanized
areas (Červinka et al., 2014). Human population density has been
suggested to be a good proxy for anthropogenic food subsidies (Oro et
al., 2013), which are used by red foxes and badgers (Rosalino et al.,
2010, Gomes et al., 2019). Manlick and Pauli (2020) found strong dietary
responses by a large variety of generalist carnivores to human
disturbance, suggesting substantial use of human subsidies. These human
resources can potentially increase dietary overlap (Sévêque et al.,
2020), which may increase the probability of interspecific competition
and intraguild predation in human-dominated landscapes (Manlick and
Pauli, 2020, Newsome et al., 2015). However, these potential effects
were not strong enough to prevent both red foxes and badgers from being
positively associated with these areas. Pine marten, on the other hand,
showed a tendency to avoid areas of high human disturbance mostly in
winter. This negative association between humans and pine marten is in
line with previous studies (e.g. Fusillo et al., 2009, Goszczyński et
al., 2007), suggesting that pine marten is sensitive to human
disturbance.
Human disturbance had a negative effect on both large carnivore species,
but stronger on wolf in both seasons. Wolves in Norway are strongly
managed and restricted to the so-called “wolf zone”, which is located
in an area with low human population density. Wolf distribution is
therefore strongly influenced by politics and management restrictions.
Furthermore, lynx populations in Norway are heavily managed, and
human-caused sources of mortality such as hunting, poaching and vehicle
collisions are high (Andrén et al., 2006). All those factors may explain
the observed negative effect of humans on both wolves and lynx in our
study. Yet, it seems that both species are less negatively influenced by
humans in winter, which could be related to prey seasonal movements, as
explained above. Additionally, high roe deer densities often occur in
agricultural, fragmented and disturbed areas (Basille et al., 2009),
which are generally associated with higher human densities. Thus, wolves
and lynx distribution may be determined by a trade-off between the
availability of food and the risk of human presence. A higher
availability of main prey closer to more populated areas in winter, when
alternative prey is difficult to find, could be attracting both lynx
(Bunnefeld et al., 2006, Basille et al., 2009) and wolves to these areas
(Carricondo-Sanchez et al., 2020), thus reducing the negative effect of
humans. Furthermore, local-scale avoidance and temporal adjustments in
habitat use might facilitate large predators sharing the landscape with
humans (Thorsen et al., 2022).
It is important to highlight the potential weakness of the use of
by-catch data from camera traps from a study designed to target a single
species to study multiple species and their interactions (Hofmeester et
al., 2019). However, Hofmeester et al. (2021) showed high detection
probability of multiple carnivore species at lynx-targeted camera traps
in boreal ecosystems, including high detectability of wolf, red fox and
badger. Furthermore, all the camera traps used in this study were
deployed with the same sampling design. Therefore, we argue that
comparing trapping rates of different species from camera traps within
this study design should not result in biased estimates of species
interactions.