INTRODUCTION
The study of interspecific interactions among mammalian carnivores is
fundamental to conservation biology (Linnell and Strand, 2000), but the
factors influencing these interactions can be complex and difficult to
disentangle. Interactions among coexisting species can potentially have
large consequences for community structure by influencing the
demography, distribution, and behavior of the species within the
community (de Satge et al., 2017, Grassel et al., 2015, St-Pierre et
al., 2006). The potential top-down effect of large carnivores and their
importance in maintaining ecosystem functioning has been widely
recognized (Estes et al., 2011, Ripple et al., 2014, Ritchie and
Johnson, 2009). Declines in the numbers and distribution of large
carnivores due to human persecution and habitat loss in many regions has
led to changes in species interactions and food webs, highlighting their
ecological role in ecosystems worldwide (Ripple et al., 2014). One
commonly proposed outcome following the loss of apex predators is the
increase in the abundance of mesopredators. This phenomenon is known as
“mesopredator release” (Prugh et al., 2009), and it can potentially
have negative impacts on prey species through increased predation from
mesopredators, as well as on other smaller carnivores through intraguild
predation.
Even though negative interspecific interactions among carnivores seem to
be widespread, there is also a growing recognition of the importance of
positive interactions in structuring predator communities (Prugh and
Sivy, 2020). Large carnivores can facilitate mesocarnivores by providing
resource subsidies in the form of carrion (Pereira et al., 2014, Prugh
and Sivy, 2020). Scavenging is a widespread behavior that has clear
implications for food web structure and population dynamics (Mellard et
al., 2021). Carrion subsidies can be important food sources in areas
where several opportunistic mesocarnivores coexist (Sivy et al., 2018),
or when other food sources are scarce (Jedrzejewski and Jedrzejewska,
1992, Killengreen et al., 2011). Interactions between large carnivores
and mesocarnivores can therefore range from facilitation to suppression,
and both may even occur simultaneously (Prugh and Sivy, 2020, Wikenros
et al., 2017). In addition, the direction and strength of these
interactions may be scale dependent (Sivy et al., 2017).
Interactions among predators in human-dominated landscapes can be
different from those occurring in undisturbed habitats. Furthermore,
ecological phenomena such as mesopredator release can be difficult to
separate from land-use changes (Prugh et al., 2009). Mesopredator
numbers tend to increase in human-modified habitats, as a response to
higher resource availability, while apex predators are more likely to
disappear due to direct persecution and habitat loss (Prugh et al.,
2009). Unfortunately, large-scale experimental approaches that might
help disentangle the relative importance of top-down versus bottom-up
effects are rarely logistically possible (Nilsen et al., 2020). However,
modeling approaches based on large-scale observational data can be
useful (Dorresteijn et al., 2015, Elmhagen and Rushton, 2007).
Anthropogenic influence on food webs may operate through diverse
processes and influence multiple trophic levels simultaneously. For
example, humans can decrease predator density directly through hunting,
but they can also trigger behavioral responses at both spatial and
temporal scales (e.g., by changing predators’ habitat use and activity
patterns) (Milner et al., 2007, Ordiz et al., 2012, Ordiz et al., 2021),
potentially causing top-down cascades that may affect species at lower
trophic levels. On the other hand, humans may also influence predators
through bottom-up processes via food subsidization (Gompper and Vanak,
2008, Newsome et al., 2015, Newsome et al., 2014), or by enhancing
forage availability of herbivores, thus increasing prey density (Muhly
et al., 2013). The effect of such food subsidies may be particularly
relevant for systems with low productivity (Melis et al., 2009).
Ecosystem productivity and seasonal change in resource availability can
determine the relative strength and direction of trophic interactions
(Elmhagen and Rushton, 2007, Ritchie and Johnson, 2009, Stoessel et al.,
2018). In particular, Stoessel et al. (2018) found that harsh winter
conditions and food scarcity increased the importance of bottom-up
constraints on species interactions as compared to top-down factors in
an arctic ecosystem. Furthermore, Elmhagen and Rushton (2007) found a
stronger degree of bottom-up rather than top-down control of red foxes
(Vulpes vulpes ) in low productivity ecosystems in Sweden. These
studies highlight the importance of considering both top-down and
bottom-up processes when studying mesopredator interspecific
interactions in ecosystems with strong seasonality. The relevance of
such insights is of special importance in the face of climate change,
which will alter seasonal conditions and species interactions.
Several large carnivore species are now recovering across large parts of
Europe (Chapron et al., 2014), with potential cascading effects through
the entire carnivore community. In Southern Spain for example, the
recovery of the Iberian lynx (Lynx pardinus ) exerted a strong
suppression control of two sympatric mesocarnivores (Burgos et al.,
2023). However, the strength of this top-down effect differed for
different mesocarnivore species, and it was modulated by prey
availability. In Scandinavia, the recovery of Eurasian lynx (Lynx
lynx ) and wolves (Canis lupus ) in human-modified ecosystems is
raising a key question regarding the ecological role that large
carnivores play in these anthropogenic landscapes and their importance
relative to the effects of humans on mesocarnivores (Dorresteijn et al.,
2015, Kuijper et al., 2016). There is some evidence that the recovering
lynx populations in Scandinavia significantly limit mesocarnivore
populations such as red fox in some areas (Elmhagen et al., 2010,
Fedriani et al., 1999, Helldin et al., 2006). This top-down effect has
also been observed at a continental scale in Eurasia (Pasanen-Mortensen
et al., 2013). However, the presence of lynx may also provide a stable
food supply in the form of carrion for red foxes (Helldin and
Danielsson, 2007) and other mesocarnivores, which can be vital during
winter (Needham et al., 2014). Mesocarnivores are also strongly
influenced by anthropogenic food supplies, and red fox and badger
(Meles meles ) densities have been found to be higher, and their
home ranges smaller, in urban and suburban areas compared to
semi-natural habitats (Šálek et al., 2015). An increase in red fox
numbers might in turn have negative effects on smaller carnivore
species, like pine marten (Martes martes ), through intraguild
predation (Lindström et al., 1995).
The aim of this study was to assess how interactions among
mesocarnivores are affected by large carnivores, land cover variables
(proportion of agricultural land and primary productivity), and human
disturbance, as well as how the relative strength of these top-down and
bottom-up mechanisms is influenced by season (summer vs winter). The
interactions among mesocarnivores were assessed using encounter rates
from a national level camera trapping study in Norway. We used three
years of camera trapping data to study a carnivore guild that included
lynx and wolves as apex predators, red foxes and badgers as dominant
mesocarnivores, and pine martens as a subordinate mesocarnivore.