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.