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.