Scavenging patterns of an inbred wolf population in a landscape with a pulse of human-provided carrion.

Scavenging is an important part of food acquisition for many carnivore species that switch between scavenging and predation. In landscapes with anthropogenic impact, humans provide food that scavenging species can utilize. We quantified the magnitude of killing versus scavenging by gray wolves (Canis lupus) in Scandinavia where humans impact the ecosystem through hunter harvest, land use practices, and infrastructure. We investigated the cause of death of different animals utilized by wolves, and examined how the proportion of their consumption time spent scavenging was influenced by season, wolf social affiliation, level of inbreeding, density of moose (Alces alces) as their main prey, density of brown bear (Ursus arctos) as an intraguild competitor, and human density. We used data from 39 GPS-collared wolves covering 3198 study days (2001-2019), including 14,205 feeding locations within space-time clusters, and 1362 carcasses utilized by wolves. Most carcasses were wolf-killed (80.5%) while a small part had died from other natural causes (1.9%). The remaining had either anthropogenic mortality causes (4.7%), or the cause of death was unknown (12.9%). Time spent scavenging was higher during winter than during summer and autumn. Solitary wolves spent more time scavenging than pack-living individuals, likely because individual hunting success is lower than pack success. Scavenging time increased with the mean inbreeding coefficient of the adult wolves, possibly indicating that more inbred individuals resort to scavenging, which requires less body strength. There was weak evidence for competition between wolves and brown bears as well as a positive relationship between human density and time spent scavenging. This study shows how both intrinsic and extrinsic factors drive wolf scavenging behavior, and that despite a high level of inbreeding and access to carrion of anthropogenic origin, wolves mainly utilized their own kills.

Whole-genome resequencing of temporally stratified samples reveals substantial loss of haplotype diversity in the highly inbred Scandinavian wolf population.

Genetic drift can dramatically change allele frequencies in small populations and lead to reduced levels of genetic diversity, including loss of segregating variants. However, there is a shortage of quantitative studies of how genetic diversity changes over time in natural populations, especially on genome-wide scales. Here, we analyzed whole-genome sequences from 76 wolves of a highly inbred Scandinavian population, founded by only one female and two males, sampled over a period of 30 yr. We obtained chromosome-level haplotypes of all three founders and found that 10%-24% of their diploid genomes had become lost after about 20 yr of inbreeding (which approximately corresponds to five generations). Lost haplotypes spanned large genomic regions, as expected from the amount of recombination during this limited time period. Altogether, 160,000 SNP alleles became lost from the population, which may include adaptive variants as well as wild-type alleles masking recessively deleterious alleles. Although not sampled, we could indirectly infer that the two male founders had megabase-sized runs of homozygosity and that all three founders showed significant haplotype sharing, meaning that there were on average only 4.2 unique haplotypes in the six copies of each autosome that the founders brought into the population. This violates the assumption of unrelated founder haplotypes often made in conservation and management of endangered species. Our study provides a novel view of how whole-genome resequencing of temporally stratified samples can be used to visualize and directly quantify the consequences of genetic drift in a small inbred population.

Rewilding by Wolf Recolonisation, Consequences for Ungulate Populations and Game Hunting.

The ongoing recolonisations of human-transformed environments in Europe by large carnivores like the wolf Canis lupus means that conservation conflicts could re-surface, among other reasons, due to predation on ungulate game species. We estimated the effect of wolves on ungulate species using data on wolf prey selection, kill rates and territory size to build a hypothetical case of future expansion. We extrapolated results on predation from the current wolf distribution in central Sweden and eastern Poland to the eventual wolf recolonisation of southern Sweden. We then calculated the proportion of five ungulate game species killed annually by wolves, and the ratio between the predicted annual predation by wolves given future colonization and the number of ungulates currently harvested by hunters. Results showed that wolf recolonization in southern Sweden would have a minor impact on the estimated population densities of red deer Cervus elaphus, fallow deer Dama dama and wild boar Sus scrofa, but is likely to lead to a significant reduction in human captures of moose Alces alces and roe deer Capreolus capreolus. The current five-ungulate species system in southern Sweden suggests a potential for two to four times higher wolf density than the two-ungulate species system in the northern part of their current distribution. Management and conservation of recolonizing large carnivores require a better understanding of the observed impact on game populations under similar ecological conditions to ameliorate conservation conflicts and achieve a paradigm of coexistence. Integrating these predictions into management is paramount to the current rewilding trend occurring in many areas of Europe or North America.

Multiple species-specific molecular markers using nanofluidic array as a tool to detect prey DNA from carnivore scats.

Large carnivore feeding ecology plays a crucial role for management and conservation for predators and their prey. One of the keys to this kind of research is to identify the species composition in the predator diet, for example, prey determination from scat content. DNA-based methods applied to detect prey in predators' scats are viable alternatives to traditional macroscopic approaches, showing an increased reliability and higher prey detection rate. Here, we developed a molecular method for prey species identification in wolf (Canis lupus) scats using multiple species-specific marker loci on the cytochrome b gene for 18 target species. The final panel consisted of 80 assays, with a minimum of four markers per target species, and that amplified specifically when using a high-throughput Nanofluidic array technology (Fluidigm Inc.). As a practical example, we applied the method to identify target prey species DNA in 80 wolf scats collected in Sweden. Depending on the number of amplifying markers required to obtain a positive species call in a scat, the success in determining at least one prey species from the scats ranged from 44% to 92%. Although we highlight the need to evaluate the optimal number of markers for sensitive target species detection, the developed method is a fast and cost-efficient tool for prey identification in wolf scats and it also has the potential to be further developed and applied to other areas and large carnivores as well.

Behavioral effects of wolf presence on moose habitat selection: testing the landscape of fear hypothesis in an anthropogenic landscape.

Landscape of fear refers to the spatial variation in prey perception of predation risk, that under certain conditions, may lead to changes in their behavior. Behavioral responses of prey in relation to large carnivore predation risk have mainly been conducted in areas with low anthropogenic impact. We used long-term data on the distribution of moose in different habitat types in a system characterized by intensive management of all three trophic levels (silviculture, harvest of wolves and moose) to study effects on moose habitat selection resulting from the return of an apex predator, the wolf. We assumed that coursing predators such as wolves will cause an increased risk for moose in some habitat types and tested the hypotheses that moose will avoid open or young forest habitats following wolf establishment. After wolf recolonization, moose reduced their use of one type of open habitat (bog) but there was neither change in the use of the other open habitat type (clear-cut), nor in their use of young forest. Wolf establishment did not influence the use of habitat close to dense habitat when being in open habitats. Thus, the effect of wolves varied among habitat types and there was no unidirectional support for a behavioral effect of wolves' establishment on moose habitat use. Human-driven habitat heterogeneity, concentration of moose forage to certain habitat types, and the effects of a multiple predator guild on moose may all contribute to the results found. We conclude that the landscape of fear is likely to have weak ecological effects on moose in this system.

Impact of a recolonizing, cross-border carnivore population on ungulate harvest in Scandinavia.

Predation from large carnivores and human harvest are the two main mortality factors affecting the dynamics of many ungulate populations. We examined long-term moose (Alces alces) harvest data from two countries that share cross-border populations of wolves (Canis lupus) and their main prey moose. We tested how a spatial gradient of increasing wolf territory density affected moose harvest density and age and sex composition of the harvested animals (n = 549,310), along a latitudinal gradient during 1995-2017. In areas containing average-sized wolf territories, harvest density was on average 37% (Norway) and 51% (Sweden) lower than in areas without wolves. In Sweden, calves made up a higher proportion of the moose harvest than in Norway, and this proportion was reduced with increased wolf territory density, while it increased in Norway. The proportion of females in the adult harvest was more strongly reduced in Sweden than in Norway as a response to increased wolf territory density. Moose management in both countries performed actions aimed to increase productivity in the moose population, in order to compensate for the increased mortality caused by wolves. These management actions are empirical examples of an adaptive management in response to the return of large carnivores.

Wolf habitat selection when sympatric or allopatric with brown bears in Scandinavia.

Habitat selection of animals depends on factors such as food availability, landscape features, and intra- and interspecific interactions. Individuals can show several behavioral responses to reduce competition for habitat, yet the mechanisms that drive them are poorly understood. This is particularly true for large carnivores, whose fine-scale monitoring is logistically complex and expensive. In Scandinavia, the home-range establishment and kill rates of gray wolves (Canis lupus) are affected by the coexistence with brown bears (Ursus arctos). Here, we applied resource selection functions and a multivariate approach to compare wolf habitat selection within home ranges of wolves that were either sympatric or allopatric with bears. Wolves selected for lower altitudes in winter, particularly in the area where bears and wolves are sympatric, where altitude is generally higher than where they are allopatric. Wolves may follow the winter migration of their staple prey, moose (Alces alces), to lower altitudes. Otherwise, we did not find any effect of bear presence on wolf habitat selection, in contrast with our previous studies. Our new results indicate that the manifestation of a specific driver of habitat selection, namely interspecific competition, can vary at different spatial-temporal scales. This is important to understand the structure of ecological communities and the varying mechanisms underlying interspecific interactions.

Testing the influence of habitat experienced during the natal phase on habitat selection later in life in Scandinavian wolves.

Natal habitat preference induction (NHPI) occurs when characteristics of the natal habitat influence the future habitat selection of an animal. However, the influence of NHPI after the dispersal phase has received remarkably little attention. We tested whether exposure to humans in the natal habitat helps understand why some adult wolves Canis lupus may approach human settlements more than other conspecifics, a question of both ecological and management interest. We quantified habitat selection patterns within home ranges using resource selection functions and GPS data from 21 wolf pairs in Scandinavia. We identified the natal territory of each wolf with genetic parental assignment, and we used human-related characteristics within the natal territory to estimate the degree of anthropogenic influence in the early life of each wolf. When the female of the adult wolf pair was born in an area with a high degree of anthropogenic influence, the wolf pair tended to select areas further away from humans, compared to wolf pairs from natal territories with a low degree of anthropogenic influence. Yet the pattern was statistically weak, we suggest that our methodological approach can be useful in other systems to better understand NHPI and to inform management  about human-wildlife interactions.

Data to model risks for recolonizing wolves in Scandinavia through the integration of territory presence and human-driven mortalities.

This dataset article describes the data and sources used to model risks for the recolonizing wolf (Canis lupus) in Sweden and Norway in the article "Integrated spatially-explicit models predict pervasive risks to recolonizing wolves in Scandinavia from human-driven mortality" (Recio et al., 2018). Presences on wolf territories were used to model the potential distribution of the species. Presences of human-driven mortalities including traffic collisions, culling (protective/defensive, and licensed hunting), and illegal killing (i.e. poaching) were used to model predictions on the distribution of these mortalities. Sources for the independent variables used for the models are also described.

Habitat segregation between brown bears and gray wolves in a human-dominated landscape.

Identifying how sympatric species belonging to the same guild coexist is a major question of community ecology and conservation. Habitat segregation between two species might help reduce the effects of interspecific competition and apex predators are of special interest in this context, because their interactions can have consequences for lower trophic levels. However, habitat segregation between sympatric large carnivores has seldom been studied. Based on monitoring of 53 brown bears (Ursus arctos) and seven sympatric adult gray wolves (Canis lupus) equipped with GPS collars in Sweden, we analyzed the degree of interspecific segregation in habitat selection within their home ranges in both late winter and spring, when their diets overlap the most. We used the K-select method, a multivariate approach that relies on the concept of ecological niche, and randomization methods to quantify habitat segregation between bears and wolves. Habitat segregation between bears and wolves was greater than expected by chance. Wolves tended to select for moose occurrence, young forests, and rugged terrain more than bears, which likely reflects the different requirements of an omnivore (bear) and an obligate carnivore (wolf). However, both species generally avoided human-related habitats during daytime. Disentangling the mechanisms that can drive interspecific interactions at different spatial scales is essential for understanding how sympatric large carnivores occur and coexist in human-dominated landscapes, and how coexistence may affect lower trophic levels. The individual variation in habitat selection detected in our study may be a relevant mechanism to overcome intraguild competition and facilitate coexistence.

Genomic consequences of intensive inbreeding in an isolated wolf population.

Inbreeding (mating between relatives) is a major concern for conservation as it decreases individual fitness and can increase the risk of population extinction. We used whole-genome resequencing of 97 grey wolves (Canis lupus) from the highly inbred Scandinavian wolf population to identify 'identical-by-descent' (IBD) chromosome segments as runs of homozygosity (ROH). This gave the high resolution required to precisely measure realized inbreeding as the IBD fraction of the genome in ROH (F ROH). We found a striking pattern of complete or near-complete homozygosity of entire chromosomes in many individuals. The majority of individual inbreeding was due to long IBD segments (>5 cM) originating from ancestors ≤10 generations ago, with 10 genomic regions showing very few ROH and forming candidate regions for containing loci contributing strongly to inbreeding depression. Inbreeding estimated with an extensive pedigree (F P) was strongly correlated with realized inbreeding measured with the entire genome (r 2 = 0.86). However, inbreeding measured with the whole genome was more strongly correlated with multi-locus heterozygosity estimated with as few as 500 single nucleotide polymorphisms, and with F ROH estimated with as few as 10,000 single nucleotide polymorphisms, than with F P. These results document in fine detail the genomic consequences of intensive inbreeding in a population of conservation concern.

No place like home? A test of the natal habitat-biased dispersal hypothesis in Scandinavian wolves.

Natal dispersal is an important mechanism for the viability of populations. The influence of local conditions or experience gained in the natal habitat could improve fitness if dispersing individuals settle in an area with similar habitat characteristics. This process, defined as 'natal habitat-biased dispersal' (NHBD), has been used to explain distribution patterns in large carnivores, but actual studies evaluating it are rare. We tested whether grey wolf Canis lupus territory establishment was influenced by the habitat characteristics of the natal territory using the long-term monitoring of the Scandinavian wolf population. We paired the locations of natal and established territories, accounted for available habitats along the dispersing route, and compared their habitat characteristics for 271 wolves during 1998-2012. Wolves with the shortest dispersal distances established in natal-like habitat types more than expected by chance, whereas wolves that dispersed longer distances did not show NHBD. The pattern was consistent for male and female wolves, with females showing more NHBD than males. Chances to detect NHBD increased with the size of habitat defined as available. This highlights the importance of considering the biological characteristics of the studied species when defining habitat availability. Our methodological approach can prove useful to inform conservation and management to identify habitats to be selected by reintroduced or naturally expanding populations.

Fear or food - abundance of red fox in relation to occurrence of lynx and wolf.

Apex predators may affect mesopredators through intraguild predation and/or supply of carrion from their prey, causing a trade-off between avoidance and attractiveness. We used wildlife triangle snow-tracking data to investigate the abundance of red fox (Vulpes vulpes) in relation to lynx (Lynx lynx) and wolf (Canis lupus) occurrence as well as land composition and vole (Microtus spp.) density. Data from the Swedish wolf-monitoring system and VHF/GPS-collared wolves were used to study the effect of wolf pack size and time since wolf territory establishment on fox abundance. Bottom-up processes were more influential than top-down effects as the proportion of arable land was the key indicator of fox abundance at the landscape level. At this spatial scale, there was no effect of wolf abundance on fox abundance, whereas lynx abundance had a positive effect. In contrast, at the wolf territory level there was a negative effect of wolves on fox abundance when including detailed information of pack size and time since territory establishment, whereas there was no effect of lynx abundance. This study shows that different apex predator species may affect mesopredator abundance in different ways and that the results may be dependent on the spatiotemporal scale and resolution of the data.

Competition between apex predators? Brown bears decrease wolf kill rate on two continents.

Trophic interactions are a fundamental topic in ecology, but we know little about how competition between apex predators affects predation, the mechanism driving top-down forcing in ecosystems. We used long-term datasets from Scandinavia (Europe) and Yellowstone National Park (North America) to evaluate how grey wolf (Canis lupus) kill rate was affected by a sympatric apex predator, the brown bear (Ursus arctos). We used kill interval (i.e. the number of days between consecutive ungulate kills) as a proxy of kill rate. Although brown bears can monopolize wolf kills, we found no support in either study system for the common assumption that they cause wolves to kill more often. On the contrary, our results showed the opposite effect. In Scandinavia, wolf packs sympatric with brown bears killed less often than allopatric packs during both spring (after bear den emergence) and summer. Similarly, the presence of bears at wolf-killed ungulates was associated with wolves killing less often during summer in Yellowstone. The consistency in results between the two systems suggests that brown bear presence actually reduces wolf kill rate. Our results suggest that the influence of predation on lower trophic levels may depend on the composition of predator communities.

Group or ungroup - moose behavioural response to recolonization of wolves.

BACKGROUND: Predation risk is a primary motivator for prey to congregate in larger groups. A large group can be beneficial to detect predators, share predation risk among individuals and cause confusion for an attacking predator. However, forming large groups also has disadvantages like higher detection and attack rates of predators or interspecific competition. With the current recolonization of wolves (Canis lupus) in Scandinavia, we studied whether moose (Alces alces) respond by changing grouping behaviour as an anti-predatory strategy and that this change should be related to the duration of wolf presence within the local moose population. In particular, as females with calves are most vulnerable to predation risk, they should be more likely to alter behaviour. METHODS: To study grouping behaviour, we used aerial observations of moose (n = 1335, where each observation included one or several moose) inside and outside wolf territories. RESULTS: Moose mostly stayed solitary or in small groups (82% of the observations consisted of less than three adult moose), and this behavior was independent of wolf presence. The results did not provide unequivocal support for our main hypothesis of an overall change in grouping behaviour in the moose population in response to wolf presence. Other variables such as moose density, snow depth and adult sex ratio of the group were overall more influential on grouping behaviour. However, the results showed a sex specific difference in social grouping in relation to wolf presence where males tended to form larger groups inside as compared to outside wolf territories. For male moose, population- and environmentally related variables were also important for the pattern of grouping. CONCLUSIONS: The results did not give support for that wolf recolonization has resulted in an overall change in moose grouping behaviour. If indeed wolf-induced effects do exist, they may be difficult to discern because the effects from moose population and environmental factors may be stronger than any change in anti-predator behaviour. Our results thereby suggest that caution should be taken as to generalize about the effects of returning predators on the grouping behaviour of their prey.

Let's stay together? Intrinsic and extrinsic factors involved in pair bond dissolution in a recolonizing wolf population.

For socially monogamous species, breeder bond dissolution has important consequences for population dynamics, but the extent to which extrinsic or intrinsic population factors causes pair dissolution remain poorly understood, especially among carnivores. Using an extensive life-history data set, a survival analysis and competing risks framework, we examined the fate of 153 different wolf (Canis lupus) pairs in the recolonizing Scandinavian wolf population, during 14 winters of snow tracking and DNA monitoring. Wolf pair dissolution was generally linked to a mortality event and was strongly affected by extrinsic (i.e. anthropogenic) causes. No divorce was observed, and among the pair dissolution where causes have been identified, death of one or both wolves was always involved. Median time from pair formation to pair dissolution was three consecutive winters (i.e. approximately 2 years). Pair dissolution was mostly human-related, primarily caused by legal control actions (36·7%), verified poaching (9·2%) and traffic-related causes (2·1%). Intrinsic factors, such as disease and age, accounted for only 7·7% of pair dissolutions. The remaining 44·3% of dissolution events were from unknown causes, but we argue that a large portion could be explained by an additional source of human-caused mortality, cryptic poaching. Extrinsic population factors, such as variables describing the geographical location of the pair, had a stronger effect on risk of pair dissolution compared to anthropogenic landscape characteristics. Population intrinsic factors, such as the inbreeding coefficient of the male pair member, had a negative effect on pair bond duration. The mechanism behind this result remains unknown, but might be explained by lower survival of inbred males or more complex inbreeding effects mediated by behaviour. Our study provides quantitative estimates of breeder bond duration in a social carnivore and highlights the effect of extrinsic (i.e. anthropogenic) and intrinsic factors (i.e. inbreeding) involved in wolf pair bond duration. Unlike the effects of intrinsic and extrinsic factors that are commonly reported on individual survival or population growth, here we provide quantitative estimates of their potential effect on the social unit of the population, the wolf pair.

Prey Selection of Scandinavian Wolves: Single Large or Several Small?

Research on large predator-prey interactions are often limited to the predators' primary prey, with the potential for prey switching in systems with multiple ungulate species rarely investigated. We evaluated wolf (Canis lupus) prey selection at two different spatial scales, i.e., inter- and intra-territorial, using data from 409 ungulate wolf-kills in an expanding wolf population in Scandinavia. This expansion includes a change from a one-prey into a two-prey system with variable densities of one large-sized ungulate; moose (Alces alces) and one small-sized ungulate; roe deer (Capreolus capreolus). Among wolf territories, the proportion of roe deer in wolf kills was related to both pack size and roe deer density, but not to moose density. Pairs of wolves killed a higher proportion of roe deer than did packs, and wolves switched to kill more roe deer as their density increased above a 1:1 ratio in relation to the availability of the two species. At the intra-territorial level, wolves again responded to changes in roe deer density in their prey selection whereas we found no effect of snow depth, time during winter, or other predator-related factors on the wolves' choice to kill moose or roe deer. Moose population density was only weakly related to intra-territorial prey selection. Our results show that the functional response of wolves on moose, the species hitherto considered as the main prey, was strongly dependent on the density of a smaller, alternative, ungulate prey. The impact of wolf predation on the prey species community is therefore likely to change with the composition of the multi-prey species community along with the geographical expansion of the wolf population.

Mobility of moose-comparing the effects of wolf predation risk, reproductive status, and seasonality.

In a predator-prey system, prey species may adapt to the presence of predators with behavioral changes such as increased vigilance, shifting habitats, or changes in their mobility. In North America, moose (Alces alces) have shown behavioral adaptations to presence of predators, but such antipredator behavioral responses have not yet been found in Scandinavian moose in response to the recolonization of wolves (Canis lupus). We studied travel speed and direction of movement of GPS-collared female moose (n = 26) in relation to spatiotemporal differences in wolf predation risk, reproductive status, and time of year. Travel speed was highest during the calving (May-July) and postcalving (August-October) seasons and was lower for females with calves than females without calves. Similarly, time of year and reproductive status affected the direction of movement, as more concentrated movement was observed for females with calves at heel, during the calving season. We did not find support for that wolf predation risk was an important factor affecting moose travel speed or direction of movement. Likely causal factors for the weak effect of wolf predation risk on mobility of moose include high moose-to-wolf ratio and intensive hunter harvest of the moose population during the past century.

Genetic rescue in a severely inbred wolf population.

Natural populations are becoming increasingly fragmented which is expected to affect their viability due to inbreeding depression, reduced genetic diversity and increased sensitivity to demographic and environmental stochasticity. In small and highly inbred populations, the introduction of only a few immigrants may increase vital rates significantly. However, very few studies have quantified the long-term success of immigrants and inbred individuals in natural populations. Following an episode of natural immigration to the isolated, severely inbred Scandinavian wolf (Canis lupus) population, we demonstrate significantly higher pairing and breeding success for offspring to immigrants compared to offspring from native, inbred pairs. We argue that inbreeding depression is the underlying mechanism for the profound difference in breeding success. Highly inbred wolves may have lower survival during natal dispersal as well as competitive disadvantage to find a partner. Our study is one of the first to quantify and compare the reproductive success of first-generation offspring from migrants vs. native, inbred individuals in a natural population. Indeed, our data demonstrate the profound impact single immigrants can have in small, inbred populations, and represent one of very few documented cases of genetic rescue in a population of large carnivores.