Karin Norén

Carnivore conservation in practice: replicated management actions on a large spatial scale

Summary 1. More than a quarter of the world’s carnivores are threatened, often due to multiple and complex causes. Considerable research efforts are devoted to resolving the mechanisms behind these threats in order to provide a basis for relevant conservation actions. However, even when the underlying mechanisms are known, specific actions aimed at direct support for carnivores are difficult to implement and evaluate at efficient spatial and temporal scales. 2. We report on a 30-year inventory of the critically endangered Fennoscandian arctic fox Vulpes lagopus L., including yearly surveys of 600 fox dens covering 21 000 km 2 . These surveys showed that the population was close to extinction in 2000, with 40–60 adult animals left. However, the population subsequently showed a fourfold increase in size. 3. During this time period, conservation actions through supplementary feeding and predator removal were implemented in several regions across Scandinavia, encompassing 79% of the area. To evaluate these actions, we examined the effect of supplemental winter feeding and red fox control applied at different intensities in 10 regions. A path analysis indicated that 47% of the explained variation in population productivity could be attributed to lemming abundance, whereas winter feeding had a 29% effect and red fox control a 20% effect. 4. This confirms that arctic foxes are highly dependent on lemming population fluctuations but also shows that red foxes severely impact the viability of arctic foxes. This study also highlights the importance of implementing conservation actions on extensive spatial and temporal scales, with geographically dispersed actions to scientifically evaluate the effects. We note that population recovery was only seen in regions with a high intensity of management actions. 5. Synthesis and applications. The present study demonstrates that carnivore population declines may be reversed through extensive actions that target specific threats. Fennoscandian arctic fox is still endangered, due to low population connectivity and expected climate impacts on the distribution and dynamics of lemmings and red foxes. Climate warming is expected to contribute to both more irregular lemming dynamics and red fox appearance in tundra areas; however, the effects of climate change can be mitigated through intensive management actions such as supplemental feeding and red fox control.

Pulses of movement across the sea ice: population connectivity and temporal genetic structure in the arctic fox

Lemmings are involved in several important functions in the Arctic ecosystem. The Arctic fox (Vulpes lagopus) can be divided into two discrete ecotypes: “lemming foxes” and “coastal foxes”. Crashes in lemming abundance can result in pulses of “lemming fox” movement across the Arctic sea ice and immigration into coastal habitats in search for food. These pulses can influence the genetic structure of the receiving population. We have tested the impact of immigration on the genetic structure of the “coastal fox” population in Svalbard by recording microsatellite variation in seven loci for 162 Arctic foxes sampled during the summer and winter over a 5-year period. Genetic heterogeneity and temporal genetic shifts, as inferred by STRUCTURE simulations and deviations from Hardy–Weinberg proportions, respectively, were recorded. Maximum likelihood estimates of movement as well as STRUCTURE simulations suggested that both immigration and genetic mixture are higher in Svalbard than in the neighbouring “lemming fox” populations. The STRUCTURE simulations and AMOVA revealed there are differences in genetic composition of the population between summer and winter seasons, indicating that immigrants are not present in the reproductive portion of the Svalbard population. Based on these results, we conclude that Arctic fox population structure varies with time and is influenced by immigration from neighbouring populations. The lemming cycle is likely an important factor shaping Arctic fox movement across sea ice and the subsequent population genetic structure, but is also likely to influence local adaptation to the coastal habitat and the prevalence of diseases.

Reproductive isolation and patterns of genetic differentiation in a cryptic butterfly species complex

Molecular studies of natural populations are often designed to detect and categorize hidden layers of cryptic diversity, and an emerging pattern suggests that cryptic species are more common and more widely distributed than previously thought. However, these studies are often decoupled from ecological and behavioural studies of species divergence. Thus, the mechanisms by which the cryptic diversity is distributed and maintained across large spatial scales are often unknown. In 1988, it was discovered that the common Eurasian Wood White butterfly consisted of two species (Leptidea sinapis and Leptidea reali), and the pair became an emerging model for the study of speciation and chromosomal evolution. In 2011, the existence of a third cryptic species (Leptidea juvernica) was proposed. This unexpected discovery raises questions about the mechanisms preventing gene flow and about the potential existence of additional species hidden in the complex. Here, we compare patterns of genetic divergence across western Eurasia in an extensive data set of mitochondrial and nuclear DNA sequences with behavioural data on inter‐ and intraspecific reproductive isolation in courtship experiments. We show that three species exist in accordance with both the phylogenetic and biological species concepts and that additional hidden diversity is unlikely to occur in Europe. The Leptidea species are now the best studied cryptic complex of butterflies in Europe and a promising model system for understanding the formation of cryptic species and the roles of local processes, colonization patterns and heterospecific interactions for ecological and evolutionary divergence.

Kin encounter rate and inbreeding avoidance in canids

Mating with close kin can lead to inbreeding depression through the expression of recessive deleterious alleles and loss of heterozygosity. Mate selection may be affected by kin encounter rate, and inbreeding avoidance may not be uniform but associated with age and social system. Specifically, selection for kin recognition and inbreeding avoidance may be more developed in species that live in family groups or breed cooperatively. To test this hypothesis, we compared kin encounter rate and the proportion of related breeding pairs in noninbred and highly inbred canid populations. The chance of randomly encountering a full sib ranged between 1–8% and 20–22% in noninbred and inbred canid populations, respectively. We show that regardless of encounter rate, outside natal groups mates were selected independent of relatedness. Within natal groups, there was a significant avoidance of mating with a relative. Lack of discrimination against mating with close relatives outside packs suggests that the rate of inbreeding in canids is related to the proximity of close relatives, which could explain the high degree of inbreeding depression observed in some populations. The idea that kin encounter rate and social organization can explain the lack of inbreeding avoidance in some species is intriguing and may have implications for the management of populations at risk.

Harmonizing circumpolar monitoring of Arctic fox: benefits, opportunities, challenges and recommendations

ABSTRACT The biodiversity working group of the Arctic Council has developed pan-Arctic biodiversity monitoring plans to improve our ability to detect, understand and report on long-term change in Arctic biodiversity. The Arctic fox (Vulpes lagopus) was identified as a target of future monitoring because of its circumpolar distribution, ecological importance and reliance on Arctic ecosystems. We provide the first exhaustive survey of contemporary Arctic fox monitoring programmes, describing 34 projects located in eight countries. Monitored populations covered equally the four climate zones of the species’ distribution, and there were large differences between populations in long-term trends, multi-annual fluctuations, diet composition, degree of competition with red fox and human interferences. Den density, number of active dens, number of breeding dens and litter size were assessed in almost all populations, while projects varied greatly with respect to monitoring of other variables indicative of population status, ecosystem state or ecosystem function. We review the benefits, opportunities and challenges to increased integration of monitoring projects. We argue that better harmonizing protocols of data collection and data management would allow new questions to be addressed while adding tremendous value to individual projects. However, despite many opportunities, challenges remain. We offer six recommendations that represent decisive progress toward a better integration of Arctic fox monitoring projects. Further, our work serves as a template that can be used to integrate monitoring efforts of other species, thereby providing a key step for future assessments of global biodiversity.

The impact of maternal experience on post-weaning survival in an endangered arctic fox population

Behavioural differences in parental care can influence offspring survival through variation in e.g. antipredator behaviour and ability to provide food. In a broad range of species, offspring survival has been found to be higher for experienced females compared to inexperienced first-time breeders. The increase in offspring survival for experienced females has mainly been explained by improved experience in providing food. In this paper, we have studied post-weaning juvenile survival in relation to maternal experience in an endangered population of arctic foxes (Vulpes lagopus) in Fennoscandia. For cubs raised by inexperienced and experienced females, the survival rate was 0.42 (CI 95% ± 0.31) and 0.87 (CI 95% ± 0.08), respectively. There was no difference in body condition between the cubs and no observations of starvation. We suggest that the difference in survival was due to lack of experience to one of the most common predators, the golden eagle (Aquila chrysaetos). Golden eagles were mainly observed on dens with litters where the females were inexperienced first-time breeders. From a conservation perspective, it is therefore important to increase adult survival through actions to enlarge the proportion of experienced breeders.

Homage to Hersteinsson and Macdonald: climate warming and resource subsidies cause red fox range expansion and Arctic fox decline

ABSTRACT Climate change can have a marked effect on the distribution and abundance of some species, as well as their interspecific interactions. In 1992, before ecological effects of anthropogenic climate change had developed into a topical research field, Hersteinsson and Macdonald published a seminal paper hypothesizing that the northern distribution limit of the red fox (Vulpes vulpes) is determined by food availability and ultimately climate, while the southern distribution limit of the Arctic fox (Vulpes lagopus) is determined by interspecific competition with the larger red fox. This hypothesis has inspired extensive research in several parts of the circumpolar distribution range of the Arctic fox. Over the past 25 years, it was shown that red foxes can exclude Arctic foxes from dens, space and food resources, and that red foxes kill and sometimes consume Arctic foxes. When the red fox increases to ecologically effective densities, it can cause Arctic fox decline, extirpation and range contraction, while conservation actions involving red fox culling can lead to Arctic fox recovery. Red fox advance in productive tundra, concurrent with Arctic fox retreat from this habitat, support the original hypothesis that climate warming will alter the geographical ranges of the species. However, recent studies show that anthropogenic subsidies also drive red fox advance, allowing red fox establishment north of its climate-imposed distribution limit. We conclude that synergies between anthropogenic subsidies and climate warming will speed up Arctic ecosystem change, allowing mobile species to establish and thrive in human-provided refugia, with potential spill-over effects in surrounding ecosystems.

Genetic footprints reveal geographic patterns of expansion in Fennoscandian red foxes.

Population expansions of boreal species are among the most substantial ecological consequences of climate change, potentially transforming both structure and processes of northern ecosystems. Despite their importance, little is known about expansion dynamics of boreal species. Red foxes (Vulpes vulpes) are forecasted to become a keystone species in northern Europe, a process stemming from population expansions that began in the 19th century. To identify the relative roles of geographic and demographic factors and the sources of northern European red fox population expansion, we genotyped 21 microsatellite loci in modern and historical (1835-1941) Fennoscandian red foxes. Using Bayesian clustering and Bayesian inference of migration rates, we identified high connectivity and asymmetric migration rates across the region, consistent with source-sink dynamics, whereby more recently colonized sampling regions received immigrants from multiple sources. There were no clear clines in allele frequency or genetic diversity as would be expected from a unidirectional range expansion from south to north. Instead, migration inferences, demographic models and comparison to historical red fox genotypes suggested that the population expansion of the red fox is a consequence of dispersal from multiple sources, as well as in situ demographic growth. Together, these findings provide a rare glimpse into the anatomy of a boreal range expansion and enable informed predictions about future changes in boreal communities.

Inbreeding depression in a critically endangered carnivore

Harmful effects arising from matings between relatives (inbreeding) is a long‐standing observation that is well founded in theory. Empirical evidence for inbreeding depression in natural populations is however rare because of the challenges of assembling pedigrees supplemented with fitness traits. We examined the occurrence of inbreeding and subsequent inbreeding depression using a unique data set containing a genetically verified pedigree with individual fitness traits for a critically endangered arctic fox (Vulpes lagopus) population. The study covered nine years and was comprised of 33 litters with a total of 205 individuals. We recorded that the present population was founded by only five individuals. Over the study period, the population exhibited a tenfold increase in average inbreeding coefficient with a final level corresponding to half‐sib matings. Inbreeding mainly occurred between cousins, but we also observed two cases of full‐sib matings. The pedigree data demonstrated clear evidence of inbreeding depression on traditional fitness traits where inbred individuals displayed reduced survival and reproduction. Fitness traits were however differently affected by the fluctuating resource abundande. Inbred individuals born at low‐quality years displayed reduced first‐year survival, while inbred individuals born at high‐quality years were less likely to reproduce. The documentation of inbreeding depression in fundamental fitness traits suggests that inbreeding depression can limit population recovery. Introducing new genetic material to promote a genetic rescue effect may thus be necessary for population long‐term persistence.

Red foxes colonizing the tundra: genetic analysis as a tool for population management

Climate change accelerates biodiversity alterations in northern ecosystems. A prevalent example is that tundra regions are invaded by boreal species. This impacts negatively on native species through competition, predation and transmission of zoonoses. Scandinavian red foxes (Vulpes vulpes) have emerged into the tundra and have altered the structure and function of the tundra community. For instance, they threaten persistence of the endangered Swedish Arctic fox (Vulpes lagopus). County board administrations implement control of the tundra red foxes, but little is known about the underlying expansion dynamics. A broad-scale study revealed high connectivity where northern areas were supplemented with red foxes from surrounding population. However, red fox expansion is most prevalent in tundra regions and the fine-scaled expansion dynamics in these areas have not yet been disseminated. With the aim of identifying the invasive pathways of tundra red foxes, we present microsatellite data for 205 Swedish red foxes and mitochondrial sequence variation in 102 foxes sampled across the historical boreo-nemoral distribution and recently colonized tundra regions. Genetic structuring was low with high levels of ongoing, asymmetric dispersal from surrounding boreal zones into tundra habitats causing high genetic admixture. In both tundra and boreo-nemoral regions, inter-individual relatedness decreased with increasing geographic distance and data suggests male-biased dispersal patterns. Overall, fine-scaled expansion patterns were affected by multiple factors and we discuss its implications for future red fox management.