Download Workshop II: Fox Ecology, Stockholm, August 17 2015

Workshop II: Fox Ecology, Stockholm, August 17 2015
Room: E306, Arrhenius Laboratory building
Contact: Karin Norén ([email protected] ), Department of Zoology, Stockholm University
09.00-09.20
09.20-09.30
FIKA
Introduction
Karin Norén, Stockholm
University
Population ecology and conservation
09:30-09.50
Red fox ecology in a landscape gradient
09.50-10.30
10.30-10.50
10.50-11.10
11.10-11.20
11.20-11.40
Leg length adaptation in the Scandinavian red fox (Vulpes
vulpes)
The demography and of the Icelandic arctic fox: long
term fluctuations AND stability
SHORT BREAK
Conservation work in practise: Saving the Endangered
Fennoscandian Alopex SEFALO
Arctic fox social organization
Tomas Willebrand, Hedmark
University
Jan Englund
Ester Rut Unnsteinsdottir, The
Icelandic Institute of Natural
History
Anders Angerbjörn, Stockholm
University
Bodil Elmhagen, Stockholm
University
11.40-13.40
LUNCH
Genetics and taxonomy
13.40-14.00
Deep secrets revealed: A view into the phylogeography,
historical demography, and speciation in the world's
most basal canid, Urocyon spp
14.00-14.20
Peninsulas and islands in a sea of red: phylogeography
and population substructure of the European red fox
14.20-14.40
Genomic variation and signatures of selection in
European red foxes (Vulpes vulpes)
14.40-15.00
Genetic complexity of a simple behavioral pattern
Benjamin N. Sacks, University of
California, Davis
Mark J. Statham, University of
California, Davis
Allan McDevitt, Mammal
Research Institute, Poland
Anna Kukekova, University of
Illinois at Urbana-Champaign
15.00-15.20
FIKA
Community ecology
15.20-15.40
The arctic fox as model system to study trophic
interactions
15.40-16.00
Species interactions along a productivity gradient mesopredator dynamics in different ecosystems
15.30-15.50
The red fox (Vulpes vulpes) in a trophic interaction
perspective
15.50-16.10
Focused sampling of red fox faeces for identification of
Echinococcus multilocularis in Sweden
16.10-16.30
Interference in the tundra predator guild studied using
local ecological knowledge
Future research projects and collaboration
16.30-16.45
Knowledge about fox migration needed to predict the
16.45-17.00
17.00-17.15
spread of Echinococcus multilocularis
The ECOFUNC project
Prey preferences of red foxes in their native and
introduced ranges
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Dominique Berteaux, Université
du Québec à Rimouski
Rasmus Erlandsson, Stockholm
University
Marianne Pasanen Mortensen,
Stockholm University
Andrea Miller, Swedish
University of Agriculture
Siw Killengreen, The Arctic
University of Norway
Helene Wahlström, National
Veterinary Institute
Nina Eide, Norwegian Institute
for Nature Research
Matt Hayward, Bangor
University
ABSTRACTS
Red fox ecology in a landscape gradient
Tomas Willebrand, M. Odden, G. Samelius, J. Englund
In this red fox project we have captured 84 individuals, and have equipped 67 with radio collars since
2011. Sixteen of these are presently active and sending data. The project is a cooperation between
Grimsö Research Station, SLU, Sweden and Campus Evenstad, HiHM. We work with foxes in a
gradient from the mixed agricultural/forest areas south of Stockholm, to the mixed forest/tundra
landscape in central Norway. In this presentation, we will show some preliminary results on home
range sizes, movement and dispersal distance, and mortality data. We will also propose
characteristics of the population dynamics in the different parts of the productivity gradient, and
compare estimates of survival with those from just before and during the outbreak of the sarcoptic
mange.
Leg length adaptation in Scandinavian red fox
Jan Englund
The habitats used by the red fox (Vulpes vulpes) in the five areas studied in Scandinavia show great
variability in climate, prey offered and total productivity. In the far north, the winter is long, the
ground is covered by thick snow and the productivity is low. In the south there is little or no snow
and the productivity is high. The prey is mostly voles, but in the south rabbits and hare are in
majority, demanding a different hunting technique. How these ecological factors have influenced the
anatomy of the fox is discussed with special focus on the hind legs.
The demography of the Icelandic arctic fox: long term fluctuations AND stability.
Ester Rut Unnsteinsdottir
According to hunting statistics and scientific studies, the arctic fox population expressed long term
fluctuations during a period of half a century. The population had been large in 1950´s, but from then
it declined and reached a minimum of 1.000 individuals in 1970´s and began to rise since then until
2008 when it exceeded 10.000 individuals. In an attempt to explain the fall and rise of the Icelandic
arctic fox, these fluctuations have been associated with climate conditions and productivity of birds
and other prey. No cycling rodents exist in Iceland and in most regions, foxes feed on birds of various
types, eggs, carrion (sheep, reindeer, seals), invertebrates and berries. Predictable and steady food
resources are reflected in low fertility as the arctic fox vixens give birth to litters of 4-6 cubs annually.
Thus, in contrast to the situation in “lemming areas”, changes in fertility in accordance to changeable
food conditions have not been observed and therefore do not regulate the population dynamics of
the Icelandic arctic fox. Milder climate caused improved conditions for both predator and prey and is
therefore likely to have affected survival rate and body condition. Thus, higher proportion of mature
individuals taking part in breeding could play an important role. This could be explained by increased
carrying capacity, either by higher density or extended distribution. It is therefore important to look
into the data with both spatial and biological aspect. The regulation and limitation of the Icelandic
arctic fox population is apparently based on a mixture of environmental and demographical events,
regardless of heavy but steady hunting effort.
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Conservation work in practise: Saving the Endangered Fennoscandian Alopex SEFALO
Anders Angerbjörn
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. We report on a 30-year inventory of
the critically endangered Fennoscandian arctic fox. 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. 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. This demonstrates that carnivore population declines may
be reversed through extensive actions that target specific threats. The 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.
Arctic fox social organization
Bodil Elmhagen
Canids display pronounced intraspecific variation in social organization, ranging from single breeding
females to large and complex groups. We investigate social organization – intraspecific tolerance and
group occurrence during breeding - in a socially flexible canid, the arctic fox (Vulpes lagopus).
Comparing four different ecosystems, we found a significant relationship between resource
conditions and formation of complex groups. Within Sweden, supplemental feeding increased group
formation and alloparental behaviour among related females in "fox towns" could also contribute to
group formation. We conclude that sufficient amounts of food is a prerequisite for group formation,
but that improved predator defence further increases the benefits of living in larger groups.
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Deep secrets revealed: A view into the phylogeography, historical demography, and speciation in
the world's most basal canid, Urocyon spp
Benjamin N. Sacks, M.J. Statham, N. Goddard, L. Serieys, and S. Riley
We investigated cross-continental and regional phylogeography of Urocyon, the most basal extant
lineage of canid in the world. In North America, many temperate forest-associated vertebrates split
into eastern and western lineages due to Pleistocene aridification in the central portion of the
continent, yet currently occur in continuous distributions due to secondary contact associated with
Holocene expansions. Because of the antiquity of Urocyon in the fossil record on both ends of the
North American continent, we investigated whether gray foxes Urocyon exhibited a deep, cryptic
divergence associated with eastern and western refugia. Sequence divergence and coalescent
simulations based on mitochondrial DNA sequences from 180 foxes indicated divergence between
eastern and western foxes approximately 500,000 years ago, which is comparable to that between
recognized sister species within the Canidae. Second, we investigated the regional phylogeography
of gray (U. cinereoargenteus) and island (U. littoralis) foxes associated with the putative western
refugium. Analysis of mtDNA and microsatellites revealed some unexpected findings, prompting new
questions about the origins of island foxes relative to contemporary mainland gray foxes.
Peninsulas and islands in a sea of red: phylogeography and population substructure of the
European red fox.
Mark J. Statham, C.J. Edwards, K. Norén, O’Mahoney, O’Reilly, C.D. Soulsbury, B. N. Sacks
Historical climate change during the Quaternary Period caused both temperate and arctic adapted
species to cycle through periods of range expansion and contraction. Such changes alternately
facilitated and constrained gene flow, and resulted in both the evolution of local endemic lineages
and in genetic homogenization. Previous investigations of red fox (Vulpes vulpes) population
substructure within Europe have concluded that there is relatively limited population subdivision
evident in mtDNA, while regional microsatellite based studies have found both minimal subdivision
and local subdivision. Here we examined the continent-wide subdivision of 275 European red foxes
examined at two mitochondrial gene regions and 21 nuclear microsatellite markers. We identified
distinct populations on continental peninsulas and off-shore islands, and a central population derived
from multiple sources. These findings along with population splitting time estimates shed light on the
post-glacial colonization history of the species.
Genomic variation and signatures of selection in European red foxes (Vulpes vulpes)
Allan McDevitt, M.J. Statham, A. Ruiz-González, I. Ruczyńska, E. Randi, C. Pertoldi, J. Mullins, B.N.Sacks, R.
Kowalczyk and J. Wójcik
The advent of next-generation sequencing techniques has the potential to revolutionize our
understanding of phylogeographic and adaptive processes in mammals at the continental scale. A
total of 373 red foxes were genotyped in 24 populations using genotype-by-sequencing (GBS) to
identify patterns of variation and signatures of selection in the genomes of red foxes across Europe.
Almost 22,000 SNPs were retained after various quality control and filtering steps. Levels of genomic
diversity were similar among populations but were generally lower in the most northerly populations
in Scandinavia and the island populations. Fst-outlier analysis identified a large number of SNPs
showing evidence of selection across a wide variety of genomic regions. Ongoing work will
incorporate additional samples from Britain, the Mediterranean peninsulas and Russia in order to
further elucidate phylogeographic and adaptive processes in this charismatic carnivore across
Europe.
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Genetic complexity of a simple behavioral pattern
Anna V. Kukekova, J.L. Johnson, S.V. Temnykh, A.V. Kharlamova, A.V. Vladimirova, R.G. Gulevich and L.N. Trut
Two strains of foxes (Vulpes vulpes) selected for specific behaviors demonstrate markedly different
responses to humans. Tame strain foxes solicit attention and initiate tactile interaction with an
experimenter while aggressive strain foxes avoid contact and demonstrate defensive aggression
when approached. Fox behavior was tested in a four stage test which was designed to evaluate fox
responses in situations with different level of interaction between the experimenter and tested
animal. Fox behavior was deconstructed from video records into a set of traits and the main
components of behavior at each test stage were reconstructed using Principal Component (PC)
analysis. PC1 clearly differentiated between the tame and aggressive foxes at each test stage. An F2
population was produced by cross-breeding tame and aggressive strains and then breeding the F1
individuals to each other. In addition to displaying the behavioral patterns of the parental strains, F2
offspring also demonstrated novel patterns. These findings suggest that the behavioral patterns of
parental tame and aggressive foxes although constant from stage to stage (consistently high or low
PC1 values) contain subsets of behaviors that can re-assort in segregant populations to yield novel
patterns of sequential behaviors. Genetic mapping of F2 pedigrees identified loci that are common to
behavioral PCs extracted from different test stages and loci associated with behaviors specific to a
particular stage, further supporting the underlying genetic complexity of tame and aggressive
patterns.
The arctic fox as model system to study trophic interactions
Dominique Berteaux
The arctic fox inhabits a simplified food web where predators, competitors, and prey are few. In this
context, identifying its preferred, alternative, and incidental prey is possible, as well as
quantifying most trophic interactions structuring its tundra ecosystem. Arctic foxes can also use the
sea ice as foraging habitat in winter. The above opens many opportunities for hypothesis testing
at the community, ecosystem, and meta-ecosystem scales. I use 20 years of work from Bylot Island
(Nunavut, Canada) to illustrate how foxes can be used as model system to study trophic interactions.
In particular, I show how an ecosystem-based monitoring combined with state-of-the-art field (stable
isotopes, satellite tracking, movement-triggered cameras, etc.) and modeling techniques have
allowed recent progress in ecology, using foxes as study model. I also try to identify some of the
attributes of Vulpes that make them interesting models to study trophic interactions.
Species interactions along a productivity gradient - mesopredator dynamics in different ecosystems
Rasmus Erlandsson
Species belonging to a certain trophic level have the potential to limit species on the level below
them, and to be limited by species above them. Interactions between different animal species is
however not limited to the basic ecology of the species involved, but could also be subject to
modification by environmental factors; for example primary productivity. According to the
Exploitation Ecosystem Hypothesis the number of trophic levels increases with primary productivity.
Therefore, primary productivity, and hence the number of trophic levels, could be expected to affect
animal interactions. Primary productivity is related to the amount of available sunlight but could be
limited by temperature or availability of water. As sunlight and growth season varies over the world
it is possible to compare different ecosystems along a productivity gradient and investigate
differences in species interactions. The /Vulpes/ genus (foxes) has a large distribution range
representing species of different body sizes, ecological niches and distribution. Foxes are common
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both as top predators and mesopredators depending on ecological setting and different fox species
could hence be a suitable study group when comparing population dynamics and interactions in
different habitats. In this study I go through available literature on population dynamics and
interspecific interactions of fox species in a wide range of ecosystems over the world, and relate
them to primary productivity.
The red fox (Vulpes vulpes) in a trophic interaction perspective
Marianne Pasanen Mortensen
The red fox seem to hold an intermediate position in the food web where they interact with prey as
well as with larger predators - they function as mesopredators. This implies that the red fox can be
limited top-down by predators at the top of the food chain, apex predators, and bottom-up by
environmental conditions affecting food access. The red fox is thus an ideal study species for trophic
interactions, and as the red fox has a wide distribution range it is also ideal to study trophic processes
that occur on large scales. This presentation will describe relationships between the red fox, apex
predators, and drivers related to prey abundance - primary productivity, climate, land use and
human density – at a continental scale, assessed in two studies of the fox population in Europe and
northern Eurasia. According to the mesopredator release hypothesis extinction of apex predators can
result in an increase of mesopredators, as top-down limitation is lost. The studies show that the
Eurasian lynx, together with winter severity, is important in limiting red fox abundance, and it
supports the mesopredator release hypothesis as red fox abundance is higher where lynx has been
eradicated than where lynx is still present. In the absence of lynx, red fox abundance is boosted by
anthropogenic land use, and red fox abundance is highest when croplands constitute 30% of the
landscape, where after social regulation seems to limit foxes. Using the red fox as a model species of
trophic interactions at a continental scale, we conclude that apex predators can be important in
structuring ecosystems by limiting mesopredators, and that there are two ecosystem states in
Eurasia – one in north where lynx function as apex predator and the red fox as mesopredator, and
one in south-west where lynx is eradicated and the red fox has assumed the role of an apex predator.
Focused sampling of red fox (Vulpes vulpes) feces for identification of Echinococcus multilocularis
in Sweden
Andrea L. Miller, G.E. Olsson, S. Sollenberg, M. Skarin, H. Wahlström and J. Höglund
Following the first identification of Echinococcus multilocularis in a red fox (Vulpes vulpes) shot in
December 2010 in Sweden, a research project began to identify and further investigate the role of
the rodent intermediate host in the parasite’s lifecycle. As part of this research, fox feces are
collected to assess the level of environmental contamination of parasite eggs in rodent habitats.
Seasonal sampling has occurred in four areas chosen according to their E. multilocularis status at the
beginning of the study in 2013 [Uddevalla (U) and Katrineholm (K)-known parasite status; Växjö (V)
and Gnesta/Nyköping (G)-unknown parasite status]. Although fecal samples are collected throughout
each ~20x20 km area, special effort is put in habitats, such as fields, where rodent trapping occurs.
These focused collection methods result in intense sampling [e.g 28 feces collected in one field (~25
ha), winter 2014]. Parasite eggs are isolated from feces by sieving methods and tested with PCR and
sequencing for species identification. To date, 612 fecal samples have been collected. Although
collection and analysis are still ongoing, preliminary results show positive fecal samples in all areas [U
5/193 (2.6%); K 3/110 (2.7%); V 2/58 (3.4%); G 6/41 (14.6%)]. These results indicate “hot spots” of E.
multilocularis where the prevalence in foxes may be higher than the national prevalence of 0.1%
estimated from two recent nation-wide screenings. This collection method has also identified two
additional positive areas (V and G) not detected in the initial screening. We suggest that risk-based
surveillance (i.e. focused sampling in presumed high risk habitats) is an effective strategy to identify
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E. multilocularis in the environment. Particularly for countries declared E. multilocularis free, these
findings are an important consideration for the allocation of surveillance resources.
THIS ABSTRACT ALSO ACCEPTED FOR PRESENTATION AT THE NORDIC WILDLIFE DISEASE ASSOCIATION MEETING JUNE 10-12, 2015
Interference in the tundra predator guild studied using local ecological knowledge
D. Ehrich, M. Strømeng and Siw T. Killengreen
The decline or recolonization of apex predators such as wolves and lynx often driven by management
decisions, and the expansion of smaller generalist predators such as red foxes can have important
ecosystem impacts. The mesopredator release hypothesis proposes that apex predators control
medium sized predator populations through competition and/or intraguild predation. The decline of
apex predators leads thus to an increase in mesopredators, possibly with a negative impact on prey
populations. Information about the abundance of mammalian tundra predators (wolf, lynx,
wolverine, red fox and arctic fox) was collected from local active outdoors people during semistructured interviews in 14 low arctic or sub-arctic settlements in western Eurasia.
Results: The perceived abundance of red fox decreased with higher wolf abundance, but the negative
effect of wolves decreased in more Arctic and therefore less productive ecosystems. The perceived
abundance of arctic fox increased towards the Arctic and in areas with colder winters. Red fox
abundance did only have a major effect on arctic fox abundance in the western part of the study
area, possibly because of interference between wolves and red foxes in eastern areas. Our results
support the mesopredator release hypothesis regarding the expansion of red foxes in subarctic areas
and indicate that top down control by apex predators is weaker in less productive and more Arctic
ecosystems. Significance: We showed that local ecological knowledge is a valuable source of
information about large-scale processes which are difficult to study through direct biological
investigations.
Knowledge about fox population migration needed to predict the spread of Echinococcus
multilocularis
Helene Wahlström
Echinococcus multilocularis (Em) is an emerging parasitic disease with a life cycle that involves canids,
usually foxes, as the definitive host and rodents as intermediate hosts. Humans can act as an
accidental intermediate host and develop a serious, potentially fatal disease if untreated. The
endemic area of this parasite in Europe is considered to be expanding and there is evidence that both
the fox population and the prevalence of Em has increased in many areas. Over the past two decades
the parasite has spread from central Europe to Northern, Eastern and Western Europe. A few
countries are documented to be free from Em: UK, Ireland, Malta, Norway and Finland. To prevent
introduction of Em, these countries are allowed to require that dogs imported are dewormed prior to
entry. To maintain these import requirements, the countries are required to document, on an annual
basis that the prevalence of Em in foxes is below 1% with 95% confidence. These requirements are
presently being revised and it has been discussed if freedom from Em should be documented at a
lower level, for example 0.1%, the current prevalence of Em in Sweden. This would require that
approximately 3000 fox scats are analysed annually, which would be very expensive. However, by
using a baysian methodology, where results from surveillance done in previous years are taken into
account, the required sample size could be decreased. However, this methodology requires an
estimate of the probability of introduction of the parasite into the country. Although data is scarce,
the risk of introduction by dogs may be estimated. However, for Norway and Finland the highest
probability of introduction would be by foxes or racoon dogs. This requires estimates of the density
of foxes/racoon dogs, the prevalence of Em in foxes/racoon dogs and knowledge of migration
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patterns between Norway/Finland and adjacent Em-endemic countries. If this is possible is a
question that needs to be answered.
The ECOFUNC project
Nina E. Eide
Understanding ecosystem functionality, expansion and retreat of species in the Scandinavian mountain tundra
under multiple drivers of change. Using Scandinavian foxes as indicators of change. The Fennoscandian
mountain range comprises a series of separate arctic and alpine tundra areas. This natural fragmentation is
expected to be magnified following climate mediated forest advance with associated invasion of boreal species.
Cumulative effects of climate change, land use changes and management practices will likely have large
impacts on both structure and function of the mountain tundra ecosystem; strongly affect biodiversity and the
viability of species in these habitats, and the mountain tundra ecosystem's ability to deliver ecosystem services.
The proposed project has a tri-trophic ecosystem approach, testing hypotheses about how climate change,
land use, and management practices drive species expansion and retreat in the mountain tundra ecosystem.
We use forest advancement, red fox invasion and arctic fox retreat as our model system and as indicators of
ecosystem change. The project will deliver hard data on the relationship between environmental change and
functional and structural responses of individuals, populations, and communities of the mountain tundra
ecosystem. We will apply an interdisciplinary approach, including observational and experimental methods at
large spatial scales, GIS and spatial modelling, landscape genomics, and population viability analyses, providing
the basis for a predictive model for the future structure of the mountain tundra ecosystem in Fennoscandia.
The project is highly relevant to conservation management. We aim to develop tools that could forecast
cumulative impacts from different drivers, providing potential management options showing the outcome of
different solutions. Indeed, such tools would be useful for planning and optimizing conservation programs,
restoration of landscapes, targeting management action, or controlling the spread of diseases.
Prey preferences of red foxes in their native and introduced ranges
Matt Hayward
Be aware - this talk is a call for research collaboration rather than a description of my research
results. One of my research areas involves meta-analyses of the prey preferences of predators by
comparing what they eat with what prey is available. Myself and colleagues have conducted such
studies on Africa and Asia’s large carnivore guilds, and are now moving on to large carnivores in the
Americas. We have also started looking at smaller carnivores to see if they follow the same principles
of prey selection: predators invariably preferentially kill a limited number of prey species that usually
fall within a specific preferred prey weight range. I’d like to extend this work to foxes, and
particularly compare the prey preferences of red foxes Vulpes vulpes in their native and introduced
ranges. Hence, I am seeking collaborators who have data on red fox diet and the abundance (actual
or relative) of the prey community at the same sites from throughout the distribution of the species.
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Workshop participants (as of August 12)
Angerbjörn
Berteaux
Eide
Elmhagen
Englund
Ferreras de Andres
Harrison
Hayward
Killengreen
Kowalczyk
Kukekova
McDevitt
Miller
Norén
Pasanen-Mortensen
Rod-Eriksen
Sacks
Samelius
Sangin
Statham
Thierry
Ulvund Roaldsnes
Unnsteinsdottie
Wahlström
Wallén
Willebrand
Wójcik
Anders
Dominique
Nina E.
Bodil
Jan
Pablo
Stephen
Matt
Siw T.
Rafal
Anna
Allan
Andrea
Karin
Marianne
Lars
Benjamin N.
Gustaf
Kim
Mark J.
Anne-Mathilde
Kristine
Ester Rut
Helene
Johan
Thomas
Jan M.
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