Download Anthropogenic impact on predator guilds and ecosystem processes:

Anthropogenic impact
on predator guilds and ecosystem processes:
apex predator extinctions, land use and climate change
Marianne Pasanen Mortensen
Department of Zoology
Stockholm University
2013
Anthropogenic impact on predator guilds and ecosystem processes:
apex predator extinctions, land use and climate change
Doctoral Dissertation 2013
Marianne Pasanen Mortensen
Department of Zoology
Stockholm University
S-106 91
Stockholm, Sweden
©Marianne Pasanen Mortensen
ISBN 978-91-7447-860-0
Cover photo by Marianne Haage
Printed in Sweden by US-AB, Stockholm, Sweden
Distributor: Department of Zoology, Stockholm University
In memory of my father
LIST OF PAPERS
I.
Pasanen-Mortensen, M., Pyykönen, M. & Elmhagen, B. (2009) Where lynx prevail,
foxes will fail – limitation of a mesopredator in Eurasia. Global Ecology and
Biogeography. 22, 868-877.
II.
Pasanen-Mortensen, M. & Elmhagen, B. One continent, two ecosystem states? Land
cover effects on mesopredator abundance in the presence and absence of apex predators.
Submitted manuscript.
III.
Khalil, H., Pasanen-Mortensen, M. & Elmhagen, B. The relationship between wolverine
and larger predators, lynx and wolf, in a historical ecosystem context. Conditionally
accepted manuscript.
IV.
Pasanen-Mortensen, M., Elmhagen, B., Lindén, H., Andrén, H., Bergström, R.,
Wallgren, M., van det Velde, Y. & Cousins, S. A. O. Can recolonizing apex predators
reclaim their ecosystem function? Impact of land use and climate change on intraguild
interactions. Manuscript.
Copyright paper I – John Wiley & Sons
ABSTRACT
Humans affect ecosystems by changing species compositions, landscape and climate. This
thesis aims to increase our understanding of anthropogenic effects on mesopredator
abundance due to changes in apex predator status, landscape and climate. I show that in
Eurasia the abundance of a mesopredator, the red fox (Vulpes vulpes), is limited top-down by
the Eurasian lynx (Lynx lynx) and bottom-up by winter severity. However, where lynx has
been eradicated, fox abundance is instead related to bottom-factors such as summer
temperature, productivity and cropland (paper I, II). Fox abundance was highest when
croplands constituted 25% of the landscape (paper II). I also project red fox abundance in
Sweden over the past 200 years and in future scenarios in relation to lynx density, land use
and climate change. The projected fox abundance was highest in 1920, when lynx was
eradicated and the proportion of cropland was 22%. In 2010, when lynx had recolonised, the
projected fox abundance was lower than in 1920, but higher than in 1830. Future scenarios
indicated that lynx abundance must increase in respond to climate change to keep fox at the
same density as today. The results suggest a mesopredator release when lynx was eradicated,
boosted by land use and climate change, and that changes in bottom-up factors can modify the
relative strength of top-down factors (paper IV). From 1846-1922, lynx, wolverine (Gulo
gulo) and grey wolf (Canis lupus) declined in Scandinavia due to persecution; however I
show that the change in wolverine abundance was positively related to the changes in lynx
and wolf abundance. This indicates that wolverine is subsidized by carrions from lynx and
wolf kills rather than limited top-down by them (paper III). This thesis illustrates how
mesopredator abundance is determined by a combination of top-down and bottom-up
processes, and how anthropogenic impacts not only can change the structures of predator
guilds, but also may modify top-down processes through changes in bottom-up factors.
Keywords: Mesopredators, apex predators, top-down, bottom-up, interspecific killing, red
fox, Eurasian lynx, grey wolf, wolverine, productivity, winter severity, cropland.
ECOSYSTEM PROCESSES
Bottom-up and top-down processes
An ecosystem is an entity of biotic and abiotic factors that are interrelated (Tansley 1935).
Theory predicts that within an ecosystem, the number of trophic levels, and the biomass on
each trophic level, is determined by bottom-up and top-down processes (Hairston, Smith &
Slobodkin 1960; Fretwell 1977; Oksanen et al. 1981). The fundamental bottom-up factor is
the potential productivity of the ecosystem - the maximum primary gross productivity (i.e. the
rate at which photosynthesis occur) that can be generated by the ecosystem (Oksanen et al.
1981). If the potential productivity is low, only plants persists in the ecosystem (Oksanen et
al. 1981; Oksanen & Oksanen 2000). However, if the potential productivity is high, plant
biomass is high, and herbivores can also persist. The higher the potential productivity is, the
higher the herbivore biomass will be. Concurrently, as herbivores consume the surplus of
plants, they limit plant biomass top-down and keep it at a constant level regardless of the
potential productivity. Herbivore biomass, however, increases with potential productivity.
There is thus an interaction of bottom-up and top-down processes, which limits plants as well
as herbivores (Oksanen et al. 1981; Oksanen & Oksanen 2000). However, many ecosystems
are productive enough to also support a third trophic level - predators. The predators consume
the surplus of herbivores and predator biomass is thus limited bottom-up, increasing with
potential productivity, while predators simultaneously limit herbivore biomass top-down and
keep herbivores at a constant level. By limiting herbivores, predators also have an indirect
impact on plants, releasing them from top-down limitation (Oksanen et al. 1981; Oksanen &
Oksanen 2000). Thus, bottom-up and top down processes works in concert in an ecosystem,
determining the biomass at different trophic levels (Fretwell 1977; Oksanen et al. 1981;
Hunter & Price 1992; Power 1992; Oksanen & Oksanen 2000).
Predator interactions
Species within the same trophic level can be grouped into guilds, based on their food
resources and methods of foraging. As species within a guild share food resources,
competition between them can arise (Root 1967; Simberloff & Dayan 1991). Competition
over shared resources can be exploitative or through interference. Exploitative competition is
an indirect process where the use of a resource by one species limits the access of the resource
for the other species, while interference competition implies direct confrontations, such as
fighting (Park 1962).
Within predator guilds, interference competition can have a lethal outcome, and is termed
interspecific killing or intraguild killing (Palomares & Caro 1999). Intraguild predation
implies that some energy is gained from the competitor by consuming it (Polis, Myers & Holt
1989). However, among mammalian predators consumption is not always involved
(Palomares & Caro 1999; Donadio & Buskirk 2006), why the term interspecific killing might
be more useful in many cases.
Relative body size of the predators is of major importance for interspecific killing among
mammals (Palomares & Caro 1999; Donadio & Buskirk 2006). Although packs of predators
can kill solitary predators that are larger than the individuals of the pack, and adults of smaller
species can kill juveniles of larger species, large predatory species generally kills smaller ones
(Palomares & Caro 1999). But as the difference in body size between species increases,
dietary overlap decreases, and the benefit for the larger predator to kill the smaller one
probably decreases. At the other hand, as the difference in body size decreases, the risk of
being injured probably increases also for the larger species. Most interspecific killing
therefore occur when the larger predator weighs 2-5.4 times more than the smaller predator
(Donadio & Buskirk 2006).
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Apex predators and mesopredators
Apex predators are often considered to be large predators and mesopredators to be midsized
predators. However, the terms apex predator and mesopredator are context dependent, and
related to the trophic function and to the size of other predators that are present in the
ecosystem (Prugh et al. 2009; Ritchie & Johnson 2009).
Apex predators hold the top position in the food web, and limit other species within the
ecosystem, both its prey species by predation, and smaller predators by interspecific killing
(Elmhagen et al. 2010; Estes et al. 2011). Apex predators are large in relation to other
predators in the ecosystem, but can be small in relation to apex predators in other ecosystems.
If a larger predator is introduced, the apex predator can be submerged to the role of
mesopredator (Roemer, Donlan & Courchamp 2002). Also, several apex predators can exist
within the same ecosystem (Ritchie et al. 2012). This can occur when diets and habitat use of
the predators differs (Schmidt et al. 2009).
Mesopredators holds an intermediate position in the food web, where they are limited topdown by apex predators (Ritchie & Johnson 2009; Elmhagen et al. 2010). They seem to avoid
habitats utilized by apex predators, or adapt activity pattern to avoid encounters with apex
predators (Fedriani, Palomares & Delibes 1999; Thompson & Gese 2007; Bischof et al.
2014). This indirect effect of apex predator on mesopredators may add to the direct limiting
effect of killing (Ritchie & Johnson 2009; Roemer, Gompper & Valkenburgh 2009). A
species that is a mesopredator in one ecosystem can be apex predator in another ecosystem if
larger predators are absent (Ritchie & Johnson 2009; Roemer, Gompper & Valkenburgh
2009). Further, there can be several mesopredators within the same ecosystem which interact
with each other through interspecific killing (Ritchie & Johnson 2009; Levi & Wilmers 2011;
Ritchie et al. 2012; Bischof et al. 2014).
ANTHROPOGENIC IMPACT
Apex predator extinctions and cascading effects
A trophic cascade occurs when a higher trophic level has an indirect effect on a lower trophic
level, mediated by a trophic level in-between (Carpenter, Kitchell & Hodgson 1985; Estes et
al. 1998; Gilman et al. 2010). Since apex predators limit herbivores as well as mesopredators,
they can initiate trophic cascades along two routes in an ecosystem. In one route they limit the
herbivores that they prey on, and thereby indirectly affect the abundance of plants on which
the herbivores feed. In the other route they limit mesopredators and thereby indirectly affect
the abundance of smaller herbivores, i.e. the prey of mesopredators, and the plants that the
small herbivores feed on (Elmhagen et al. 2010). Therefore, extinctions and reduction of apex
predators can have extensive cascading effects on the ecosystem, and there are many
examples of this from terrestrial as well as aquatic ecosystems all over the world (Estes et al.
2011; Ripple et al. 2014).
Loss of apex predators can cause a mesopredator release, i.e. an increase of mesopredator
abundance as mesopredators are no longer limited top-down (Soulé et al. 1988). This can
result in higher rates of predation in smaller prey species (Berger, Gese & Berger 2008),
decline of prey populations (Palomares et al. 1995) and even extinction of prey species (Soulé
et al. 1988). Apex predators, even if introduced, can also limit introduced mesopredators
which otherwise can have negative effect on native wildlife (Johnson, Isaac & Fisher 2007;
Rayner et al. 2007). When herbivores are released from predation they can reach higher
densities as well as utilize habitats that earlier were avoided due to predation risk (Creel et al.
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2005). This can have negative effects on vegetation and on other species that are related to the
vegetation (Ripple & Beschta 2004).
Because of their impact on ecosystems, apex predators have sometimes been suggested to be
keystone species (Sergio et al. 2008), i.e. species that are important in structuring ecological
communities (Paine 1969). However, the effect of apex predators is context dependent and
can be affected by factors such as carrying capacity and food web structure, and they do
therefore not always function as keystone species (Sergio et al. 2008). For example, trophic
cascades can be relaxed in ecosystems with many predators (Finke & Denno 2004; Bruno &
O'Connor 2005).
Land use
Homo sapiens is an ecosystem engineer, i.e. an organism that can maintain or alter a habitat or
even create new habitats (Jones, Lawton & Shachak 1994; Laland, Odling-Smee & Feldman
2001). Humans have for example transformed 40% of the Earth´s surface into croplands and
pastures, which are used for food production. Large areas of forests have therefore been lost
globally, while many of the remaining forests are fertilized, drained or managed in other ways
to increase the wood biomass (Foley et al. 2005). Changes from natural land cover to
anthropogenic land cover have globally resulted in a decrease of net primary production.
However, land use does not always decrease productivity - intensive agriculture can increase
the net primary productivity of the natural land cover (Haberl et al. 2007).
Another consequence of anthropogenic land use is that habitats are lost or split up into
smaller areas more or less isolated from each other, a process known as fragmentation, which
impacts biodiversity as well as the abundance and distribution of species (Fahrig 2003). This
is expected to have negative effects on species that for example are habitat specialists or less
mobile (Ewers & Didham 2006). Fragmentation can also have a negative effect on apex
predators and cause mesopredator release, with following decrease and extinction of local
prey populations (Crooks & Soule 1999). Habitat generalist may even gain from
fragmentation, as they use different habitats in the landscape (Andrén 1992; Andrén, Delin &
Seiler 1997). Nevertheless, generalist mesopredators that benefit from anthropogenic land use
changes can limit generalist prey species that also are gained by anthropogenic land use
(Eagan et al. 2011). Further, apex predator persecution can be related to land use and lead to
eradication of apex predators and mesopredator release (Elmhagen & Rushton 2007).
Climate
While land use change is expected to have the largest global impact on biodiversity over the
coming 100 years, climate change is right behind and is expected to have particularly high
impact at high latitudes (Chapin III et al. 2000). The global warming over the past century
seem to be caused by a combination of anthropogenic and natural factors (Stott et al. 2000).
Over this period, temperate species have increased in abundance and expanded their
distribution range, while polar species have decreased in abundance (Parmesan & Yohe
2003).
Earlier climate changes in the history of Earth altered the distribution and abundance of
species, which led to new communities and new biotic interactions. Experiments and models
indicate that this may happen due to present-day climate change as well, resulting in for
example new predator-prey relationships (Blois et al. 2013).
Over the period of 1982-1999, when a noteworthy climate change took place, the global net
primary productivity (i.e. the energy produced by plants that can be used by higher trophic
levels) increased with 6%. However, there were regional differences; net primary productivity
increased in 25% of the vegetated areas of the Earth and decreased in 7 % of the vegetated
areas (Nemani et al. 2003). Primary production can be related to the impact of apex predators
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on herbivores and mesopredators, and to the strength of tropic cascades (Elmhagen &
Rushton 2007; Melis et al. 2009; Ritchie et al. 2012; Ripple et al. 2014). Therefore, even if
community composition in an ecosystem is not altered by climate change, the strength of
interactions and relative abundance of species may change with warming.
MESOPREDATOR AND APEX PREDATOR INTERACTIONS IN EURASIA
The red fox, Vulpes vulpes, is the most widespread canid in the world, with a distribution
range covering the entire northern hemisphere, except from Iceland, the islands of the Arctic
Ocean, parts of Siberia and extreme desserts. It has also been introduced to Australia and New
Zeeland (Macdonald & Reynolds 2008). The red fox is a medium sized omnivore, feeding on
fruit, invertebrates, mammals and birds. They kill prey up to about 3.5 kg, but scavenge on
carcasses of larger mammals (Macdonald & Reynolds 2004). Rodents, especially voles,
constitute a large part of the diet in many areas of Europe (Sequeira 1980; Lindström 1989;
Jȩdrzejewski & Jȩdrzejewska 1992; Panek & Bresiński 2002; Sidorovich, Sidorovich &
Izotova 2006; Dell'Arte et al. 2007).
The red fox can limit game species such as grouse, hare and roe deer (Lindström et al. 1994;
Jarnemo & Liberg 2005). When roe dear density is high, the red fox seem to specialize on roe
deer fawns, while at low roe deer density they function as a generalist (Panzacchi et al. 2008).
The red fox also interfere with smaller predators. Small mustelids are being killed or predated
on by the fox (Lindström et al. 1995; Dell'Arte et al. 2007; Carlsson et al. 2010). The red fox
also have extended its distribution range in for example the Scandinavian mountains, which
has a negative impact on the already threatened arctic fox population, as it kills and
outcompete the smaller arctic fox (Tannerfeldt, Elmhagen & Angerbjörn 2002). It has also
been suggested that red fox limits the southern distribution range of arctic fox (Hersteinsson
& MacDonald 1992).
In many ecosystems, the red fox is a mesopredator which interfere with and is limited by
larger predators belonging to the family Felidae (Fedriani, Palomares & Delibes 1999;
Helldin, Liberg & Glöersen 2006; Elmhagen & Rushton 2007; Elmhagen et al. 2010) and
Canidae (e.g. Sargeant & Allen 1989; Johnson & VanDerWal 2009; Letnic et al. 2011; Levi
& Wilmers 2011). The Eurasian lynx is a large predator native to the Nordic countries,
Russian boreal forest belt and central Asia (Nowell & Jackson 1996; Breitenmoser et al.
2008). While historically present in large parts of Europe, a combination of deforestation,
reduction of ungulate populations and persecution, the Eurasian lynx is today lost from
southern Europe (Breitenmoser et al. 2008). The most important prey are small ungulates, but
the Eurasian lynx take smaller prey such as hares where ungulates are scarce or absent
(Nowell & Jackson 1996; Breitenmoser et al. 2008). It is well documented that the Eurasian
lynx kills red foxes without eating them, an indication that lynx kills foxes to decrease
competition (Sunde, Overskaug & Kvam 1999; Helldin, Liberg & Glöersen 2006). In areas
with limited access of prey, lynx however predates on foxes (Mattisson et al. 2011a).
It has been suggested that the red fox is limited by lynx, but that the impact depends on the
bioclimatic productivity. Where lynx abundance is high relative to ecosystem productivity,
the red fox is limited by lynx and fox abundance does not respond to differences in
productivity. However, where lynx abundance is low relative to productivity, red fox
abundance increase with productivity (Elmhagen et al. 2010).
There are two larger canids that occur sympatric with the red fox in Eurasia - the golden
jackal (Canis aureus) and the grey wolf (Canis lupus). The diets of golden jackal and red fox
overlap to a high extent (Lanszki, Heltai & Szabó 2006), which increases the risk for
interference competition (Donadio & Buskirk 2006). As the wolf mainly feed on large
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ungulates (Mech & Boitani 2004), the diet overlap between fox and wolf is smaller. However,
little is known about interference between the red fox and these two predators in Eurasia.
Remains of red foxes in golden jackal scat have been reported a few times. However, it is not
known whether these foxes were killed by jackals or eaten from carrions (Lanszki, Heltai &
Szabó 2006). Neither does it exclude that jackals kills foxes, as they do not necessarily
consume them if they kill them.
In Sweden, historical decline and eradication of Eurasian lynx (Lynx lynx) and grey wolf
caused a mesopredator release of red fox (Elmhagen & Rushton 2007). Also, the dingo (Canis
lupus dingo) seems to limit red fox abundance in Australia (Johnson & VanDerWal 2009;
Letnic et al. 2011). However, in North America, the grey wolf (C. lupus) has an indirect
positive effect on red fox, by limiting coyotes (Levi & Wilmers 2011). It is therefore not clear
whether the grey wolf and the golden jackal are apex predators in relation the red fox in
Eurasia.
The wolverine, Gulo gulo, is a large opportunistic carnivore scavenger, preying on for
example ungulates, hares, ground squirrels, birds, voles and lemmings (Pasitschniak-Arts &
M. 1995). It is also an opportunistic scavenger, utilizing carrions from prey killed by Eurasian
lynx and grey wolf (Dijk et al. 2008; Mattisson et al. 2011a; Mattisson et al. 2011b; Koskela
et al. 2013). However, in North America, grey wolves have been reported to kill wolverines
(White et al. 2002; Krebs et al. 2004). It is therefore uncertain what net effect the grey wolf
has on wolverines.
OBJECTIVES
The objectives of my thesis were to investigate how mesopredator abundance is limited by
bottom-up and top-down factors, and to explore mesopredator abundance in relation to
anthropogenic induced changes in apex predator status, land use and climate. Therefore, in the
first paper (Paper I) we investigated red fox density at a continental scale in relation to three
apex predators - the Eurasian lynx, the grey wolf, and the golden jackal - and in relation to
different bottom-up factors - winter severity, summer temperature, primary production, tree
cover and human density (Fig. 1). We also investigated differences in bottom-up impact in the
presence and absence of apex predators. In the second paper (Paper II) we explored the effect
of land use on red fox abundance in the presence and absence of the Eurasian lynx. In the
third paper (Paper III) we investigated whether wolverine was positively or negatively related
to the historical decline and eradication of Eurasian lynx and grey wolf in Sweden and
Norway, and in relation to relative snow depth, land use and human density of study sites. In
the fourth paper (Paper IV) we projected red fox abundance in south-central Sweden in the
past, present and future, to explore how anthropogenic changes in apex predator status
(Eurasian lynx), land use and climate impact mesopredator abundance, and to explore how
changes in bottom-up factors affect apex predator impact on mesopredators.
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Fig. 1. Network of top-down and bottom-up factors that are assumed to directly or indirectly
impact red fox abundance in Eurasia.
METHODS
Studies at continental scale
For the studies of ecosystem processes at the continental scale (Paper I, II), we collected
published data on red fox density from 111 different sites in Europe and northern Eurasia
(Fig. 2). We assessed presence-absence of potential apex predators - Eurasian lynx (Paper I,
II), grey wolf (Paper I) and golden jackal (Paper I) - from each paper or report and from
published descriptions of distribution range of each apex predator at the period when each red
fox survey was conducted. As the golden jackal only was present at two of the sites, we
grouped it together with grey wolf as “Canis”.
We used remote sensing data from online databases in geographic information system to
assess bottom-up factors in a buffer zone of 10 km (314 km²) around each red fox site (Paper
I, II). We used a yearly mean of the fraction of photosynthetically active radiation (FPAR) to
measure net primary productivity (Yang et al. 2006) in each buffer zone (Paper I, II). As
FPAR measures the ratio of radiation at 0.4–0.7 absorbed by the vegetation, it reflects the
energy absorption capacity of vegetation (Myneni et al. 2002). To assess winter severity in
each buffer zone, we used information on snow depth and mean temperatures for DecemberFebruary. These variables were strongly correlated, so we reduced multicollinearity by a
principal component analysis. The first principal component was used as a measure of winter
severity in the analyses (Paper I, II). Mean temperatures for June-August were used to
represent summer temperatures (Paper I, II). We also assessed human density (Paper I, II),
tree cover (Paper I) and the proportion of cropland (anthropogenic open habitat), grassland
(semi-natural and natural open habitats) and a gradient of openness (anthropogenic, seminatural and natural open habitats) (Paper II) in each buffer zone.
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Fig. 2. Red fox study sites and density of red
fox in presence (black dots) and absence
(white dots) of Eurasian lynx.
Studies at regional and local scale
To investigate whether there was a positive or negative relationship between wolverine and
the two larger predators Eurasian lynx and grey wolf, we used historical hunting bags from
Norwegian and Swedish counties in 1846-1922 (Paper III). As data on bottom-up variables
were not available for this time period, we used present-day remote sensing data as a proxy.
We could do this as we did not investigate the change over time in bottom-up variables, but
only the relative conditions between counties, which we assumed to be constant over time.
We included April snow depth, proportion of cropland and productivity (FPAR) as bottom-up
variables, all assessed from remote sensing data.
To project historical (1830 and 1920), present (2010) and future (2050) red fox abundance
and analyse how changes in land use and climate impact top-down processes, we
implemented a two-step model building (Paper IV, Fig. 3). In the first step we analysed the
impact of Eurasian lynx, winter temperatures (December-February) and land use (cropland
and other open habitats) on red fox density in present-day Finland and south-central Sweden,
in 106 squares of 50x50 km. We used data on species abundance from wildlife triangles and
remote sensing data to assess the bottom-up factors within each square. In the second step we
created models for lynx density, land use and winter temperatures in 1830, 1920 and 2010 in
the Norrström Drainage Bassin in south-central Sweden. We used historical hunting bags and
present-day data from authority lynx surveys to model historical and present-day lynx density.
To model land use we used cadastral maps from 1897-1901 together with soil and bedrock
maps. Present day land use was assessed from remote sensing data. We used temperature
stations from 1980-2000 together with information on elevation, latitude and distance to the
sea to model winter temperatures. We then used the model derived from the first step and the
data derived from the second step to project red fox abundance in Norrström Drainage Bassin
in south-central Sweden. For future scenarios with different lynx density we assumed a
continued global warming.
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Fig. 3. The two steps to develop a model of red fox abundance in Norrström Drainage Bassin. In
the first step (left graph) the effects of top-down and bottom-up variables on red fox abundance
was analysed. In the second step (right graph) top-down and bottom-up variables for Norrström
Drainage Bassin in 1830, 1920 and 2010 were modeled. Data on present-day land cover was
assessed from remote sensing data. Information from these two steps was used to project red fox
abundance at the different time steps, as well as for future scenarios.
RESULTS AND DISCUSSION
Although earlier studies have investigated relationships between mesopredators abundance
and either top-down or bottom-up factors on a continental scale (Bartoń & Zalewski 2007;
Letnic et al. 2011), no studies until now have investigated the combined effect of bottom-up
and top-down factors on mesopredators at large scale. We showed that there was a combined
effect of top-down and bottom-up factors on red fox abundance at a continental scale (Paper I,
Fig. 4). Winter severity had a negative effect on red fox abundance, and our results therefore
supports theory that red fox is limited by winter climate (Hersteinsson & MacDonald 1992;
Bartoń & Zalewski 2007). However, also presence of Eurasian lynx had direct negative
impacts on red fox density (Paper I). Furthermore, lynx mediated a negative effect of winter
severity and tree cover on red fox, indicating that lynx are mainly present in forested areas
with harsh winters. There was, however, no direct effect of tree cover on red fox abundance.
An important finding was also that the presence of canids - mainly grey wolf but also golden
jackal - was not related to red fox abundance. This suggests that the grey wolf does not have a
significant effect on red fox abundance at a continental scale, while the result is more
uncertain for the golden jackal due to the small sample size of this species (Paper I). As
Eurasian lynx, but not the canids had a significant impact on red fox, we investigated the
impact of bottom-up factors only in the presence and absence of lynx (Paper I, II). We found
that within the distribution range of lynx, winter severity was the only bottom-up factor
significantly limiting red fox abundance. However, outside the distribution range of lynx, red
fox abundance was positively related to summer temperature, human density and yearly
productivity (Paper I). Also, outside the distribution range of lynx, red fox abundance was
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related cropland, indicated by a humpbacked shaped relationship (Paper II). Red fox reached
the highest abundance when
Fig. 4. Factors that affect red fox abundance in Eurasia. There was a direct negative effect of
Eurasian lynx and winter severity, as well as an indirect negative effect of winter winter severity
and tree cover, mediated through lynx. The canid species (grey wolf and golden jackal) affect
red fox abundance. Single-headed arrows represent directed relationships and double-headed
curved arrows represent correlated errors. Paths significant at the 0.05 level are indicated by
solid arrows, and insignificant paths are indicated by dotted arrows. The path coefficients are
standardized, residual errors are given for each variable, and d.e. = deviance explained.
cropland covered about 25% of the landscape. Red fox abundance thus seems to be boosted
by anthropogenic land use in absence of lynx. Our result is consistent with a study from
Finland, showing that the highest red fox abundance is reached when 20-20% of the landscape
is covered by cropland. This probably provides foxes with high access to prey in fields but
also access to breeding habitats in forest (Kurki et al. 1998). We also found a negative effect
of grassland outside the distribution range of lynx, and we suggest that this is caused by low
rodent density in grasslands (Paper II).
In Norway and Sweden, the decline of wolverine, Eurasian lynx and grey wolf was
ultimately a result of anthropogenic persecution; however, these predators did not decline at
the same rate (Paper III). When accounting for variation in land use and snow depth, a
positive relationship between wolverine and lynx remained. Our model indicated that slow
rate of decrease in lynx also led to a slow rate of decrease in wolverine. As lynx was
negatively affected by land use, there was also a mediated negative effect of land use on
wolverine. Further, year to year fluctuations of wolverine was positively related to year to
year fluctuations in grey wolf. These results support theory that wolverine is positively
affected by grey wolf and lynx, as these provides carrions for the wolverine (Dijk et al. 2008;
Mattisson et al. 2011b). The Eurasian lynx and the grey wolf therefore do not function as
apex predators on wolverines in this ecosystem, under the circumstances investigated here
(Paper III).
In a world that is changing fast due to anthropogenic impact on land use and climate, it is
important to understand how changes in bottom-up processes modify top-down processes.
Our projection of mesopredator abundance over time can contribute to the understanding of
this, as well as give an insight in historical ecosystem composition (Paper IV). Our models for
Norrström Drainage Basin suggested that in 1830, the proportion of cropland was lower than
today, winters were colder and lynx density was high. The projected red fox abundance was
therefore lower than today. In 1920, red fox abundance reached high density, as lynx were
9
eradicated and croplands covered 22% of the landscape (Paper IV), which is optimal for red
fox (Paper II). In 2010, lynx had recolonised the study area and red fox density was lower
than in 1920, but higher than in 1830 (Paper IV). Future scenarios in which the winter
temperature was 1.5°C higher than today, suggested that if red fox abundance is to be kept at
the same level as today, the lynx population should be twice as large as today. If lynx density
is kept as today, red fox abundance will increase. This illustrates that as bottom-up factors
changes in an area, the impact of top-down processes is also modified (Paper IV).
CONCLUSIONS
Altogether, the results in this thesis are in line with theory of bottom-up and top-down
impact on mesopredators (Crooks & Soule 1999; Elmhagen et al. 2010). When apex predators
are present, they limit mesopredators top-down and diminish mesopredator respond to
bottom-up factors. However, when functional apex predators are absent, mesopredators are
released from top-down control and increase in abundance as a response to bottom-up factors.
This implies that the red fox function as a mesopredator in presence of lynx, and as an apex
predator where the lynx has been eradicated (Paper I, II). Furthermore, the Eurasian lynx and
the grey wolf does not function as apex predators in relation to the wolverine, but rather
subsidize the wolverine through increased food access (Paper III). The results thus support
theory that predators have different trophic functions in different contexts. Finally, an
important insight from this thesis is that as anthropogenic impact on bottom-up factors, e.g.
land use and climate, alters ecosystems towards a state with higher carrying capacity for
mesopredators, the relative impact of apex predators is weakened. To maintain the same
relative impact of apex predators on mesopredators and prevent increased mesopredator
abundance, apex predator abundance should increase (Paper IV). Whether apex predators can
increase in abundance or not depends on anthropogenic apex predator control, as well as on
carrying capacity, i.e. on natural conditions as well as direct and indirect anthropogenic
impact on prey species.
10
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15
SAMMANFATTNING
Människan har en stor inverkan på jorden och dess ekosystem genom att förändra
landskapssammansättning och klimat. Dessa förändringar kan få följder för den biologiska
mångfalden och för interaktioner mellan olika arter. Dessutom har utrotning av stora rovdjur i
många av världens ekosystem fått konsekvenser för ekosystemens struktur. Ett ekosystem kan
delas upp i en näringspyramid med olika trofinivåer, där växter utgör den lägsta trofinivån,
växtätare den mellersta trofinivån och rovdjur den högsta trofinivån. Enligt ekologisk teori så
påverkas förekomsten av olika arter i ett ekosystem genom processer nedifrån, d.v.s. tillgång
till föda, och uppifrån, genom predation. Vidare så kan konkurrens mellan arter inom samma
trofinivå ha en begränsande effekt, då större rovdjur kan döda mindre rovdjur för att minska
konkurrensen. Större rovdjur i ett ekosystem fungerar därigenom som toppredatorer, medan
de mindre fungerar som mesopredatorer. När stora rovdjur utrotas eller minskar kraftigt i
antal kan det således få följder för förekomsten av arter på lägre trofinivåer genom en trofisk
kaskad, och detta kan ske på två olika sätt: Dels genom att stora växtätare kan öka i antal och
därmed begränsa växtbiomassan, och dels genom att mesopredatorer kan öka i antal och
begränsa antalet mindre växtätare, vilket vidare kan påverka biomassan av vissa växter.
Därmed kan minskning och utrotning av stora rovdjur förändra interaktioner mellan
organismer och påverka den biologiska mångfalden.
Denna avhandling undersöker hur människans förändring av toppredatorers förekomst,
markanvändning och klimat påverkar antalet mesopredatorer i vissa områden. Rödräven är en
vanlig mesopredator som finns spridd över en stor del av norra halvklotet. Vi undersökte hur
antalet rävar på olika platser i Eurasien (Europa och norra Asien) påverkas uppifrån av de
större predatorerna eurasiskt lodjur, varg och guldschakal, samt nerifrån av
ekosystemproduktivitet, landskapssammansättning, klimat och människotäthet. Vi fann att
vinterns hårdhet och närvaro av lodjur avgjorde täthet av räv i Eurasiaen men också att i de
områden där lodjur är utrotade så påverkas rävarna nerifrån av bl.a. sommartemperatur,
produktivitet och åkermark (artikel I, II). De högsta tätheterna av räv i frånvaro av lo nåddes
där 25 % av landskapet utgjordes av åkermark (artikel II).
Vi studerade också effekten av lodjur och varg på järv i norra Skandinavien genom att
analysera jaktstatistik från 1800- och 1900-talet för dessa tre arter. Järven är en predator som
även nyttjar kadaver från byten som fällts av andra rovdjur. Vi fann att även om nedgången av
dessa tre arter berodde på mänsklig förföljelse, så minskade antalet järvar snabbare där antalet
lodjur minskade snabbt. Dessutom var järven positivt associerad med fluktuationer i antalet
vargar. Detta indikerar att lodjur och varg inte begränsar järv uppifrån genom att fungera som
toppredatorer i förhållande till järv, utan istället påverkar järv nedifrån genom att öka
födotillgången (artikel III).
Det är inte bara antalet rovdjur som har förändrats i Skandinavien de senaste 200 åren, utan
även markanvändningen och klimatet. Vi gjorde därför en projektion av antalet rödrävar i
Mälardalen 1830, 1920 och 2010 utifrån dessa förändringar samt utforskade hur
förändringarna i landskap och klimat förändrade den effekt som lodjur har på rävar. Antalet
rävar var som högst 1920, när lodjuret hade utrotats och andelen jordbruksmark hade ökat till
22 %, samtidigt som vinterklimatet hade blivit mildare. År 2010 fanns lodjur åter i
ekosystemet och antalet rävar var färre än 1920 men fler än 1830 p.g.a. mildare vinterklimat
2010. Våra resultat tyder vidare på att förändringarna i klimat och markanvändning, där
andelen jordbruksmark har ökat till dryga 20 % av landskapet, har förändrat den relativa
effekten av lodjur, vilket innebär att det behövs fler lodjur idag än för 200 år sedan för att
begränsa antalet rävar till en viss nivå. Framtida scenarion med ytterligare förändring av
klimatet antyder att det om 50 år skulle behövas en dubbelt så stor lodjurspopulation som idag
för att behålla antalet rävar på samma nivå som idag (IV).
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Avhandlingen illustrerar hur förekomsten av mesopredatorer styrs av olika faktorer, både
uppifrån och nedifrån, och hur antropogen förändring inte bara kan förändra relativa tätheter
av predatorer men också modifiera den effekt som toppredatorer har på mesopredatorer.
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ACKNOWLEDGEMENTS
A very big thank you goes to my supervisor Bodil Elmhagen for being engaged, always
having enthusiasm and a solution for every problem; I have learned a lot from you. I am also
grateful to my co-supervisor Sara Cousins for guidance over the years.
I am thankful to all co-authors for your contributions to the papers, and to Ranga Myneni
and Arindam Samanta for contributing with productivity data. Also Anders Angerbjörn and
Ulrika Alm Bergvall in my evaluation group have been a good source of comments and
advices. I have appreciated the company of my roommates over the years, Alexandra, Jessica,
Houshuai, Alyssa and Christina, as well as meetings with the Arctic fox group and help and
advices from other colleagues at Zootis. Lina, thanks for the cakes. Marianne, thanks for the
good times and for the cover photo of this thesis.
Thanks to my friends for cheering me. Frida and Anna-Lena, I am glad to have you as my
friends.
To my family, thank you so much for your support over these years, you are invaluable.
Mother, thank you for your patience and care, I look forward to see you more often. Lene,
thank you for being there when I need it, always prepared to listen. Hanne, thanks for your
calls, they are worth a lot. Josefine, thanks for making my day every time we meet, I look
forward to share more great and fun moments with you.
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