Return of the Wolves Implications of the Role of Top Predators in Terrestrial Ecosystems for the Return of Eurasian Wolf Canis Lupus Lupus to Western Europe

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Anne M.G. Kwak Return of the wolves Implications of the role of top predators in terrestrial ecosystems for the return of Eurasian wolf Canis lupus lupus to Western Europe

Author Anne M.G. Kwak Radboud University Nijmegen E-mail: [email protected]

Education Master Biology, track Communities & Ecosystems Radboud University Nijmegen Faculty of Science Heyendaalseweg 135 6525 AJ Nijmegen Phone: 024-365 26 61 Fax: 024-355 34 50 Website: www.ru.nl/fnwi

Supervisor Prof. dr. H. (Hans) de Kroon Institute for Water and Wetland Research Radboud University Nijmegen

Date October 2013

SUMMARY

In many terrestrial ecosystems in Western Europe today, top predators are absent (Terborgh et al., 1999). Since top predators are considered to be important for the structure of ecosystems and their biodiversity, the absence of such species might have large impacts on these systems. In this thesis I want to investigate how the absence of top predators has affected terrestrial ecosystem trophic structure and biodiversity. The focus on terrestrial ecosystems comes forth from the fact that the Eurasian wolf Canis lupus lupus is currently expanding its range throughout Western Europe (Chapron et al., 2003; Randi, 2011). Here, I investigate how species like the Eurasian wolf might affect our ecosystems when they spread further, and what the implications of these effects are for the management of our ecosystems and of the Eurasian wolf.

Carnivores can be assigned the role of keystone species, where they create ecological boundaries that protect lesser competitors from exclusion (Miller et al., 2001). In this role of keystone species, carnivores are also capable of increasing plant biomass through their limiting effect on herbivore numbers, causing both plants and carnivores to flourish (Miller et al., 2001). A general pattern in terrestrial ecosystems seems to be that when top predators are absent, herbivores increase in population size, resulting in a high browsing pressure (Elmhagen and Rushton, 2007; Miller et al., 2001; Ripple and Beschta, 2004; Ripple and Beschta, 2006). This eventually leads to a lower biodiversity than in systems where predators are still present (Sergio et al., 2005). Ripple and Beschta (2006) also found that removal of top predators does not only affect the direct food chain in which the predator is present, but also other parts of the ecosystem.

So what effects can Eurasian wolves Canis lupus lupus have on ecosystems? First of all, since they are top predators, Eurasian wolves can contribute to the regulation of predator-prey relationships. Next to this they also affect the density of smaller predators (Randi, 2011). The expansion of the Eurasian wolf to western Europe may provide us with a way to passively manage and restore our ecosystems to a more natural and wild state. In each of the example areas from Europe, a wolf population will result in different effects on the present ecosystems, but it is still expected to lead to an increased biodiversity. It would also reduce the need for human interference in these systems, leading to more natural states. However, top predators like the Eurasian wolf do not only bring with them changes to ecosystems, but also evoke fear in humans either for their own safety or for that of their domestic and game animals. Management and conservation of large carnivores may thus only be successful in the long term if people can accept free ranging predators in their area. To achieve this, we will have to regulate the wolf population to address public concern, but at the same time we need to maximize population viability of these predators (Chapron et al., 2003).

To conclude, the Eurasian wolf returning to Western Europe may have very positive effects from an ecological perspective: increased biodiversity. However, we do need to consider public fear. We will have to come up with management strategies now, to build up support from the public in order to welcome back the wolf to our ecosystems.

CONTENTS

Summary 1

1 Introduction 5

2 Top-down versus bottom-up regulation of ecosystems 6 2.1 Food webs and keystone species 6 2.2 Bottom-up versus top-down ecosystem regulation 7

3 Absence of top predators 10 3.1 Importance of top predators in terrestrial ecosystems 10 3.2 Effect on the structure of ecosystems and food webs 11 3.3 Management of ecosystems lacking top predators 13

4 Current conservation issues 15 4.1 Implications for management of Eurasian wolf Canis lupus lupus 18

5 Discussion 20

6 Literature 21

MSc thesis Return of the wolves Anne M.G. Kwak

1 INTRODUCTION

There has been an ongoing discussion on top-down versus bottom-up ecosystem regulation since the 1960s (Elmhagen and Rushton, 2007; Power, 1992; Terborgh et al., 2001), when the concept of top- down regulation was first introduced by Hairston et al. (1960). The question is whether ecosystems are regulated from the top down by predators or from the bottom up by food/nutrients limitations. Most evidence for top-down regulation in ecosystems comes from aquatic ecosystems (Elmhagen and Rushton, 2007). However, mammalian predators are considered to have major influences on the trophic structure and biodiversity of terrestrial ecosystems (Hebblewhite et al., 2005; Sinclair et al., 2003; Terborgh et al., 2001).

In many terrestrial ecosystems in Western Europe today though, top predators are absent (Terborgh et al., 1999). Such ecosystems are often managed by humans to keep them in a certain state or to at least preserve a certain level of biodiversity. Since top predators are considered to be important for the structure of ecosystems and their biodiversity, the absence of such species might have had large impacts on these systems.

In this thesis I want to investigate how the absence of top predators has affected terrestrial ecosystem trophic structure and biodiversity. The focus on terrestrial ecosystems comes forth from the fact that Eurasian wolf Canis lupus lupus is currently expanding its range throughout Western Europe (Chapron et al., 2003; Randi, 2011). For example, for the first time in 150 years a wolf has been found in the Netherlands (NU.nl/ANP, 2013). Here, I investigate how species like the Eurasian wolf might affect our ecosystems when they increase in numbers, and what the implications of these effects are for the management of our ecosystems and of the Eurasian wolf.

To answer this question, I will first introduce the concepts of top-down and bottom-up ecosystem regulation and investigate whether or not a consensus has been reached within the discussion on which mechanism is most important. Next, I will investigate the effect of absence of top predators on terrestrial ecosystems to see how trophic structure and biodiversity have altered. Finally, I discuss the consequences of the expansion of Eurasian wolf to Western Europe on our ecosystems and I will link this to the implications this expansion has for management of this species and our systems.

Radboud University Nijmegen | 5 MSc thesis Return of the wolves Anne M.G. Kwak

2 TOP-DOWN VERSUS BOTTOM-UP REGULATION OF ECOSYSTEMS

2.1 FOOD WEBS AND KEYSTONE SPECIES Ecosystems can be described as food webs: several food chains linked together into a complex web of interactions between organisms (Begon et al., 2003; Jordán, 2009; Jørgensen, 2009). Using a food web approach allows us to investigate the importance of different species from an ecological perspective. While such food webs can be very large and complex, a ‘small-world’ structure seems to be common in nature: most species only interact with a small number of other species, while the connectivity of food webs as a whole is maintained by a few species that interact with a large number of other species (Jørgensen, 2009). Extinction of such major interactors may break coevolved relationships among co- adjusted sets of species and may thus significantly harm ecosystem integrity (Jordán, 2009). This concept of a ‘small-world’ with major interactors forms the basis for the idea of keystone species: small-world networks are robust to random loss of nodes (species), but they are vulnerable to attacks targeting highly connected nodes (keystone species) (Jørgensen, 2009).

When looking at the interactions between species present in food webs, one might have an initial idea of its workings. One would expect removal of predators to lead to an increase in prey density, or removal of a competitor species to lead to an increase in abundance in the species it competes with. However, this is not always the case. Occasionally, removal of a predator leads to a decrease in prey species or removing a competitor causes a decrease in the abundance of its competitors. These effects occur when direct effects in a food web are less important than indirect effects (Begon et al., 2003).

These indirect, ‘unexpected’ effects are a common occurrence in nature. They refer to the propagation of perturbations through one or more trophic levels, so that consequences are felt in organisms that may seem far removed from the subjects of perturbation (Begon et al., 2003; Terborgh, 1988). Species that show such effects in food webs upon their removal are usually keystone species (Begon et al., 2003). The term ‘keystone species’ was first introduced in 1969 by R.T. Paine as a species which presence is crucial in maintaining the organization and diversity of their ecological communities which makes it implicit that they are exceptional in their importance (Mills et al., 1993). They show disproportionally large effects relative to their abundance and are by definition single objects on which the forces keeping a community intact are concentrated (Payton et al., 2002). Removal of keystone species leads to extinction or large changes in abundance of several species (both through direct and indirect pathways), resulting in a community with a very different species composition and, to us, different physical appearance (Begon et al., 2003). So keystone species are not necessarily abundant

Figure 1. Expected distribution of community importance values (percent of species lost from a community upon removal of a given species) for a hypothetical community based on the keystone species model. Axes are arbitrarily scaled to demonstrate the general scale of the distributions. Adapted from Mills et al. (1993).

Radboud University Nijmegen | 6 MSc thesis Return of the wolves Anne M.G. Kwak in a community, but they do exert strong control on the structure of a community by their pivotal ecological roles or niches. The keystone role of species is not caused by a species-specific property, but is particular to the defined environmental setting, current species associations and responses of other species: the keystone status of species is context-dependent (Mills et al., 1993; Payton et al., 2002). The keystone role can also be adopted by different organisms and cannot be predicted on the basis of life-history traits, only by examining the function of species (Payton et al., 2002). This concept has contributed to ecology and conservation by drawing attention to differing interaction strengths in community food webs and by showing that only few species have large effects on the composition or structure of communities (figure 1)(Mills et al., 1993).

While Paine (1969) originally restricted the use of his term ‘keystone species’ to predators, other species can also have this role (see table 1 for an overview of keystone categories). For example, removal of a certain plant in a certain community could lead to changes in density and extinctions in other species (Begon et al., 2003). Nowadays, it is widely accepted that keystone species can occur at any trophic level (Begon et al., 2003). An example of a keystone species occurring at a mid-trophic level is the lesser sandeel in the North Sea (Frederiksen et al., 2006). In this system, seabirds depend on the larvae of the lesser sandeel, while the fish themselves depend on plankton. If the lesser sandeel is removed in this system, seabirds would not have enough food, while plankton could start to thrive, possibly affecting other species in the food web. So even though this system is regulated from the bottom up through plankton abundance (Frederiksen et al., 2006), the keystone species is present in the mid-trophic level.

Table 1. Four types of keystone species based on their functional role as defined by Payton et al. (2002). KEYSTONE CATEGORY DESCRIPTION Organisms controlling ‘Classic’ keystone species; promote coexistence by reducing competition potential dominants by other species. Resource providers Provide vital resource(s) to a range of organisms at a time of scarcity (often seasonally); does not have to be particularly abundant. Mutualists Elimination of one results in demise of the other; can also occur among groups (‘group mutualism’); most convincing cases are those where several species depend on a single mutualist; removal of one can result in community collapse if the other has strong interactions with the rest of the community. Ecosystem engineers Modify physical environment so that it releases resources for other species; habitat created by these species is otherwise unavailable; predation and engineering are not always distinguishable.

2.2 BOTTOM-UP VERSUS TOP-DOWN ECOSYSTEM REGULATION One might consider ecosystems with keystone predators (the first category in table 1) as top-down regulated systems and ecosystems with keystone category ‘resource providers’ (table 1) as bottom-up regulated systems (see table 2 for a comparison between both types of regulation). In top-down regulated systems, predation (also anthropogenic, e.g. hunting and fishery) controls community organization due to its limiting effect on herbivores, which in turn limit plants that in turn limit nutrient levels (Begon et al., 2003; Power, 1992). The world can be called “green” in this top-down situation: removing herbivores (through predation) does increase plant biomass, but adding limited resources does not (Power, 1992). Bottom-up regulated systems, however, are primarily controlled by resources and are thus food limited (Begon et al., 2003; Power, 1992). The removal of higher trophic levels will leave the lower levels intact, while removing the lower levels (primary producers) will cause the community to collapse (Power, 1992). Here, the world can thus be seen as “barren”: removing

Radboud University Nijmegen | 7 MSc thesis Return of the wolves Anne M.G. Kwak herbivores does not increase plant biomass, but adding limited resources does (Hairston et al., 1960; Power, 1992).

Table 2. Characteristics of bottom-up and top-down ecosystem regulation (Begon et al., 2003; Hairston et al., 1960; Power, 1992). BOTTOM-UP ECOSYSTEM REGULATION TOP-DOWN ECOSYSTEM REGULATION  Controlled by resources.  Controlled through predation.  The world is “barren”.  The world is “green”.  Resources limit primary production of  Predators limit herbivores, which in turn plants, which in turn limits herbivores, limit plants, which in turn limit nutrient which in turn limits predators. levels.  Removal of lower levels causes community  Removal of higher levels causes community collapse. collapse.

So how green is our world? In other words: are ecosystems commonly regulated from the top down or from the bottom up? This question has resulted in a controversy with a long history, starting in the 1960s when the concept of top-down ecosystem regulation was first introduced by Hairston et al. (1960). Although the words ‘top-down regulation’ were not used directly, Hairston et al. (1960) provided evidence to conclude that herbivores are seldom food limited, but most often appear to be predator limited. The theory by Hairston et al. (1960) states that biomass (fossil fuels) can accumulate in terrestrial ecosystems, because predators are keeping herbivores in check.

This view on ecosystem regulation has resulted in a discussion where some researchers state the world is ‘barren’ (adding limited resources increases plant biomass), while others see the world as ‘green’ (removing predators increases the number of herbivores which will then decrease the amount of plant biomass) (see table 3 for a selection of views). However, we also see that through the years others still are convinced that ecosystems are co-limited by both predators and resources. This is also the view that is found more often in more recent years: many ecosystems seem to have both top-down and bottom-up components, where the bottom-up components set the stage for top-down forces (Báez et al., 2006; Elmhagen and Rushton, 2007; Frederiksen et al., 2006; Terborgh et al., 2001). The level of primary productivity in these cases is influential in determining whether top-down or bottom- up control is predominant (Begon et al., 2003).

Examples of such top-down and bottom-up dualities can certainly be found in nature (Báez et al., 2006; Elmhagen and Rushton, 2007; Frederiksen et al., 2006; Terborgh et al., 2001). In this case the world resides in Figure 2. Mechanisms (curved arrows) modulating top-down and an intermediate state where consumers bottom-up forces (straight arrows) in food chains (Power, 1992).

Radboud University Nijmegen | 8 MSc thesis Return of the wolves Anne M.G. Kwak and resources co-limit plants: adding resources or removing herbivores both increase plant biomass (Power, 1992). Here, top-down forces dominate the trophic dynamics, but the food web structure is set by the bottom-up attribute of ecosystems (plant productivity) (Power, 1992). The relative efficacy of top-down versus bottom-up forces then depends in part on the efficiency with which consumers exploit their prey. This efficiency can be affected by interactions among consumers, interactions between consumers and resources and interactions between nonadjacent trophic levels. This consumer efficiency can then modify top-down forces in food webs through different routes (see also figure 2). Whether one route or another is present in a community depends on that community (Power, 1992).

We can thus conclude that there seems to be a consensus that most ecosystems are co-limited by both resources and predation, for which we can certainly find evidence in nature.

Table 3. Views on the relative importance of top-down and bottom-up regulation in food webs in decreasing order of the relative strength attributed to top-down forces. Edited from Power (1992). TOP-DOWN LIMITATION Menge and Sutherland (1976) Food webs are filled with omnivores, with larger species capable of eating most smaller species. Most trophic levels below the top are potentially predator limited. Physical disturbance shortens food chains. Hairston et al. (1960) Predators regulate herbivores, releasing plants to attain densities at which they become resource limited. Detritivores and herbivores are predator limited; plants and predators are resource limited. Fretwell (1977); Fretwell (1987); Oksanen et al. (1981) Food chains can have fewer or more than three trophic levels. Top trophic levels and those even numbers of steps below them are resource limited; trophic levels odd numbers of steps below the top are predator limited. CO-LIMITATION BY PREDATORS AND RESOURCES McQueen et al. (1989) Trophic cascades produced by top-down forces in limnetic lake food webs attenuate before reaching plants. Arditi and Ginzburg (1989); Getz (1984) Interference (broadly defined) among predators prevents their efficient exploitation of resources, so that prey populations, though reduced by exploitation, can increase with increases in their own resources. Mittelbach et al. (1988) Predators require different resources as juveniles than as adults. This decoupling prevents predator populations from efficiently tracking resources when increases involve food of only one predator life history stage. Leibold (1989) Control of prey by consumers diminishes after initial exploitation shifts community dominance to less edible species. Sinclair and Norton-Griffiths (1984) Starvation-weakened prey become more vulnerable to predation or disease. Mittelbach et al. (1988); Power (1984); Sih (1982) Prey in spatial refuges from predation become more food limited. Báez et al. (2006); Elmhagen and Rushton (2007); Frederiksen et al. (2006); Terborgh et al. (2001) Many ecosystems show both top-down and bottom-up components, where the bottom-up components set the stage for top-down forces. BOTTOM-UP LIMITATION White (1978) Plants are not appreciably limited by herbivores except when unusually stressed (for example, by drought). All trophic levels are potentially limited by availability of food resources.

Radboud University Nijmegen | 9 MSc thesis Return of the wolves Anne M.G. Kwak

3 ABSENCE OF TOP PREDATORS

Since there seems to be some consensus on the fact that many ecosystems are both regulated from the top-down and from the bottom-up, the question arises what will happen to ecosystems when top predators are missing. If many ecosystems are indeed also regulated from the top down, how will the absence of such species affect the structure and biodiversity of ecosystems? To investigate this, we first need to know what the importance of top predators is. To do this, I focus on terrestrial ecosystems.

3.1 IMPORTANCE OF TOP PREDATORS IN TERRESTRIAL ECOSYSTEMS Top vertebrate predators are often used as flagship species by conservationists to raise (financial) support, to raise environmental awareness and to plan protected areas because of top predator charisma to the public; a method that has been criticized (Sergio et al., 2005; Sergio et al., 2006). Next to this criticism, bottom-up theories provide large carnivores with little ecological importance, since they sit on top of the food chain where they receive more than they contribute. This justifies politically- based management strategies to keep predator numbers low or to remove them completely (Miller et al., 2001). However, most researchers nowadays seem to agree that many ecosystems consist of both top-down and bottom-up control (Báez et al., 2006; Elmhagen and Rushton, 2007; Frederiksen et al., 2006; Terborgh et al., 2001) and recent research does show that top predators play an important role in conserving terrestrial ecosystems (Miller et al., 2001; Sergio et al., 2005; Sergio et al., 2006). So perhaps removing large predators or eliminating them altogether may have negative effects on ecosystems. But what is then the importance of such species?

In their role of keystone species, large carnivores can create ecological boundaries that protect these lesser competitors from exclusion (Miller et al., 2001). In this role of keystone species, carnivores are also capable of increasing plant biomass through their limiting effect on herbivore numbers, causing both plants and carnivores to flourish (Miller et al., 2001).

Seeing as carnivores give lesser competitors a chance and allow plants to flourish, this would suggest an increased biodiversity in ecosystems including top predators compared to ecosystems where such predators have been eliminated. This relationship between top predators and biodiversity was indeed found by Sergio et al. (2005) on sites where five species of raptors (goshawk Accipiter gentilis, pygmy owl Glaucidium passerinum, Tengmalm’s owl Aegolius funereus, tawny owl Strix aluco and scops owl Otus scops) were either present or absent. In the presence of these five raptor species (breeding sites; red bars in figure 3a-c), biodiversity was consistently higher than in their absence (randomly selected spatial-control sites; blue bars in figure 3a-c). This increased biodiversity was only found for sites with these top predator species, not for sites occupied by species from lower trophic levels (figure 3 taxonomic controls). Finally, efficiency of simulated protected-area systems was higher for sites including top predators than for any of the control sites (figure 3d). Hence, Sergio et al. (2005) provide us with evidence of a tight relationship between top predators and an increased biodiversity.

Top predators in terrestrial ecosystems are thus shown to be important, since they can occupy keystone roles in ecosystems, leading to the creation of ecological boundaries that allow more species to coexist in the same system. Their keystone role also causes plant species to flourish. An important relationship between top predators and higher biodiversity was also found. This might justify the use

Radboud University Nijmegen | 10 MSc thesis Return of the wolves Anne M.G. Kwak of top predators as flagship species. It is therefore not the question if top predators play an important role in terrestrial ecosystems, but rather how they play their role in trophic interactions (Miller et al., 2001) and how their absence can affect the structure of ecosystems and their food webs.

3.2 EFFECT ON THE STRUCTURE OF ECOSYSTEMS AND FOOD WEBS That top predators do have an impact on ecosystem regulation has been shown in many different regions, including the Arctic/Antarctic, many aquatic systems and some terrestrial systems (Miller et al., 2001). This section discusses the impact of removal of top predators on the structure of ecosystems and food webs. Several studies have been conducted on ecosystems where data is available from periods where top predators were still present and from periods where top predators had been reduced in numbers or had been eliminated completely (Miller et al., 2001). These kind of data allow us to see how the removal of top predators can affect these structures.

An example of such a situation is a study conducted in Zion National Park, Utah (Ripple and Beschta, 2006). Here, Zion Canyon is an area inside the national park that houses almost no cougars (Puma concolor) due to high numbers of human visitors driving the cougars away. A part of the park adjacent to Zion Canyon, North Creek drainage, acts as a refugia for cougars from outside of the park to escape hunters and thus houses a stable cougar population. This allowed Ripple and Beschta (2006) to investigate the effects of presence or absence of these predators on the ecosystem as a whole. In the area cougars predate on mule deer (Odocoileus hemionus), which in turn graze on cottonwoods (Populus fremontii): cougar  mule deer  Fremont cottonwood. In the Zion Canyon area, the number of cougars decreased with an increase in visitors, causing an increase in the number of deer present in the area. This increase in deer numbers has led to a decrease in tree recruitment due to heavy browsing pressure. Increase in deer numbers also had some indirect effects: relative abundance of Figure 3. Biodiversity estimates are higher at sites occupied by hydrophytic plants, wildflowers, amphibians, five top predators than at randomly selected sites or at sites lizards and butterflies along the streams were occupied by species from lower trophic levels (taxonomic decreased due to more bank erosion from loss controls). Red bars, breeding sites; blue bars, randomly selected spatial-control sites. Values represent averages ± 1 s.e. a) of cottonwood trees. The opposite pattern Numbers of all avian species. b) Numbers of avian species occurs in the North Creek area, where a stable classified as vulnerable. c) Numbers of tree species. d) cougar population prevents the deer Percentage of maximum attainable avian species richness in a population from overexploiting cottonwood. hypothetical system of protected areas, as estimated by gap analysis (Sergio et al., 2005).

Radboud University Nijmegen | 11 MSc thesis Return of the wolves Anne M.G. Kwak

Indirectly this led to higher numbers of hydrophytic plants, wildflowers, amphibians, lizards and butterflies along the streams in this area (Ripple and Beschta, 2006). In this system we thus see that removal of top predators led to a trophic cascade along the food chain, which resulted in a regime shift. The two study areas now show different ecosystems, due to the loss of cougars in one region and the presence of these predators in the other. It shows us that removal of top predators does not simply change trophic food chains, but it can also indirectly affect other parts of the ecosystem and can even cause regime shifts when their interactions with other species are big enough.

In the previous example, and also in other studies on for example wolves and moose, predators were able to keep their prey populations at low densities. Once these predators were removed, a high browsing pressure on plants was caused by the increasing numbers of herbivores (Ripple and Beschta, 2004; Ripple and Beschta, 2006). However, there are more ways in which predators can affect ecosystems than just through direct predation. Indirect effects (predation risk) of wolves Canis lupus in Yellowstone National Park were investigated by Ripple and Beschta (2004), to see how this can affect an ecosystem’s structure. Indirect effects are defined as changes in prey behaviour due to the presence of predators. This change in behaviour can influence other species in the food web or ecosystem as well, possibly leading to trophic cascades (Ripple and Beschta, 2004). A possible effect of the presence of wolves is that ungulates are less present in the wolves’ core territories. They try to evade areas with high wolf densities by altering their use of space and their foraging patterns to increase their chances of survival. This results in potential plant refugia in the areas with these high wolf densities, because here herbivore pressure is lower (Ripple and Beschta, 2004). Plant refugia can also be created because of behavioural changes in herbivores caused by alteration of use of space and foraging patterns according to the features of the terrain and the extent to which these features affect risk of predation: where predation risk is high (e.g. very open areas), plant refugia will be created, because herbivores will avoid these areas (Ripple and Beschta, 2004). Here, the presence of wolves and other predators thus creates the same overall effect on ecosystem structure as would be caused by direct effects of predation: in areas with more wolves, less herbivores are present, creating more opportunities for plant species to grow.

An example of the effect of removal of wolves is shown in some riparian ecosystems (Ripple and Beschta, 2004). Presence of wolves in these areas causes avoidance of these areas by ungulates. This gives several tree species (e.g. aspen, willow and cottonwood) the opportunity to grow due to less browsing pressure. This then provides beavers with food. When wolves are absent in these riparian systems, ungulate densities increase, causing a loss in woody species on which beavers and various riparian functions depend. Absence of wolves and grizzly bears in Grand Teton National Park has also resulted in an increase in browsing on willow by moose. This has led to a decrease in migratory bird species. A negative correlation was found between moose abundance and avian species richness and abundance (Ripple and Beschta, 2004). Mesopredator release has also been implicated in the absence of large carnivores (Elmhagen and Rushton, 2007), resulting in decline of bird and small vertebrate populations (Ripple and Beschta, 2004).

As we saw in section 2.2, top-down and bottom-up dualities exist in nature. An example where top- down regulation is present in interplay with bottom-up regulation is that of Scandinavian forest systems. Originally, Eurasian wolves and Eurasian lynx were the top predators of these systems, keeping in check both ungulates and mesopredators (red foxes) through predation, leading to a coexistence of multiple species of mesopredators and herbivores. The top predators in these systems reached near extinction through killings by humans. It was thought that this caused the mesopredator release of red fox that had cascade effects on the lower levels of the ecosystem. They started outcompeting Arctic fox (driving it to near extinction) and drastically reducing numbers of small game

Radboud University Nijmegen | 12 MSc thesis Return of the wolves Anne M.G. Kwak prey like grouse and hare, as well as smaller predators like pine marten (Elmhagen and Rushton, 2007). However, even though this top-down regulation was present, it was not the only thing causing a drastic change in the ecosystem. During the same period, agricultural expansion caused a shift from relatively unproductive forest landscapes to mixed agricultural landscapes. These mixed agricultural landscapes hold higher densities of prey for the red fox, leading to an increase in mesopredator release of this species. This thus shows an interplay of bottom-up and top-down effects on the trophic structure of the ecosystem (Elmhagen and Rushton, 2007). The study by Elmhagen and Rushton (2007) indeed confirmed this anecdotal evidence of a top-down bottom-up duality. They showed that rate of fox expansion was linked to the rate of agricultural expansion, just like the rate of decline in top predators. Next to this they also showed that rates of increase in red foxes were most rapid in those regions where rates of decline in top predators were highest. They thus showed that the mesopredator release effect occurred in response to declining top predator populations, but that baseline ecosystem productivity set an upper limit to the impact of this effect (Elmhagen and Rushton, 2007).

These examples show that top predators can affect the structure of terrestrial ecosystems and their food webs in a direct way through increased mortality of prey species, but that they can also change ecosystem structure through indirect effects. A general pattern in terrestrial ecosystems seems to be that when top predators are absent, herbivores increase in population size, resulting in a high browsing pressure. But absence of top predators can also result in a change in ecosystem structure through an increase in the power of bottom-up regulation. This eventually leads to a lower biodiversity than in systems where predators are still present. We also saw that removal of top predators does not only affect the direct food chain in which the predator is present, but also other parts of the ecosystem (Elmhagen and Rushton, 2007; Miller et al., 2001; Ripple and Beschta, 2004; Ripple and Beschta, 2006). Next to this we saw that in top-down bottom-up dualities the impact of top predators depends on ecosystem productivity, but they may provide a buffer against anthropogenically induced changes to the system and through this facilitate the preservation of species on lower trophic levels in productive systems (Elmhagen and Rushton, 2007). Knowing this, what does this mean for management of ecosystems that lack top predators?

3.3 MANAGEMENT OF ECOSYSTEMS LACKING TOP PREDATORS So far we have seen that large carnivores indeed play important roles in ecosystems in more than just the simple direct way of affecting demography of prey species. Top predators also change movement and activity patterns of such species. Such behavioural effects can have ecological significance. Still, carnivore control has been applied in many management solutions, with little consideration of all conditions (e.g. season, behaviour) that affect a top predator’s role in an ecosystem (Miller et al., 2001). Reducing the number of top predators in ecosystems has caused and will continue to cause a reduction in ecosystem biodiversity and will affect many organisms (Miller et al., 2001). So how should we now manage our ecosystems when we lack top predators and the important roles they fulfil in these systems?

For one, in systems where top predators are absent, prey species can still show similar responses from indirect effects, only now these effects are caused by humans. For example, humans can cause the same indirect effects on such prey species as predators. Due to sports hunting, elk avoided human contact and possible predation by humans in the same way as they would with top predators, resulting in both prey and plant refugia and similar responses in ecosystem structure (Ripple and Beschta, 2004). Also, keeping herbivore numbers low through hunting might be a solution to keep ecosystem structure in a more natural state and to conserve biodiversity of that system.

Radboud University Nijmegen | 13 MSc thesis Return of the wolves Anne M.G. Kwak

Considering their importance to terrestrial ecosystems, top predators should receive more ecological importance than they have been given by supporters of the bottom-up theory. As we saw, politically- based management to keep numbers of carnivores low or to eliminate them completely is certainly not justified (loss of biodiversity) and might have more complex effects on ecosystems than we might expect from only looking at the interactions between predator and prey. We have seen that top predators can have great influences on biodiversity and ecosystem structure in both direct and indirect ways. If we want to conserve this biodiversity in ecosystems, we either need to consider reintroducing top predators, or we as humans need to take the role of top predators upon ourselves.

Since taking this role of top predators upon ourselves is also a solution that will have to be carried out all year every year, this may not be a sustainable solution and may cost us a lot of money in the end. Even more so when we consider that effects on structure and biodiversity of ecosystems can be changed more rapidly after top predator decline through bottom-up regulation that is also present in the system. Therefore, it would be desirable to reintroduce top predators or to help range expansion of these species, so that natural, stable carnivore populations can again be realised in ecosystems. In this way, ecosystems can return to their (more) natural state and will regulate themselves, resulting in biodiversity increase, and top predators might provide a buffer against anthropologically induced changes in ecosystems (Elmhagen and Rushton, 2007).

Radboud University Nijmegen | 14 MSc thesis Return of the wolves Anne M.G. Kwak

4 CURRENT CONSERVATION ISSUES

As mentioned in the introduction, the Eurasian wolf Canis lupus lupus is showing natural range expansions throughout Western Europe (Chapron et al., 2003; Randi, 2011). As we saw in the previous sections, such top predators can have great impacts on ecosystem structure. It is therefore important to discuss possible changes such a species can cause to ecosystems where these predators have been absent for many years.

The Eurasian wolf is, like all wolf species, a very social animal. Wolves live in packs that consist of a breeding pair and their offspring, sometimes from several generations (Chapron et al., 2003). Wolves can colonize new areas by means of a dispersing individual. This dispersing wolf may also join another pack, replacing a missing breeding member. If both breeding adults in a pack die, usually this pack falls apart and leaves an empty territory suitable for recolonization by a new pack (Chapron et al., 2003). The Eurasian wolf is not a habitat-specific species: it lives wherever it can find enough food. Important is also that the wolves are tolerated by humans, otherwise they will evade such areas (Chapron et al., 2003). Since wolves are highly mobile species with juveniles capable of dispersing over hundreds of kilometres, they live in very large territories. Therefore, wolf population ranges expand well across the boundaries of protected natural areas in Europe (Randi, 2011).

So what effects can wolves have on ecosystems in general? First of all, since they are top predators, Eurasian wolves can contribute to the regulation of predator-prey relationships: they have positive cascade effects on dynamics of ungulate and plant communities. Next to this they also affect the density of smaller predators (the opposite of mesopredator release)(Randi, 2011). Both the suppression of overexploitation by herbivores and the control of mesopredator population densities can provide opportunities for more species to coexist. The Eurasian wolf may thus have the potential to restore higher levels of biodiversity in ecosystems where top predators have been absent.

Another effect the Eurasian wolf can have is that they can provide scavenger species with more biomass from carcasses during spring (Wikenros, 2011). When wolves kill more prey than they need to replenish their energy requirements, they leave biomass on their carcasses. Common scavengers like red fox (Vulpes vulpes) and raven (Corvus corax) but also more threatened species like Golden Eagle (Aquila chrysaetos) may benefit from this increase in carcass biomass (Wikenros, 2011). This is especially true in areas where hunters regulate populations but do not leave carcasses for other species to consume. The Eurasian wolf might therefore also be able to increase biodiversity in ecosystems through such indirect effects.

Knowing this, let us now investigate a hypothetical situation in which a healthy Eurasian wolf population exists in Western Europe. How would our ecosystems change in such a situation? To investigate this, a description of the current state of our ecosystems is in order. One of the most well- known natural areas in the Netherlands is the Oostvaardersplassen. This nature reserve arose in 1968 and consists of 6,000 ha of open water, marshland, wet and dry open grasslands and flowering communities with trees and shrubs (Vera, 2009). In this ecosystem, management for creating all the vegetation types mentioned above is done by animals themselves. greylag geese (Anser anser) are responsible for creating a mosaic of open water and marsh vegetation. Open grasslands on dry land adjacent to marshy areas are maintained by Heck cattle (Bos domesticus) and Konik ponies as well as red deer (Cervus elaphus)(Vera, 2009). These herbivore populations are not cared for by humans, they have been allowed to become feral. Their numbers are regulated naturally through food shortage in winter. This occurs when the numbers of herbivores exceed the carrying capacity of the area (Vera, 2005; Vera, 2009). For the sake of animal welfare however, Staatsbosbeheer, the government agency

Radboud University Nijmegen | 15 MSc thesis Return of the wolves Anne M.G. Kwak responsible for the area, does use reactive management in which animals showing behaviour indicating impending death are shot. This is done to address protest from the community (Vera, 2005; Vera, 2009).

In the Amsterdamse Waterleidingduinen, another natural area in the Netherlands used for the abstraction of drinking water, a population of fallow deer (Dama dama) has established itself. Although roe deer (Capreolus capreolus) are common in this area and cause no problems, fallow deer have a more general range of food, which causes concern for the persistence of the dune system. Next to this possible effect on vegetation, Fallow deer might be able to outcompete the roe deer in the area, similar to a process on the Hoge Veluwe where roe deer is being outcompeted by red deer (Van Breukelen et al., 2000).

The national park the Hoge Veluwe is one of the most well-known and largest natural parks in the Netherlands and has been continuously protected since 1909. It is located in the centre of the country and is made up of approximately 5500 hectares of forest, heather and drift sand (Hein, 2011). Animal species in the park include wild boar, red deer, badger, mouflon and roe deer (Hein, 2011; Smit et al., 2001). The park has a long history of grazing and the number of large herbivores is controlled by hunters (Smit et al., 2001). The park provides some major ecosystem services like wood production, supply of game (wild boar and deer), groundwater infiltration, carbon sequestration, air pollution removal, recreation (also due to the Kröller-Müller art museum located inside the area), recreational hunting and biodiversity conservation (Hein, 2011).

In both natural areas, the Oostvaardersplassen and the Amsterdamse Waterleidingduinen, a hypothetical wolf population present in Western Europe might have different effects. In the Oostvaardersplassen, the herbivores seem to be food limited, which leads to believe that large predators will not affect their population numbers that much (Vera, 2005; Vera, 2009). However, they may affect movement patterns of the herbivores, possibly leading to plant refugia, leading to opportunities for even more plant species (Ripple and Beschta, 2004; Vera, 2009) and keeping mesopredator numbers in check (Randi, 2011). Also, wolves can take upon them the role Staatsbosbeheer is playing now in killing off those ungulates that show signs of impending death (Vera, 2005; Vera, 2009). This way the ecosystem can become even more natural and self-regulatory while animal welfare is still kept in mind, since less animals will die from starvation.

In the Amsterdamse Waterleidingduinen on the other hand, a healthy wolf population might be able to keep in check the numbers of fallow deer, since these do not seem to be food limited (Van Breukelen et al., 2000). This would result in the coexistence of fallow deer and roe deer and will also lead to the persistence of plant species like European spindle (Euonymus europaeus), common hawthorn (Crataegus monogyna) and young English oak (Quercus robur), which are preferred by fallow deer (Van Breukelen et al., 2000). This increased possibility for coexistence of species is expected, because it also occurred in other systems: the Zion National Park and the Yellowstone National Park examples from the USA and the example from Scandinavian forest systems all showed more coexisting species in the presence of large carnivores than in their absence. Here, multiple species from multiple trophic levels had increased chances of persistence due to the creation of more niches and due to the reduction of competition among species (Elmhagen and Rushton, 2007; Miller et al., 2001; Ripple and Beschta, 2004; Ripple and Beschta, 2006).

Currently, the Hoge Veluwe natural park only includes red fox and pine marten as small predators. No top predators are present in the area. As a consequence, populations of wild boar and deer have to be culled (Hein, 2011) to avoid overpopulation and overexploitation of the system. This can also result in a better habitat quality for small rodents, since large herbivores have a negative effect on habitat

Radboud University Nijmegen | 16 MSc thesis Return of the wolves Anne M.G. Kwak quality of this species group (Smit et al., 2001). Large carnivores can, through predation, create areas with denser understory canopy which can increase the quantity and quality of food for small rodents, promoting densities of this group.

The hunters that are responsible for the culling of large herbivores in the park have to hand the prey they shoot back to the park management (Hein, 2011), meaning that no carcasses are left in the park. If a healthy wolf population were present in the area, this hunting might become unnecessary and wolves might keep the populations of wild boar and deer in check. Wolves also result in more carcasses in the park, which may support scavengers like red fox, raven and possibly even golden eagle (Wikenros, 2011).

Since the areas mentioned above consist of different habitat types, a mosaic of cascade intensity caused by Eurasian wolves across the landscape might occur, because prey can escape predation due to habitat refugia combined with spatial and temporal variability in species’ distributions (Callan et al., 2013). However, in the Netherlands it is likely that natural areas are too small for such a mosaic to really appear.

A recent study by Ripple and Beschta (2012) indeed shows that after a 70 year absence of wolves in Yellowstone National Park wolves have now since 15 years returned to the area. This has indeed had cascading effects on the system: elk populations have decreased, but both beaver (Caster Canadensis) and bison (Bison bison) numbers have increased, and Figure 4. Comparison photographs taken in 1997, 2001, and 2010 also woody browse species became taller and near the confluence of Soda Butte Creek with the Lamar River illustrating the stature of willow plants during suppression (A) from canopy cover increased in some, but not all long-term browsing and their release (B and C) following wolf areas (mosaic; figure 4)(Ripple and Beschta, reintroduction in the winters of 1995 –1996. As of 2010, both 2012). The authors suggest that this might be, willow height and canopy cover increased compared to the earlier dates (Ripple and Beschta, 2012). indeed, due to an increase in availability of woody plants and herbaceous forage as a result of less competition from elk. The Yellowstone National Park ecosystem does still seem to be in the early stages of recovery, but it provides an example where the reintroduction of wolves indeed seems to be a particularly effective approach for passive restoration (Ripple and Beschta, 2012).

Radboud University Nijmegen | 17 MSc thesis Return of the wolves Anne M.G. Kwak

Another recent study that seems to confirm this effective approach for passive restoration through the facilitation of a healthy wolf population was done by Callan et al. (2013) in the Great Lakes region in northern Wisconsin, USA. In this study the effect of recovery of wolves on understorey plant communities. In the Great Lakes region, the wolf population has recovered through input of wolves from Minnesota. In the area, the wolves prey mainly on white-tailed deer (Odocoileus virginianus), which in turn browse on understory plants (figure 5). Callan et al. (2013) found that in general, high wolf Figure 5. Diagram of hypothesized tri-trophic interactions in northern occupancy sites had a diverse understorey Wisconsin forests. Solid arrows represent direct positive and negative community with complex vertical interactions. Dashed arrows represent hypothesized indirect interactions. Dotted line represents competitive interactions (Callan et structure. In contrast, they found that low al., 2013). wolf occupancy sites had a very limited herbaceous layer and almost no woody browse. A situation very similar to that showed in figure 4 from the study of Ripple and Beschta (2012). Callan et al. (2013) indeed also provided correlative evidence of top-down trophic effects generated by wolves. They thus conclude that wolf recovery in other regions of North America could be vital to maintaining the ecological integrity of northern white cedar wetlands and potentially other temperate and boreal forest systems as well (Callan et al., 2013).

The studies by Ripple and Beschta (2012) and Callan et al. (2013) show us that wolves can indeed have a very important role in the passive restoration of ecosystems to a more natural state. If we extrapolate these examples to Europe, we may think that the expansion of the Eurasian wolf to western Europe may indeed provide us with a way to passively manage and restore our ecosystems to a more natural and wild state. So in each of the example areas from Europe mentioned above, a wolf population will result in different effects on the present ecosystems, but it is still expected to lead to an increased biodiversity. It would also reduce the need for human interference in these systems, leading to more natural states. Human interference has been less in the USA, meaning that the effects taking place in the Dutch systems mentioned above will most likely be slightly different from those in the USA, but they will likely occur nonetheless. Next to these ecological benefits, a healthy wolf population in Western Europe may attract more tourism, also to natural parks in the Netherlands. This leads to more economical income from tourism, but also to more acceptance and public support from the community to conserve and promote top predators in our natural parks.

4.1 IMPLICATIONS FOR MANAGEMENT OF EURASIAN WOLF CANIS LUPUS LUPUS Due to their possible abilities to create more natural ecosystems with a higher biodiversity, we would like to welcome back the Eurasian wolf from an ecological perspective. However, the Eurasian wolf does not only bring with it changes to ecosystems, but also evokes fear in humans either for their own safety or for that of their domestic and game animals.

If we do want to welcome back the Eurasian wolf, we will have to come up with conservation management plans that both ensure a possibility for the development of a stable population and the safety of people and their livestock. This risk of conflict with humans is increased by the fact that

Radboud University Nijmegen | 18 MSc thesis Return of the wolves Anne M.G. Kwak wolves inhabit very large territories with population ranges often exceeding borders of natural parks (Randi, 2011). Management and conservation of wolves may thus only be successful in the long term if people can accept free ranging predators in their area. To achieve this, we will have to regulate the wolf population to address public concern, but at the same time we need to maximize population viability of these predators (Chapron et al., 2003).

A way to maximize population viability for Eurasian wolf might be to connect natural parks across Western Europe to increase available habitat and to improve dispersal possibilities. Connecting natural parks may also provide a way in which wolf-human conflicts can be minimized. Wolves prefer to roam around in natural areas rather than inhabited areas (Chapron et al., 2003), thus causing them to use connections between parks instead of urban areas. Using this type of management, we might be able to achieve a (near) maximized population viability while at the same time addressing public concern.

Radboud University Nijmegen | 19 MSc thesis Return of the wolves Anne M.G. Kwak

5 DISCUSSION

Since the 1960s the controversy between top-down and bottom-up control of ecosystems has been ongoing and it seems that researchers are still investigating which mechanism applies to their study ecosystem. However, as we have seen, it seems that a consensus was reached, since more and more researchers are finding that their ecosystems are regulated both from the top down and from the bottom up (Báez et al., 2006; Elmhagen and Rushton, 2007; Frederiksen et al., 2006; Terborgh et al., 2001). Since this seems to be the case, it seemed important to investigate the importance of top predators in (terrestrial) ecosystems.

One of the most important aspects of top predators in ecosystems is that they reduce competition pressure for some lower trophic level species (Miller et al., 2001). In this way, large carnivores create more niches in an ecosystem than would be present without these top predators. They thus allow for more species to coexist in a system, increasing the biodiversity in that area (Sergio et al., 2005). This niche creation does not only apply to animals, but also to plants. Since top predators can keep herbivore populations in check due to their important role in predator-prey relationships (Miller et al., 2001), indirectly these carnivores can create niches for less competitive plants as well.

That top predators do play these roles in ecosystems can be seen from the examples of systems where predators were removed (section 3.2). In several study areas researchers found that where top predators were absent, there was less biodiversity, more browsing pressure from herbivores and also indirect effects on other species that are not directly related in the food web to top predators (Elmhagen and Rushton, 2007; Ripple and Beschta, 2004; Ripple and Beschta, 2006).

Keeping this in mind, the current range expansion of the Eurasian wolf (Chapron et al., 2003; Randi, 2011) might have considerable effects on our ecosystems. These top predators may be able to return our ecosystems to a more natural state, since currently many ecosystems lack large predators and need to be managed by humans to keep a somewhat natural state (Terborgh et al., 1999). The return of wolves to our ecosystems might increase biodiversity in these areas through the mechanisms described in chapter 4. We have seen this happen in the USA, so it is likely to also happen in Europe (Callan et al., 2013; Ripple and Beschta, 2012). A healthy wolf population may make human management of ecosystems (partly) unnecessary, resulting in less economical costs. Next to the ecological benefits of having a healthy wolf population in Europe, tourism may also benefit from it.

However, even if this seems very desirable from an ecological and perhaps economical perspective, the return of the Eurasian wolf also brings with it fear. Wolves do live in very large territories, increasing the risk of conflict between humans and these animals. This may cause resistance from society. To ensure that humans and wolves can live together, we will have to think of management strategies where we both regulate the wolf population to address concerns from society, and we will have to try and maximize population viability for the wolves. This might prove to be somewhat of a challenge, but as discussed in section 4.1 the connection of natural parks across Europe might help to achieve this.

To conclude, from an ecological perspective it would be very interesting to welcome back the Eurasian wolf Canis lupus lupus to our ecosystems. They may be very important for the return of ecosystems to their most natural state and for the increase and conservation of biodiversity in these systems. However, we do need to address public concern about free roaming large predators and it is thus necessary to come up with conservation management strategies now, before human-wolf conflicts arise, so that we can already build up support within the community to welcome back the wolf.

Radboud University Nijmegen | 20 MSc thesis Return of the wolves Anne M.G. Kwak

6 LITERATURE

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Radboud University Nijmegen | 21 MSc thesis Return of the wolves Anne M.G. Kwak

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