PDF hosted at the Radboud Repository of the Radboud University Nijmegen

The following full text is a publisher's version.

For additional information about this publication click this link. http://hdl.handle.net/2066/131689

Please be advised that this information was generated on 2021-09-24 and may be subject to change. invasions

Laura Verbrugge Going Global Going biological Perceiving, assessing and managing and managing assessing Perceiving,

Mechanisms and constraints in biodiversity conservation and restoration 9 Going Global Laura Verbrugge

Going Global

Perceiving, assessing and managing biological invasions Verbrugge LNH (2014) Going global. Perceiving, assessing and managing biological invasions. Thesis, Radboud University, Nijmegen. © LNH Verbrugge, 2014

ISBN: 978-94-61087-84-3

Printed by: Gildeprint - Enschede Lay-out: AM Antheunisse Cover photos: The blue marble (NASA), ring necked parakeet (Luuk Punt), zebra mussels (Gerard van der Velde), red swamp crayfish (WikiCommons), water pennywort (Roy Kleukers), American bullfrog (WikiCommons). Going Global

Perceiving, assessing and managing biological invasions

PROEFSCHRIFT

ter verkrijging van de graad van doctor aan de Radboud Universiteit Nijmegen op gezag van de rector magnificus prof. dr. Th.L.M. Engelen, volgens besluit van het college van decanen in het openbaar te verdedigen op maandag 24 november 2014 om 14.30 uur precies

door

Laura Nicoline Halley Verbrugge

geboren op 9 augustus 1986 te Rhenen Promotoren: Prof. dr. H.A.E. Zwart Prof. dr. ir. A.J. Hendriks

Copromotoren: Dr. R.S.E.W. Leuven Dr. R.J.G. van den Born

Leden manuscriptcommissie: Prof. dr. P. Leroy (voorzitter) Prof. dr. L.P.M. Lamers Prof. dr. M.N.C. Aarts (Universiteit van Amsterdam)

Paranimfen: Lisette de Hoop Dieuwertje de Vries “… the era of globalization - the single, turbulent economic and ecological exchange that today engulfs the entire habitable world.” Charles C. Mann – 1493: Uncovering the New World Columbus Created Published by Random House, New York in 2011

Contents

1 General introduction 9

2 Sensitivity of native and non-native mollusc species to changing river 29 water temperature and salinity

3 Risk classifications of aquatic non-native species: application 49 of contemporary European assessment protocols in different biogeographical settings 4 Metaphors in invasion science: implications for risk assessment and 65 management of biological invasions

5 Exploring public perception of non-native species from a visions of 81 nature perspective

6 Evaluating stakeholder awareness and involvement in risk prevention 101 of aquatic invasive plant species by a national code of conduct

7 Synthesis 123

Appendices 139

Summary 149

Samenvatting 155

Dankwoord 161

Curriculum vitae 165

List of publications 167

Chapter 1

General introduction

Laura Verbrugge Chapter 1

10 Globalization, the Anthropocene, and the homogenization of the world’s biota Humans have become the most dominant species on earth and have an enormous, often irreversible influence on their surroundings. Our ability to travel over great distances allowed us to populate every corner on this planet, making it suitable for human habitation. The sway of human beings is such that we now (informally) refer to the present as the ‘Anthropocene’, seeing human beings as the key protagonists in the current geological changes and climatological disruptions (Crutzen 2002). This term is closely related to the ‘Homogenocene’, a word used to describe our current era as a period of diminishing biodiversity and increasing similarities of ecosystems around the globe (Samways 1999). Almost 500 years ago, the discovery of the America’s by Columbus marked the start of the ‘Homogenocene’ era. It was the onset of great changes in the world’s civilizations and biota. It not only led to a mixing of different cultures, but also to the exchange of plants and animals between the continents, also referred to as the ‘Columbian Exchange’ (Mann 2011). The term globalization is often used to describe economic developments (Levitt 1983) but its biological impact is at least as significant. Human activities associated with globalization are the main cause for the relocation of species and their introduction in remote locations. Centuries ago, plants and animals were transported across the globe (from country of origin to colonies and back) as source of food, ornamentals and companions, or to make new places feel like home. By transporting species to formerly unreachable places, we acted as global vectors of dispersal for a plethora of other species and made the worldwide spread of non-native species, also referred to as neobiota, alien, foreign, exotic, introduced or non-indigenous species, possible. Technological innovations in the 20th century have accelerated the process of globalization. At present, it is possible to visit or import goods from nearly any place on earth. This increase in number of transports is astounding, with seemingly endless possibilities to travel over air, water and land. For example, more than 90 per cent of the world trade volume is shipped and over the last four decades total seaborne trade estimates have nearly quadrupled (International Chamber of Shipping 2013). Several studies have shown that socio-demographic variables, such as population densities and national wealth, are positively correlated with the number of species introductions (Essl et al. 2011; Pyšek et al. 2010; Westphal et al. 2008), clearly linking trade activities with biological invasions. Introductions of non-native species have developed at the same astonishing pace as human ‘invasions’ and have forced us to consider the consequences of mixing the world’s biota. Biological invasions can be perceived as a symptom of present times, where natural borders have lost much of their former meaning and significance. The term ‘McDonaldization’ (Lövei 1997) has been invented to describe the occurrence of globally wide spread species, such as the American bullfrog Lithobates catesbeianus, water hyacinth Eichhornia crassipes and purple loosestrife Lythrum salicaria, that are now present on almost every continent. These species are listed as one of the hundred worst invasive alien species in the world by the Invasive Species Specialist Group (ISSG) due to their invasion history and records of high impacts on humans and the environment (Lowe et al. 2000). General introduction

11 Box 1. The crow case This is the story about the house crow Corvus splendens, a bird species native to India and South- East Asia, and its arrival in The Netherlands. First sightings of this species in Hoek van Holland were reported in 1994, where a pair had arrived (presumably) by ship from Egypt. In 1997, breeding activities were reported and since 2007 a small population of about 20 birds has been established. The early sightings of the species, in combination with the very small likelihood of new introductions would, in theory, have made it very simple and cost-effective to intervene and have them removed. However, the authorities were reluctant to do so for two very different reasons. At first they awaited the results from a risk assessment to provide the evidence that the species was indeed harmful in some way (Slaterus et al. 2009). When this step was taken, their hands were bound because the species had (wrongfully, in fact) been placed on a list of legally protected species. While this was sorted out in court, another problem arose, namely public opposition to the eradication of the house crow in the Netherlands. Bird watchers and animal welfare activists strongly objected to decimation and even took matters in their own hands by putting a halt to reporting sightings (so that the authorities could not adequately locate them) and by providing a safe house so they could be reintroduced afterwards. At this stage, the public debate even made the national newspapers. This account of the events becomes even more interesting if one considers the various types of arguments used in the debate by proponents and opponents, as well as their different interpretations of the status of the animal in the Netherlands. The ship-related vector for introduction can unmistakably be linked to human activities, and so meets the definition of non-native species. However, others state that the ability of birds to fly and choose their own way of travel makes them cosmopolitan species that cannot be given such a status. Due to the small numbers, the present population does not as yet cause much harm and they are regarded rare birds in the Netherlands which bird watchers are eager to spot. However, the risk assessment results show that there is potential for harmful effects when the population grows and spreads. From a manager’s perspective, it is evident that a species that poses a significant threat to biodiversity or society will require intervention, in this case the catching of a limited number of birds that form the small population currently ‘invading’ the Netherlands. This opinion is not shared by other members of society who wish to protect wild fauna in the Netherlands. Thus, on the one hand, these crows are framed as non-native species with harmful impacts, and therefore perceived as a threat. On the other hand, they are seen as endangered or novel species enriching biodiversity and therefore regarded as object of protection and concern. Among other things, this story tells us that biological invasions are complex, multi-scale problems with many uncertainties and involving a large number of different actors (e.g. policy makers, nature managers, bird watchers and ecological and risk assessment experts). In other words, they represent a ‘wicked problem’ for which solutions are not easily found (Rittel and Webber 1973). Even with the legal permission for eradicating the house crow in the Netherlands that has now been obtained, fierce societal opposition may form an even larger obstacle for the government to take action. The wickedness of these problems served as a source of inspiration for writing this thesis.

House crows (Corvus splendens) at Hoek van Holland (The Netherlands). Photo: Luuk Punt Chapter 1

12 Our role as Homo sapiens is a complex and ambivalent one. We strive to overcome barriers for our benefit but at the same time try to guard our borders to keep out what may harm us. Richardson et al. (2008) have adequately put it as follows: “Humans cause invasions, humans perceive invasions, and humans must decide whether, when, where and how to manage invasions ”. Depending on our backgrounds, biological invasions can be framed in different ways, each one providing a different perspective on management of invasive species (Heger et al. 2013b). The example given in Box 1 illustrates the role of humans and how this influences our perceptions and interpretations of biological invasions. It is a case study from the Netherlands, but at the same time exemplifies the intricacies and ambiguities of global biological mobility as such. The relationship between human society and biological invasions, as well as our perceptions of risks posed by non-native species are further explored in the remainder of this chapter and will result in the formulation of the research aim of this thesis.

Drivers of biological invasions Non-native species are generally defined as animals, plants or microorganisms that have been introduced outside their natural range by human mediated means. Over the past centuries, many species have been introduced intentionally because of their utilitarian values, such as crops, fish for aquaculture or ornamentals. Societies have received great benefit from these species in terms of resources, food, scientific research or human well- being. However, the increase in global trade, transport, travel and tourism around the globe (also referred to as the four T’s) has also facilitated unintentional or accidental introduction of species. Over the past decades, the total number of introductions has increased tremendously (Pyšek et al. 2010). The introduction of non-native species can be categorized into six principal pathways (Hulme et al. 2008): (1) intentional releases, (2) escapes from confinement, (3) as contaminant of a commodity, (4) as stowaway related to a transport vector, (5) through corridors linking previously unconnected regions and (6) unaided through natural dispersal from other regions where the species was introduced. Pathways describe the means and routes that result in a species introduction. An overview

Table 1.1 Main vectors facilitating introductions of non-native species (main source Hulme et al. 2008).

Taxonomic group Main vector(s) Additional references Terrestrial vertebrates Pet trade and fauna improvement (escapes from captivity and (Bertolino 2009; Masin et deliberate releases), hitchhiking on planes or ships al. 2014) Terrestrial Biocontrol (deliberate releases), contaminant of host species, (Liebhold et al. 2012) invertebrates hitchhiking in containers, packaging or raw materials Terrestrial plants Ornamental trade and landscape improvement (deliberate (Reichard and White 2001) releases or plantings and escapes) Aquatic vertebrates Shipping (ballast water), construction canals, aquaculture (Carlton and Ruiz 2005; and fisheries, pet trade (escapes from captivity and deliberate Padilla and Williams 2004; releases) Tricarico 2012) Aquatic invertebrates Shipping (ballast water, hull fouling), aquaculture, construction (Briski et al. 2012; Carlton canals, pet trade and seafood, bait and aquarium industries and Ruiz 2005; Leuven et al. 2009) Aquatic plants Ornamental trade (escapes and deliberate releases), (Brunel 2009) aquaculture Pathogens, Tourists or travellers, (rail)roads or vehicles, contaminant of (Von der Lippe et al. 2013; microorganisms and seed or host species Ware et al. 2012) plant seeds General introduction

13 of the main vectors (i.e. the actual medium that facilitates the transport) per species group is given in Table 1.1. Mammals and birds were often deliberately released into the environment to serve as game animals and in attempts to improve local fauna or they may escape from captivity. Small (micro)organisms, on the other hand, mainly travel as a contaminant of a commodity, for example small insects present on plant leaves or the Parapox virus carried by North American grey squirrels. Ornamental trade is the main vector for the introduction of plants, while seeds may also be transported as contaminant or by vehicles or travellers. Finally, the spread of aquatic species is largely facilitated by ballast water of ships, hull fouling and the construction of canals between formerly isolated river basins.

A framework for predicting and managing biological invasions For a biological invasion to occur, a species has to cross several barriers (Blackburn et al. 2011; see also Figure 1.1). The first barrier is a geographical one in the form of an ocean, mountain or area otherwise unsuitable for dispersal of a particular species. In the case of biological invasions, humans facilitate the crossing of this barrier by transporting the species to a new area or enhancing dispersal across barriers, e.g. by creating interbasin

Non-native

Casual Naturalized or established

Invasive Terminology

Introduction Establishment Spread SURVIVAL DISPERSAL GEOGRAPHIC REPRODUCTIVE ENVIRONMENTAL

Barrier

Prevention Containment Mitigation

Control

Eradication Management

Figure 1.1 A schematization of barriers limiting the distribution of introduced species, including the associated terminology and management strategies. Adapted from Blackburn et al. (2011). Chapter 1

14 connectivity. The second critical step is survival; if a species cannot tolerate the conditions during transport or the climate in the recipient area, it will not survive. The third barrier is related to reproduction as the organism needs suitable conditions to produce offspring, for example in the form of a mate, a certain type of habitat or environmental conditions. Offspring is needed to ensure that the species can establish a permanent population independent of any new arrivals. The fourth level is secondary spread, i.e. the dispersal from the area where it was introduced into adjacent areas. Finally, the species can become widespread in the new region. From this barrier-concept, it becomes clear that not all introduced species will gain a permanent residence, and even fewer species will be able to spread further. The chance of establishment and spread increases with (1) the invasibility of the receiving region (i.e. susceptibility to invasion) and with (2) an increasing number of introductions and individuals per introduction, also termed ‘propagule pressure’. The generally accepted ‘tens rule’ describes that, as a rule of thumb, ten per cent of the species that are introduced are able to establish, and that ten per cent of those established species will have the ability to spread further (i.e. become invasive) (Williamson 1996). This rule seems to give a rough indication of what happens, but should be applied cautiously for two reasons: (1) only the second step is supported by empirical evidence, and (2) variability exists between different species groups and recipient areas (e.g. islands) (Jeschke and Strayer 2005; Ricciardi and Kipp 2008). The time between the establishment of a species and subsequent spread is referred to as the lag time or lag phase. This period, in which the species remains innocuous in a restricted area before becoming invasive, can last years or even decades. This creates uncertainty in predicting if and when a species may become invasive. Considering the number of introductions in the past decades, we may expect more of these surprises in the (near) future (Essl et al. 2011).

Ecological and societal impacts of biological invasions Invasive species have become a major issue for policy because of the risk they pose to the environment, economy and human health. Ecological impacts include predation on or competition with (native) species already present in the area resulting in population reduction or (local) extinction, (irreversible) changes in ecosystem functioning, genetic hybridization and the transmission of diseases (EEA 2012). The latter poses a significant risk to all living entities, including humans, as noted by the introduction of the tiger mosquito Aedes albopictus in Europe (Hofhuis et al. 2009). Socioeconomic impacts of invasive species include damage to key economic sectors, such as agriculture, livestock breeding, forestry, human health and infrastructure (Pejchar and Mooney 2009). Examples are damage to crops or trees by insects, clogging of industrial pipes by zebra mussels and obstruction of waterways by aquatic weeds. The attention from governmental bodies has risen quickly over the past decades (Butchart et al. 2010) because of the high costs of mitigation and control of invasive species. In Europe, more than a thousand species are categorized as invasive, i.e. as causing ecological or economic damage (Vilà et al. 2009). The associated costs are estimated conservatively at 12.5 billion Euros per year while it is suggested that 20 billion is probably a more realistic estimate (Kettunen et al. 2009). Most of this budget is spent on damage and control of, General introduction

15 in particular, vertebrate species. However, other nuisance species such as aquatic weeds and invertebrates (especially molluscs) may also weigh heavily on government budgets. In the Netherlands, the yearly costs of damage and control of invasive species is estimated at 1.3 billion Euros (Van der Weijden et al. 2007). Recent figures show that Dutch water boards spent 36 million Euros per year on the removal of over twenty invasive species, such as muskrats and aquatic weeds (Bos and Moerkens 2013). The muskrat Ondatra zibethicus, originating from North America, is intensively managed to prevent damage of digging activities to dikes and other infrastructures. Another well-known example of a non-native species with devastating impacts in the Netherlands is the shipworm Teredo navalis representing a historical and potential future threat to wooden structures and increasing flood risk (Paalvast and Van der Velde 2011). More recently, floating pennywort Hydrocotyle ranunculoides, an ornamental species that was imported for water gardening, spread into natural water systems outcompeting native species and creating obstructions in waterways (Pot 2002).

Response to biological invasions The multitude of impacts and associated costs has triggered many national and international policy responses. Globally, invasive species impacts have been recognized as one of the major threats to biodiversity (Millennium Ecosystem Assessment, 2005). Article 8(h) of the Convention on Biological Diversity states that “each contracting party shall, as far as possible and as appropriate, prevent the introduction of, control or eradicate those alien species which threaten ecosystems, habitats or species ”. The European Union published the European strategy on invasive alien species (Genovesi, Shine 2003) and is now preparing legislation to further prevent the introduction and spread of invasive species in EU Member States (European Commission 2013). On national and state levels risk management frameworks have already been developed in response to biological invasions and advances in this field are proceeding rapidly. For example, in Belgium the Invasive Species Environment Impact Assessment (ISEIA) protocol was developed to assess and classify over a hundred species (Branquart 2007). Recently, an update has been released in the form of the Harmonia+ protocol, which is a screening tool for new pests and invasive species and includes assessments of harm to the environment, infrastructures and human, animal and plant health (D’hondt et al. 2014). Another example is the Fish Invasiveness Scoring Kit (FISK), a decision support tool that has been adapted for different species groups (i.e. freshwater invertebrates, amphibians, marine fish and marine invertebrates) and climatic zones (Copp 2013). All these initiatives on different institutional levels share a common aim: to identify (potentially) invasive species and provide information on their pathways and impacts relevant for management interventions. The main strategies for management of non-native species include prevention, eradication, control, containment and mitigation (Wittenberg and Cock 2001). The chosen strategy depends on the invasion stage (e.g. few individuals or widespread) and the costs and feasibility of management strategies (see also Figure 1.1). Preventing new introductions is considered most cost-effective strategy, but is often not feasible. Early warning and rapid response may result in timely eradications of species before they become established, while eradication programmes on smaller scales (i.e. within a restricted area) may also Chapter 1

16 be effective in later stages. Once a non-native species becomes established, control can be aimed at keeping species within certain regional barriers (i.e. containment) or at suppressing population levels below an acceptable threshold. If eradication, control and containment fail, the last option is to mitigate the impacts of invasive species.

Risk analysis: a tool to predict and prioritize Risk analysis has come to play a major role in invasive species policies (Andersen et al. 2004). Risk analysis consists of three major components: risk assessment, risk management and risk communication (Figure 1.2; Van Leeuwen and Vermeire 2007). Risk assessment is the process in which hazards are identified, assessed and characterized. This process requires scientific development of risk assessment methodologies and quantifications of risk. Risk management is the decision making process that entails “weighing political, social and economic information against risk-related information to develop, analyse and compare regulatory options and select the appropriate regulatory response to a potential health or environmental hazard ” (Van Leeuwen and Vermeire 2007, p. 2). Finally, risk communication encompasses the contextual definition of risk and provides a platform for interaction and knowledge exchange with relevant stakeholders. In the past years, a shift has occurred from a technocratic risk model (with emphasis on scientific considerations and expert advice) to a more transparent model in which socioeconomic, cultural and political values are acknowledged (Van Leeuwen and Vermeire 2007). The increase in awareness of the crucial role of relevant stakeholders in the risk management process has resulted in more attention to risk perception and risk communication. Internationally, the need for improved communication efforts and interdisciplinary approaches in the field of biological invasions is increasingly recognized, and the involvement of social sciences (such as communication science and sociology) is highly recommended (EPPO 2013).

C. Risk communication • Inventories of risk perceptions • Stakeholder involvement • Legitimization of risk policies

A. Risk assessment B. Risk management • Vectors / pathway assessment • Risk classification • Spread or invasiveness • Risk benefit analysis • Effects assessment • Risk reduction • Risk characterization • Monitoring and review

Figure 1.2 Risk analysis consists of three components: risk assessment, risk management and risk communication (adapted from Van Leeuwen and Vermeire 2007). General introduction

17 Predicting biological invasions is extremely difficult due to stochastic introduction events, spatial and temporal variability of population developments (e.g. lag times), possible interactions with other species and the abiotic environment, and the various impacts they may have. Uncertainty is inherent to the risk assessment process and can be the result of gaps in knowledge, measurement uncertainties, observation uncertainties or inadequacy of the model (Van Leeuwen and Vermeire 2007). Finally, the use of imprecise or vague language and differences in interpretation (or linguistic uncertainty) can also be identified as a source of uncertainty (Leung et al. 2012).

Social contours of risk The complexity of biological invasions, the context dependency of impacts and the scientific methods used to predict these impacts are of major importance in risk related research. However, the existence of disparate perceptions of invasive species is just as vital (Heger et al. 2013a). Whether something is perceived as risky depends on personal interests, beliefs and values and therefore differs between individuals and groups. For example, ecological risks are perceived differently by scientists and lay people. The latter are less concerned about long term problems, such as ecosystem impacts, than the former (Slimak and Dietz 2006). Biological invasions are placed high on the science and political agenda (e.g. in the Millennium Ecosystem Assessment and by the European Commission). However, an EU survey showed that this concern is not shared by the general public as only 2 per cent of the respondents regarded invasive alien species as an important threat to biodiversity while pollution, climate change and intensive agriculture were seen as the three largest threats (Gellis Communications 2007). How can these differences in ecological risk perceptions be explained? In general, economic and health risks are relatively easy to quantify in terms of costs or losses and this information may be sufficient to feed perceptions of risk. Nature, however, isa ‘common’ good that cannot be captured easily in monetary or other quantitative terms. Factors playing a role in ecological risk perception are not only the severity of ecological impacts, but also the level of scientific understanding, associated benefits, controllability and aesthetic values (Willis and Dekay 2007). An often cited sentiment is that a non- native species does not belong in the place where it is introduced (Qvenild 2013; Warren 2011). Recurring concepts such as naturalness, authenticity and sense of place are in fact meanings we attribute to nature based on our experience and knowledge and are part of the overarching term visions of nature. Anthropocentrism and ecocentrism are central themes in such perceptions of nature. In an anthropocentric worldview, nature is valued and protected because of its commodities and benefits for humans and in order to preserve or enhance human qualities of life. Ecocentrics believe nature to have value on its own, an intrinsic value, which has to protected. These worldviews also inform public opinions on invasive species management (Sharp et al. 2011). Chapter 1

18 A short history of invasion science The number of publications on bioinvasions has increased tremendously over the past decades (Richardson and Pyšek 2008). Initial efforts were aimed at gaining insights in species traits, distribution patterns and other predictors for invasions that can aid management of invasive species (Huenneke et al. 1988). Over time, it became clear that impacts of non-native species were not limited to ecological processes. In addition, they may include adverse societal effects. There was also increasing recognition of the fact that humans play a fundamental role in biological invasions and invasive species management. In his book “The great reshuffling: human dimensions of invasive alien species” McNeely (2001) discusses the many facets to the problem of biological invasions: “the historical, economic, cultural, linguistic, health, psychological, sociological, management, legal, military, philosophical, ethical, and political dimensions ”. The research field broadened and became multi-disciplinary, now receiving contributions from many of these disciplines, as well as risk management and policy sciences. Invasion ecology is developing more and more into an invasion science. One of the striking features of this field is the terminology that is used in scientific as well as in public and policy domains, such as ‘invasive species’, ‘fighting invaders’ and ‘explosive growth’. These militant wordings are as old as the field itself and can be traced back to one of the first and certainly one of the most influential publications: “The ecology of invasions by animals and plants” written by Elton (1958). In this book the colonization of New Zealand by non-native species is described as follows: “No place in the world has received for such a long time such a steady stream of aggressive invaders, especially among the mammals…” (p. 89). The bellicose nature of these phrases is even more striking when compared to the language used by Wodzicki (1965) ten years later, who describes the same phenomenon with a different set of metaphors, namely as “an imposing record of intentional and unintentional animal introductions ” of which some became “very successful colonizers ” (p. 454-455). Now, more than 50 years later, the linguistic problems still remain (Larson 2007). These not only relate to the use of value-laden concepts to describe biological invasions, but also to differences in interpretation of existing terms (Falk- Peterson et al. 2006). Invasion science has its roots in ecology, and as a result, its conceptualization and the setting of the research agenda were defined in ecological terms. Current difficulties in establishing a comprehensive view needed for developing effective management strategies should at least partly be attributed to this historical development. One difficulty lies in the fact that differences in terminology and (modelling) approaches inhibit the development of interdisciplinary research fields. In bibliometric analyses disciplinary boundaries were identified as obstacles to integrative research involving both natural and social sciences (Vugteveen et al. 2014). Invasion science proves no exception as collaboration between, for example, ecologists and economists are scarce (Bampfylde et al. 2010). Other problems are set in the science-policy interface where a knowing-doing gap has been uncovered, i.e. what we actually know is not directly very helpful in making decisions on what to do. Besides different levels of pragmatism, scientists and policymakers also have different interpretations of popular terms used to describe biological invasions. For example, the mainstream view by ecologists is that invasive species depict the group of non-native species that reproduce in large numbers and spread quickly over large General introduction

19 distances (Richardson et al. 2010). In the public and policy domain, however, invasive species are usually defined as species that have measurable ecological or socioeconomic impacts, thus strongly relating it to the risk of species becoming harmful. In order to ensure that research on bioinvasions will progress, it is important to build bridges between disciplines that will facilitate cooperation and integration of research results relevant for invasive species management. This will require the search for ‘boundary objects’ that have meaning to both policy makers and researchers in different fields of expertise.

Rationale for this study Most studies attempting to close the gap between science and policy focus on the availability of scientific knowledge and whether or not they meet the needs of policy makers and nature managers (Bayliss et al. 2013; Esler et al. 2010; Kumschick and Richardson 2013). In these attempts, the social aspects of biological invasions often remain a blind spot. Several studies, however, have shown that collaborative management and the understanding of social factors are of major importance for nature conservation (Austin et al. 2013) and ecosystem management (Endter-Wada et al. 1998). Moreover, risks posed by invasive species are socially constructed and require an integrated approach in order to effectively manage them (Kueffer and Hirsch Hadorn 2008; Liu et al. 2011; Mills et al. 2011). The most common form of social science in environmental management concerns public involvement and provides information on public support for management strategies and general values or beliefs of relevant stakeholder groups (Endter-Wada et al. 1998). This type of research generates information on conflicting views that may assist in problem solving and therefore matters greatly from a management perspective. In the case of biological invasions, public involvement matters in three ways. First, it is important that people understand and acknowledge their role in the spread and introduction of non- native species before preventive measures can be effective. Second, help of volunteers is essential for early discovery of new introductions, but they will need the appropriate tools and knowledge to be able to do so. Finally, general support among the public for preventive measures and eradication campaigns is of major importance for them to succeed. These observations have led to an increasing recognition that public understanding and public engagement are fundamental for effective governance of biological invasions (Brunel et al. 2013). Contributions from social science include studies on perceptions of different stakeholder groups (Andreu et al. 2009; Vanderhoeven et al. 2011), their willingness to pay for invasive alien species management (García-Llorente et al. 2008, 2011) and their support for management interventions (Bremner and Park 2007). However, this is a limited view on social science contributions in environmental management, as it is only focused on problem solving (Endter-Wada et al. 1998). Integration of social considerations on a deeper level, in science itself, is much less common but equally valuable. This type of data includes, for example, research on social processes and global changes in relation to environmental changes and management. Attempts to integrate the natural and social sciences in biological invasions are rare and often limited in scope, addressing single species in a specific region (Binimelis et al. 2007; Epanchin- Niell et al. 2009). Theoretical frameworks describing the invasion process as presented earlier (Figure 1.1) have been criticized for being only partly able to integrate natural and Chapter 1

20 social sciences (Kueffer and Hirsch Hadorn 2008). The key role of humans in the setting of biological invasions makes the understanding of social values, beliefs and processes in a broader framework extremely relevant. The underlying normative assumptions (e.g. the distinction between native and non-native species or the valuation of impacts) have been increasingly criticized but this has not yet led to any new conceptual understandings, for example in relation to nature conservation. The acknowledgment of normative aspects is especially important in risk analysis, which requires the assessment of both facts and values (Kapler et al. 2012; Liu et al. 2011; Mills et al. 2011). A general assessment of normative thinking in assessing and managing risks posed by invasive species is still lacking, which currently inhibits successful implementation of social science contributions in the risk analysis framework. This thesis will contribute to the existing body of knowledge by addressing this gap in a comprehensive way, including all three components of the risk analysis framework (i.e. risk assessment, risk management and risk communication). Moreover, studies on social aspects of non-native species are needed to increase our understanding of the relationship between humans and nature, and our contemporary visions of nature and landscapes. To sum up, there is a strong need for studies that integrate social and natural sciences in existing theoretical and decision making frameworks for managing biological invasions.

Aim of this thesis There are many challenges involved in predicting and managing invasive species risk. Policy makers will have to weigh the arguments brought forward by (ecology) experts and other (public) stakeholders, to identify feasible policy options that will be publicly supported. Risk analysis is the key element in this process. Yet, risk analysis is complex due to the involvement of governmental and public stakeholders with divergent and, possibly, conflicting views. The aim of this thesis is twofold. First, it aims to analyse the scientific, societal and policy considerations in risk analysis of biological invasions in order to reflect on the wider implications for decision making. Second, it will evaluate how environmental science and social science may be combined to enhance understanding of policy practices concerning invasive species management. Fulfilling this aim requires integration of the natural and social science disciplines. Thus, this thesis will combine aspects of ecological, social and communication sciences relevant in risk analysis of non-native species. This interdisciplinary approach is reflected in the different approaches and methods used in the chapters of this thesis. The chapters will address the following research questions (letters correspond with the three major components of risk analyses in Figure 1.2).

Research questions • What is the role of science in predicting, assessing and communicating ecological impacts of biological invasions? (A - C) • What methods are used for risk assessment of non-native species and which factors contribute to the variability in risk classifications? (A - B) • What are the implications of the use of (strong) metaphors in describing biological invasions for effective risk management of invasive species? (B) General introduction

21 • How does the lay public perceive biological invasions and what is the relationship between these public perceptions and their visions of nature? (C) • What is the effectiveness of voluntary trade mechanisms and public outreach campaigns in increasing public awareness and preventing new introductions of ornamental plants? (B - C)

Outline The main body of this thesis consists of five research chapters, including four empirical (case) studies (Chapters 2-3 and Chapters 5-6) and one reflective paper (Chapter 4). The scope is restricted in the sense that the focus is on risk analysis of biological invasions in a European context, and risk management (including risk perception and communication) in a national context (i.e. The Netherlands). However, generalizations of the outcomes of this thesis are relevant in other contexts as well, as similar concepts and mechanisms are used elsewhere. Chapters 2 and 3 address the role of science in assessing impacts of biological invasions. The best way to study the role and contribution of science in identifying and quantifying impacts of invasive species is to place oneself in the position of a researcher studying ecological impacts of non-native species and, thus, to experience this role in real life. Chapter 2 is such a case study. The main objective of Chapter 2 is to analyse the effects of changing environmental conditions, resulting from climate change, on the composition of mollusc assemblages in the river Rhine. The results from this study may serve as input for risk assessments of non-native mollusc species but, more importantly, they provide valuable insights in framing and communicating these results when writing a report, scientific paper or recommendations, as will be discussed in Chapter 7. Chapter 3 provides an overview of different types of risk assessment tools for prioritizing high risk species currently in use in Europe and includes a comparison of risk classifications between European countries for similar species. Based on the results from this study, I seek for possible explanations in the variability of risk outcomes and discuss current difficulties in performing consistent risk assessments. The fourth chapter builds on the first two empirical studies and further explores science- policy interactions in the field of risk assessments. This chapter entails a philosophical reflection on the implications of the use of (strong) metaphors in describing biological invasions for invasive species policies. It particularly focuses on the role of scientists in ecological impact assessments and the concept of responsible metaphor management in managing and communicating invasive species risks. The chapters 5 and 6 address the relevance of social science data for invasive species management (i.e. risk perception and risk communication). Chapter 5 presents the results of a survey held in the Netherlands in order to uncover perceptions of non-native species and associated risks in the public domain. In addition, it explores possible relationships between these lay public perceptions of non-native species and values and meanings attributed to nature (i.e. their visions of nature). Chapter 6 links risk perception and risk communication. It entails an evaluation of the effectiveness of a voluntary policy instrument and associated public outreach campaigns in increasing public awareness and, ultimately, in preventing new introductions. The policy instrument in question is a code of Chapter 1

22 conduct for the sale and use of aquatic plants and was signed by the Ministry of Economic Affairs, regional water authorities and the horticultural sector of the Netherlands. This study combines quantitative and qualitative social science methods to measure the effect of the code of conduct among all relevant stakeholders (i.e. the government, commercial sector and the general public). It reports changes in respondents’ level of knowledge, in their views on the introductions of non-native species and in their compliance with the measures issued in the code of conduct. Finally, the results from five case studies will be integrated and discussed in the synthesis (Chapter 7). This chapter shows what lessons can be learned for the development of an interdisciplinary approach to biological invasions and how scientific knowledge may aid effective risk management of wicked problems, as exemplified by the Crow case mentioned above.

References Andersen MC, Adams H, Hope B et al. (2004) Risk assessment for invasive species. Risk Analysis 24:787-793 Andreu J, Vilà M, Hulme PE (2009) An assessment of stakeholder perceptions and management of noxious alien plants in Spain. Environmental Management 43:1244-1255 Austin Z, Raffaelli DG, White PCL (2013) Interactions between ecological and social drivers in determining and managing biodiversity impacts of deer. Biological Conservation 158:214- 222 Bampfylde CJ, Peters JA, Bobeldyk AM (2010) A literature analysis of freshwater invasive species research: are empiricists, theoreticians, and economists working together? Biological Invasions 12:1207-1219 Bayliss HR, Stewart GB, Wilcox A et al. (2013) A perceived gap between invasive species research and stakeholder priorities. NeoBiota 19:67-82 Bertolino S (2009) Animal trade and non-indigenous species introduction: the world-wide spread of squirrels. Diversity and Distributions 15:701-708 Binimelis R, Monterroso I, Rodriguez-Labajos B (2007) A social analysis of the bioinvasions of Dreissena polymorpha in Spain and Hydrilla verticillata in Guatemala. Environmental Management 40:555-566 Blackburn TM, Pysek P, Bacher S et al. (2011) A proposed unified framework for biological invasions. Trends in Ecology & Evolution 26:333-339 Bos D, Moerkens D (2013) Waterschappen en invasieve exoten. Themadag Werkgroep Exoten: Hoe moeten we nu eigenlijk omgaan met exoten? Over perceptie, risicobeoordeling en beleid. Werkgroep Ecologisch Waterbeheer / NECOV, Baarn, The Netherlands (in Dutch) Branquart E (2007) Guidelines for environmental impact assessment and list classification of non-native organisms in Belgium. Belgian Biodiversity Platform, Belgium, pp. 4 Bremner A, Park K (2007) Public attitudes to the management of invasive non-native species in Scotland. Biological Conservation 139:306-314 Briski E, Ghabooli S, Bailey S et al. (2012) Invasion risk posed by macroinvertebrates transported in ships’ ballast tanks. Biological Invasions 14:1843-1850 Brunel S (2009) Pathway analysis: aquatic plants imported in 10 EPPO countries. EPPO Bulletin 39:201-213 Brunel S, Fernández-Galiano E, Genovesi P et al. (2013) Invasive alien species: a growing but neglected threat? In: European Environmental Agency (eds) Late lessons from early warnings: science, precaution, innovation. European Environmental Agency, pp. 518-540 General introduction

23 Butchart SHM, Walpole M, Collen B et al. (2010) Global biodiversity: indicators of recent declines. Science 328:1164-1168 Carlton JT, Ruiz G (2005) The magnitude and consequences of bioinvasions in marine ecosystems: implications for conservation biology. In: Norse E and Crowder L (eds) Marine Conservation Biology. Island Press, Washington, DC, pp. 123-148 Copp GH (2013) The Fish Invasiveness Screening Kit (FISK) for non-native freshwater fishes: a summary of current applications. Risk Analysis 33:1394-1396 Crutzen PJ (2002) Geology of mankind. Nature 415:23 D’hondt B, Vanderhoeven S, Roelandt S, et al. (2014) Harmonia+ and Pandora+: first-line screening tools for potentially invasive organisms - beta version. Belgian Biodiversity Platform, Brussels, Belgium, 57 pp. EEA (2012) Impacts of invasive alien species in Europe. EEA Technical Report No. 16/2012, Copenhagen, Denmark, pp. 114 Elton CS (1958) The ecology of invasions by animals and plants. Methuen, London Endter-Wada J, Blahna D, Krannich R et al. (1998) A framework for understanding social science contributions to ecosystem management. Ecological Applications 8:891-904 Epanchin-Niell RS, Hufford MB, Aslan CE et al. (2009) Controlling invasive species in complex social landscapes. Frontiers in Ecology and the Environment 8:210-216 EPPO (2013) Workshop conclusions. EPPO/CoE/IUCN ISSG International Workshop “How to communicate on pests and invasive alien plants?”, October 8-10 2013. Oeiras, Portugal, pp. 1 Esler K, Prozesky H, Sharma G et al. (2010) How wide is the “knowing-doing” gap in invasion biology? Biological Invasions 12:4065-4075 Essl F, Dullinger S, Rabitsch W et al. (2011) Socioeconomic legacy yields an invasion debt. Proceedings of the National Academy of Sciences of the United States of America 108:203- 207 European Commission (2013) Proposal for a regulation of the European parliament and of the council on the prevention and management of the introduction and spread of invasive alien species. COM/2013/0620, Brussels, Belgium, pp. 36 Falk-Petersen J, Bøhn T, Sandlund O (2006) On the numerous concepts in invasion biology. Biological Invasions 8:1409-1424 García-Llorente M, Martín-López B, González JA et al. (2008) Social perceptions of the impacts and benefits of invasive alien species: implications for management. Biological Conservation 141:2969-2983 García-Llorente M, Martín-López B, Nunes P et al. (2011) Analyzing the social factors that influence willingness to pay for invasive alien species management under two different strategies: eradication and prevention. Environmental Management 48:418-435 Gellis Communications (2007) Scoping study for an EU wide communications campaign on biodiversity and nature. Final report to the European Commission/DG ENV, Brussels, Belgium, pp. 57 Genovesi P, Shine C (2003) European strategy on invasive alien species. Nature and Environment, No. 137. Council of Europe Publishing, Strasbourg, pp. 68 Heger T, Pahl A, Botta-Dukát Z et al. (2013a) Conceptual frameworks and methods for advancing invasion ecology. Ambio 42:527-540 Heger T, Saul W-C, Trepl L (2013b) What biological invasions ‘are’ is a matter of perspective. Journal for Nature Conservation 21:93-96 Hofhuis A, Reimerink J, Reusken C et al. (2009) The hidden passenger of Lucky Bamboo: do imported Aedes albopictus mosquitoes cause Dengue virus transmission in the Netherlands? Vector-Borne and Zoonotic Diseases 9:217-220 Chapter 1

24 Huenneke L, Glick D, Waweru FW et al. (1988) SCOPE program on biological invasions: a status report. Conservation Biology 2:8-10 Hulme PE, Bacher S, Kenis M et al. (2008) Grasping at the routes of biological invasions: a framework for integrating pathways into policy. Journal of Applied Ecology 45:403-414 International Chamber of Shipping (2013) Shipping facts: shipping and world trade. Online source: http://www.ics-shipping.org/shipping-facts/shipping-and-world-trade (Accessed February 25, 2014) Jeschke JM, Strayer DL (2005) Invasion success of vertebrates in Europe and North America. Proceedings of the National Academy of Sciences of the United States of America 102:7198- 7202 Kapler EJ, Thompson JR, Widrlechner MP (2012) Assessing stakeholder perspectives on invasive plants to inform risk analysis. Invasive Plant Science and Management 5:194-208 Kettunen M, Genovesi P, Gollasch S et al. (2009) Technical support to EU strategy on invasive alien species (IAS) - assessment of the impacts of IAS in Europe and the EU. Institute for European Environmental Policy, Brussels, pp. 44 Kueffer C, Hirsch Hadorn G (2008) How to achieve effectiveness in problem-oriented landscape research: the example of research on biotic invasions. Living Reviews in Landscape Research 2, Online source: www.livingreviews.org/lrlr-2008-2 (Accessed February 25, 2014) Kumschick S, Richardson DM (2013) Species-based risk assessments for biological invasions: advances and challenges. Diversity and Distributions 19:1095-1105 Larson BMH (2007) An alien approach to invasive species: objectivity and society in invasion biology. Biological Invasions 9:947-956 Levitt T (1983) The globalization of markets. Harvard Business Review, May/June issue, pp. 92-102 Leung B, Roura-Pascual N, Bacher S et al. (2012) TEASIng apart alien species risk assessments: a framework for best practices. Ecology Letters 15:1475-1493 Leuven RSEW, Velde G, Baijens I et al. (2009) The river Rhine: a global highway for dispersal of aquatic invasive species. Biological Invasions 11:1989-2008 Liebhold AM, Brockerhoff EG, Garrett LJ et al. (2012) Live plant imports: the major pathway for forest insect and pathogen invasions of the US. Frontiers in Ecology and the Environment 10:135-143 Liu S, Sheppard A, Kriticos D et al. (2011) Incorporating uncertainty and social values in managing invasive alien species: a deliberative multi-criteria evaluation approach. Biological Invasions 13:2323-2337 Lövei GL (1997) Biodiversity: global change through invasion. Nature 388:627-628 Lowe S, Browne M, Boudjelas S et al. (2000) 100 of world’s worst invasive alien species: a selection from the Global Invasive Species Database. Invasive Species Specialist Group, IUCN, pp. 12 Mann CC (2011) 1493: Uncovering the new world Columbus created. Random House, New York Masin S, Bonardi A, Padoa-Schioppa E et al. (2014) Risk of invasion by frequently traded freshwater turtles. Biological Invasions 16:217-231 McNeely JA (2001) The great reshuffling: human dimensions of invasive alien species. International Union for Conservation of Nature and Natural Resources. IUCN, Gland, Switzerland; Cambridge, UK, pp. 242 Millennium Ecosystem Assessment (2005) Ecosystems and human well-being. Island Press, Washington, DC, pp. 53 Mills P, Dehnen-Schmutz K, Ilbery B et al. (2011) Integrating natural and social science perspectives on plant disease risk, management and policy formulation. Philosophical Transactions of the Royal Society B: Biological Sciences 366:2035-2044 General introduction

25 Paalvast P, Van der Velde G (2011) New threats of an old enemy: the distribution of the shipworm Teredo navalis L. (Bivalvia: Teredinidae) related to climate change in the Port of Rotterdam area, the Netherlands. Marine Pollution Bulletin 62:1822-1829 Padilla DK, Williams SL (2004) Beyond ballast water: aquarium and ornamental trades as sources of invasive species in aquatic ecosystems. Frontiers in Ecology and the Environment 2:131- 138 Pejchar L, Mooney HA (2009) Invasive species, ecosystem services and human well-being. Trends in Ecology & Evolution 24:497-504 Pot R (2002) Invasion and management of Floating Pennywort (Hydrocotyle ranunculoides L.f.) and some other species in the Netherlands. In: Dutartre A, Montel M et al. (eds) Proceedings of the 11th EWRS International Symposium on Aquatic Weeds. Moliets et Maa (France), pp. 435-438 Pyšek P, Jarosik V, Hulme PE et al. (2010) Disentangling the role of environmental and human pressures on biological invasions across Europe. Proceedings of the National Academy of Sciences of the United States of America 107:12157-12162 Qvenild M (2013) Wanted and unwanted nature: landscape development at Fornebu, Norway. Journal of Environmental Policy & Planning 16:183-200 Reichard SH, White P (2001) Horticulture as a pathway of invasive plant introductions in the United States. Bioscience 51:103-113 Ricciardi A, Kipp R (2008) Predicting the number of ecologically harmful exotic species in an aquatic system. Diversity and Distributions 14:374-380 Richardson DM, Pyšek P (2008) Fifty years of invasion ecology – the legacy of Charles Elton. Diversity and Distributions 14:161-168 Richardson DM, Pyšek P, Carlton JT (2010) A compendium of essential concepts and terminology in invasion ecology. In: Richardson DM (ed) Fifty years of invasion ecology. Wiley-Blackwell, Oxford, UK, pp. 409-420 Richardson DM, Pysek P, Simberloff D et al. (2008) Biological invasions - the widening debate: a response to Charles Warren. Progress in Human Geography 32:295-298 Rittel HWJ, Webber MM (1973) Dilemmas in a general theory of planning. Policy Sciences 4:155-169 Samways MJ (1999) Editorial: Translocating fauna to foreign lands: here comes the Homogenocene. Journal of Insect Conservation 3:65-66 Sharp RL, Larson LR, Green GT (2011) Factors influencing public preferences for invasive alien species management. Biological Conservation 144:2097–2104 Slaterus R, Aarts B, Van den Bremer L (2009) De Huiskraai in Nederland: risicoanalyse en beheer. SOVON-onderzoeksrapport 2009/08. SOVON Vogelonderzoek Nederland, Beek- Ubbergen, pp. 59 Slimak MW, Dietz T (2006) Personal values, beliefs, and ecological risk perception. Risk Analysis 26:1689-1705 Tricarico E (2012) A review on pathways and drivers of use regarding non-native freshwater fish introductions in the Mediterranean region. Fisheries Management and Ecology 19:133-141 Van Leeuwen CJ, Vermeire TG (2007) Risk assessment of chemicals: an introduction. Second edition. Springer, Dordrecht, the Netherlands Van der Weijden W, Leewis R, Bol P (2007) Biological globalisation. Bio-invasions and their impacts on nature, the economy and public health. KNNV publishing, Utrecht, The Netherlands Vanderhoeven S, Piqueray J, Halford M et al. (2011) Perception and understanding of invasive alien species issues by nature conservation and horticulture professionals in Belgium. Environmental Management 47:425-442 Chapter 1

26 Vilà M, Basnou C, Pyšek P et al. (2009) How well do we understand the impacts of alien species on ecosystem services? A pan-European, cross-taxa assessment. Frontiers in Ecology and the Environment 8:135-144 Von der Lippe M, Bullock JM, Kowarik I et al. (2013) Human-mediated dispersal of seeds by the airflow of vehicles. Plos One 8:e52733 Vugteveen P, Lenders HJR, Van den Besselaar PAA (2014) The dynamics of interdisciplinary research fields: the case of river research. Scientometrics 100:73-96 Ware C, Bergstrom DM, Muller E et al. (2012) Humans introduce viable seeds to the Arctic on footwear. Biological Invasions 14:567-577 Warren CR (2011) Nativeness and nationhood: what species belong in post-devolution Scotland? In: Rotherham ID and Lambert RA (eds) Invasive and introduced plants and animals: human perceptions, attitudes and approaches to management. Earthscan, London, UK, pp. 67-79 Westphal M, Browne M, MacKinnon K et al. (2008) The link between international trade and the global distribution of invasive alien species. Biological Invasions 10:391-398 Williamson MH (1996) Biological Invasions. Chapman and Hall, London, UK Willis HH, Dekay ML (2007) The roles of group membership, beliefs, and norms in ecological risk perception. Risk Analysis 27:1365-1380 Wittenberg R, Cock MJW (2001) Invasive alien species: a toolkit of best prevention and management policies. CABI Pub, Wallingford, UK, pp. 228 Wodzicki K (1965) The status of some exotic vertebrates in the ecology of New Zealand. In: Baker HG and Stebbins GL (eds) The genetics of colonizing species. Proceedings of the First International Union of Biological Sciences Symposia on General Biology. Academic Press, New York and London, pp. 425-458

Chapter 2

Sensitivity of native and non-native mollusc species to changing river water temperature and salinity

Laura Verbrugge, Aafke Schipper, Mark Huijbregts, Gerard van der Velde and Rob Leuven

Biological Invasions 14: 1187-1199, 2012 Chapter 2

Abstract Climate change may strongly affect the abiotic conditions in riverine ecosystems, for example by changing water temperature regimes and salinisation due to sea water intrusion and evaporation. We analysed the effects of changes in water temperature and salinity on the species pool of freshwater molluscs in the river Rhine. Species sensitivity 30 distributions (SSDs) for maximum temperature and salinity tolerance were constructed for native and non-native species that are currently present in the river Rhine. The maximum temperature tolerance was significantly higher for non-native mollusc species than native ones. For salinity tolerance, no significant difference was found between the two groups. The SSDs were used to determine the potentially not occurring fractions (PNOFs) of each species group corresponding with the yearly maximum water temperature and salinity levels recorded in (1) different river sections for the extreme warm and dry year 2003, and (2) the river Rhine at Lobith (The Netherlands) over the period 1960-2009. Changing temperature and salinity conditions in the river Rhine over the past 50 years corresponded with a net increase in PNOF for native species. This was mainly due to rising river water temperatures, which had a larger influence than decreasing salinity levels. For non-native species no change in PNOF was found, indicating that future temperature rise will disproportionally affect native mollusc species. Validation of the PNOF estimated for Lobith with the not occurring fraction (NOF) of mollusc species derived from monitoring data revealed similar trends for native as well as non-native mollusc species richness. The increase in the PNOF accounted for 14 per cent of the increase in the NOF. The construction and application of SSDs appeared a promising approach to address the separate and combined effects of changing abiotic conditions on native and non-native species pools.

Introduction Physiological responses to environmental conditions may differ between native and non-native freshwater species, which may influence establishment of non-native species and interspecific competition (Karatayev et al. 2009; Leuven et al. 2007, 2011). Climate change may affect environmental conditions, and subsequently bioinvasions, by altering the pool of potential invaders and influencing the chance that non-native species will establish (Rahel and Olden 2008). Studies on the effects of climate change in lake and river systems have shown changes in freshwater species composition and diversity for fish (Buisson et al. 2008; Daufresne and Boet 2007) and macroinvertebrates (Burgmer et al. 2007; Chessman 2009; Daufresne et al. 2004; Mouthon and Daufresne 2006). Abiotic changes in river systems typically include increases in water temperature, river dynamics and salinity (Gornitz 1991; Webb 1996). So far, however, most research has focused on water temperature effects on fish species (Chu et al. 2005; Jackson and Mandrak 2002; Lehtonen 1996; Leuven et al. 2007, 2011). Responses of macroinvertebrate species to climate change are difficult to predict due to a lack of knowledge on species-specific physiological tolerances (Heino et al. 2009). Rising water temperatures may lead to replacement of cold water mollusc species by more thermophilic ones (Daufresne et al. 2004), but the mechanisms that may explain this shift are not yet understood. As molluscs constitute a large share of the group of macroinvertebrate invaders (Karatayev et al. 2009; Leuven et al. 2009) and invasive, fouling molluscs have serious economic and Sensitivity of native and non-native mollusc species ecological impacts (Connelly et al. 2007; Pimentel et al. 2005; Strayer 2010; Vanderploeg et al. 2002), there is a particular need for knowledge on physiological tolerances of these species. Knowledge on facilitating or limiting factors for the establishment of non-native mollusc species could be helpful to predict future species replacements and to derive management options for invasive species. The aim of this study was to identify differences in maximum temperature and salinity 31 tolerance between native and non-native mollusc species and to assess the impact of changes in water temperature and salinity on the occurrence of both species groups in the river Rhine. To this end, we first analysed which mollusc species are currently present in the river Rhine. Next, we constructed species sensitivity distributions (SSDs) with regard to temperature and salinity tolerance and used these relations to analyse differences in sensitivity between native and non-native mollusc species. We applied the SSDs to assess the potentially not occurring fraction (PNOF) of species in various sections of the river Rhine using temperature and salinity data obtained during the heat wave in the year 2003. Further, we analysed the separate and combined effects of changes in water temperature and salinity on the potential occurrence of mollusc species in the river Rhine at Lobith over a period of 50 years (i.e. 1960-2009). Finally, we compared the temporal trends in PNOF to the actual not occurring fraction (NOF) of mollusc species using monitoring data obtained at Lobith from 1988 through 2003.

Material and methods

Species sensitivity distributions In order to assess the differences in sensitivity to thermal and saline stress, SSDs were constructed for native as well as non-native mollusc species. An SSD is a statistical distribution that describes the variation in a (group of) species in sensitivity to an environmental stressor (Leuven et al. 2007, 2011; Posthuma et al. 2002; Smit et al. 2008). In our study, the calculated fraction of species affected is addressed as the potentially not occurring fraction (PNOF) (Van Zelm et al. 2007), representing the fraction of mollusc species potentially excluded from the river Rhine because of water temperature and salinity limitations. Various distribution curves can be used to describe an SSD, because there are no theoretical grounds to favour a particular distribution function. In this study, the logistic distribution was used, as outlined by Aldenberg and Slob (1993) and recently used by De Zwart (2005). In a logistic distribution, the PNOF is determined by the location parameter alpha (α) and the scale parameter beta (β) (Eq. 1).

1 PNOF = α − x− )( β (1) 1+e where x represents the environmental stressor (temperature in °C or salinity in ‰). The location parameter α equals the sample mean of the species-specific upper tolerance values. The scale parameter β of the logistic distribution depends on the sample standard deviation (SD) of the upper tolerance values (Aldenberg and Slob 1993). Assuming independent action, the combined effects of both temperature (PNOFT) and salinity (PNOFS) on the occurrence of species can be calculated (Eq. 2) (Traas et al. 2002). Chapter 2

PNOFTS = 1 – (1 – PNOFT ) × (1 – PNOFS ) (2)

Parameterization and comparison 32 A list of freshwater mollusc species present in the river Rhine was compiled based on the results of a large-scale international survey of macroinvertebrate species conducted in 2000 (IKSR 2002) and a more recent study on macroinvertebrate invaders by Leuven et al. (2009). Next, a database of upper tolerance values was set up with data from the literature (Table 2.1). Data were obtained from scientific articles and a survey of freshwater molluscs of the Netherlands (Gittenberger et al. 1998) (see Table 2.1 for

references). Upper tolerance values represent the maximum temperature (Tmax; °C) or salinity (Smax; ‰) at which individuals were recorded in the field. If the upper tolerance value for a species was given as a range or if more than one value was found in the literature, the highest value was added to the database. If available, we also included the temperature and salinity ranges measured over the sites investigated, as this may confirm the absence of species at environmental conditions exceeding their maximum tolerance levels. Next, we tested the reliability of the field-derived maximum tolerance levels by a comparison with lethal temperature and salinity levels for 50 per cent of the species based on laboratory tests, which have been reported for a few of the species. A paired- samples t-test was used for the comparison (SPSS 15.0). Field-derived tolerance levels

did not significantly differ from LC/LT50 values reported from available laboratory tests for salinity (n = 10; P = 0.71) and temperature (n = 6; P = 0.22) (unpublished data). The salinity tolerance data were log-transformed, because of their skewed distribution. The temperature tolerance data were within one order of magnitude, obviating the need for log-transformation. Differences in upper tolerance limits between the two species groups were tested with independent-samples t-tests (SPSS 15.0) and were considered to be statistically significant atP < 0.05.

Table 2.1 Maximum temperature and salinity tolerances for native and non-native mollusc species of the river Rhine, including available ranges measured at sampling sites per species in brackets.

Species Abbr. Smax (‰) Refs. Tmax (°C) Refs. Native species Acroloxus lacustris (Linnaeus, 1758) Al 3 8 30 (0-33) 9;15 Ancylus fluviatilis (Müller, 1774) Af 4 8 30 (0-33) 9;15;35 Anodonta anatina (Linnaeus, 1758) Aa 3 8 24 1;24 Anodonta cygnea (Linnaeus, 1758) Ac 2 8 28 (0-32) 1;15;24;29 Bathyomphalus contortus (Linnaeus, 1758) Bc 8.5 (0-33.5) 5;8 Bithynia leachii (Sheppard, 1823) Bl 6 8 25 (0-32) 15 Bithynia tentaculata (Linnaeus, 1758) Bt 12 (0-33.5) 5;8 30 (0-32) 15 Galba truncatula (Müller, 1774) Gt 19 (0-33.5) 5;8 25 8 Gyraulus albus (Müller, 1774) Ga 5 8 30 (0-32) 15 Lymnaea stagnalis (Linnaeus, 1758) Ls 7 8 Mercuria anatina (Poirot, 1801)a Mc 5.5 8 Sensitivity of native and non-native mollusc species

Table 2.1 (Continued)

Species Abbr. Smax (‰) Refs. Tmax (°C) Refs. Native species Physa fontinalis (Linnaeus, 1758) Pf 11 (0-33.5) 5;8 25 (0-32) 15 Pisidium amnicum (Müller, 1774) Pam 0.5 8 29.5 (0-32) 15;23 Pisidium casertanum (Poli, 1791) Pcm 3 14 33 Pisidium henslowanum (Sheppard, 1823) Ph 1.5 8 Pisidium moitessierianum Paladilhe, 1866 Pm 0.5 8 Pisidium nitidum Jenyns, 1832 Pn 3.5 14 Pisidium supinum Schmidt, 1851 Ps 0.5 14 Planorbis carinatus (Müller, 1774) Pcs 3 8 Planorbis planorbis (Linnaeus, 1758) Pp 11 (0-33.5) 5;8 29 (0-29) 4 Pseudanodonta complanata (Rossmässler, 1835) Pca 0.5 8 24 (0-24) 1 Radix auricularia (Linnaeus, 1758) Ra 6 (0-33.5) 5;8;28 25 (0-32) 15;30 Radix balthica (Linnaeus, 1758)b Rb 14 (0-33.5) 5;8 32 (0-32) 13;15 Sphaerium corneum (Linnaeus, 1758) Sc 5 8 Sphaerium rivicola (Lamarck, 1818) Sr 2 8 Sphaerium solidum (Normand, 1844) Ss 2 8 Stagnicola corvus (Gmelin, 1791) - Theodoxus fluviatilis (Linnaeus, 1758) Tf 18 8;10;28 Unio crassus (Philipsson, 1788)c Uc 0.5 8 Unio pictorum (Linnaeus, 1758) Up 3 8 28 (0-32) 1;15;24 Unio tumidus Philipsson, 1788 Ut 3 8 24 (0-24) 1 Valvata cristata Müller, 1774 Vc 5 (0-33.5) 5;8 Valvata piscinalis (Müller, 1774) Vp 5 8 29.5 (0-29.5) 23 Viviparus viviparus (Linnaeus, 1758)d Vv 3 8 25 (0-32) 15 Non-native species Corbicula fluminalis (Müller, 1774) Cfs 27 (0-34.5) 8;20;21 Corbicula fluminea (Müller, 1774) Cfa 17 (0-34.5) 8;12;21 37 (0-42) 3;6;17;19 Dreissena polymorpha (Pallas, 1771) Dp 6 8;11;16;33 34 11;15;18;26 Dreissena rostriformis bugensis Andrusov, 1897 Dr 5 (0-33.5) 11;12;27 34 11;32 Ferrissia wautieri (Mirolli 1960)e Fw 1 8 33 (0-33) 9;31 Lithoglyphus naticoides (Pfeiffer, 1828) Ln 3 8 29.5 (0-29.5) 22 Menetus dilatatus (Gould, 1841) Md 32 2;25 Musculium transversum (Say, 1829) - Physella acuta (Draparnaud, 1805)f Pac 8 (0-33.5) 5;8 35 (7-44) 7;8;15 Potamopyrgus antipodarum (Gray, 1843)g Pan 28 (0-33.5) 5;8 30 (0-34) 8;15;34

References (Refs.) to studies with highest reported tolerance value for a species in italics. References included: 1:Aldridge (1999); 2:Berger and Dzięczkowski (1979) 3:Britton and Morton (1982); 4:Costil and Daguzan (1995); 5:reviewed in Costil et al. (2001); 6:Dreier and Tranquilli (1981); 7:Forcart (1948); 8:reviewed in Gittenberger et al. (1998); 9:Hadderingh et al. (1987); 10:Kangas and Skoog (1978); 11:reviewed in Karatayev et al. (1998); 12:reviewed in Karatayev et al. (2007); 13:Krkac (1979); 14:reviewed in Kuiper and Wolff (1970); 15:Langford (1971); 16:McMahon (1996); 17:McMahon and Williams (1986); 18:Mihuc et al. (1999); 19:Morgan et al. (2003); 20:Morton (1986); 21:Morton and Tong (1985); 22:Mouthon (2007); 23:Mouthon and Daufresne (2008); 24:Müller and Patzner (1996) 25:Müller et al. (2005); 26:Orlova (2002); 27:Orlova et al. (2005); 28:reviewed in Perez-Quintero (2007); 29:Ricken et al. (2003); 30:Rossetti et al. (1989); 31:Van der Velde (1991); 32:reviewed in Van der Velde et al. (2010); 33:Walton (1996); 34:Winterbourn (1969); 35:Wulfhorst (1991). a Synonymous with Mercuria confusa; b Synonymous with Radix peregra / ovata; c probably extinct; d Species is regarded as non-native in Germany and the Upper Rhine (Kinzelbach 1995; Bernauer and Jansen 2006) however the non-native status is disputed for the Dutch part of the river Rhine as fossil remnants of this species have been found (Gittenberger et al. 1998); e Synonymous with Ferrissia clessiniana; taxonomic status uncertain, possibly Ferrissia fragilis (Walther et al. 2006); f Synonymous with Physa acuta, Haitia acuta, Physella costatella and Physella heterostropha (Dillon et al. 2002); g Synonymous with Potamopyrgus jenkinsi. Chapter 2

River Rhine case study and comparison with survey data The SSDs for native and non-native molluscs for the two stressors were used to calculate the PNOFs of each group corresponding with water temperatures and salinity levels recorded in the river Rhine. The river Rhine is one of the large rivers in Europe, rising in the Swiss and Austrian Alps and flowing through Germany, France and the Netherlands 34 to the North Sea, and is characterized by a high richness and abundance of non-native species (Arbačiauskas et al. 2008; Bij de Vaate et al. 2002; Leuven et al. 2009; Panov et al. 2009). To obtain insight into spatial differences along the river, PNOFs were calculated for various river sections based on temperature and salinity data from seven water quality measurement stations. These data were obtained from the International Commission for the Protection of the Rhine (IKSR), the Directorate-General for Public Works and Water Management (2009) and Uehlinger et al. (2009) for the year 2003 (i.e. an extreme dry and warm year). Potential influences of temporal changes in water temperature and salinity were assessed based on measurements conducted in the surface water layer of the main river channel near the Dutch-German border at Lobith. Data were obtained from a web-based portal (i.e. Waterbase) and covered the period 1960-2009 (Directorate- General for Public Works and Water Management 2009). Water temperature values from the Directorate-General for Public Works and Water Management (2009) were obtained as daily measurements with an accuracy of 0.1 °C. Water temperature data from the IKSR portal were available as maximum water temperatures of two-week periods from continuous measurements (IKSR 2011). The salt content of the river Rhine was expressed as conductivity (mS/m) which was typically measured twice a month. Conductivity values were transformed to salinity units, using the method described by Grabowski et al. (2009). Yearly maximum water temperatures (°C) and salinities (‰) were used to calculate the PNOFs. Linear regression confidence intervals (95%) were calculated to reveal whether temporal trends in PNOF at Lobith were significant. We compared the PNOFs calculated for Lobith with the actual not occurring fraction (NOF) of mollusc species derived from survey data (Eq. 3).

NOF = 1 – R / Rmax (3)

in which R is the number of species found at Lobith and Rmax the total species pool of the river Rhine (i.e. the same number of species used for calculating the PNOF). Monitoring data on molluscs in the river Rhine at Lobith were obtained from Limnodata Neerlandica of the Dutch Foundation for Applied Water Research STOWA (www.limnodata.nl). These data originated from monitoring activities over the period 1988-2003, including sampling of hard substrates (groyne stones, rip rap, large woody debris), sediment (core and Van Veen samplers), artificial substrates (marbles), and other microhabitats (dip nets). All available survey data were pooled per year and regression lines were fitted through the resulting NOFs in order to facilitate comparison with the PNOFs. Sensitivity of native and non-native mollusc species

Results

Species sensitivity distributions In total 34 native and 10 non-native mollusc species were recorded in the river Rhine. The non-native species originate from North America (n = 4), the Ponto-Caspian Area (n = 3), Asia (n = 2) and New Zealand (n = 1). The non-native status of one species is 35 still ambiguous (i.e. Ferrissia wautieri). Temperature tolerance data were found for 18 native and 8 non-native species, accounting for 53 per cent and 80 per cent of their species pool in the river Rhine, respectively. The maximum temperature tolerance of native species ranged from 24.0 to 32.0 °C. For non-native species this range was 29.5 to 37.0 °C (Figure 2.1). The maximum temperature tolerance was significantly higher for non-native than for native species (P < 0.01).

100% Rb Cfa Bt, Ga, Al, Af

80% Pac

Pam, Vp Dp, Dr

60% Pp

Up, Ac

Ra, Pf, Bl, Vv, Gt Fw 40%

Md

Pan 20% Aa, Pca, Ut Native

Potentially Not Occurring Fraction NotOccurring Potentially Ln Non-native 0% 15 20 25 30 35 40 Tmax (°C)

Figure 2.1 Species sensitivity distributions for maximum temperature tolerances of native and non-native molluscs of the river Rhine. The data points represent individual species’ tolerances based on Hazen plotting positions (Native: n = 18; α = 27.39, β = 1.49; Non-native: n = 8; α = 33.06, β = 1.39). Full species names can be found in Table 2.1

The SSDs for salinity were based on data for 33 native and 8 non-native species, constituting 97 per cent and 80 per cent of their species pool in the river Rhine, respectively. For native species the maximum salinity tolerance ranged from 0.5 to 19.0 ‰, while for non- native species this range was 1.0 to 28.0 ‰. The mean maximum salinity tolerance was not significantly different between native and non-native species (P = 0.08), although all data points belonging to the non-native species sensitivity curve were below the native species curve. Two non-native species (Corbicula fluminalis and Potamopyrgus antipodarum) showed a considerably higher salinity tolerance than all native species (Figure 2.2). Chapter 2

100% Tf Gt Rb Bt Pan

Pf, Pp Ls Cfs 80% Bc Bl, Ra

Ga, Vc, Mf Cfa 36 Vp, Sc 60% Al, Pcs, Af Pac Vv, Aa, Pn Pcm, Up, Ut Dp 40% Sr, Ss, Ac Dr

20% Ph L n Native Pam, Pm, Potentially Not Occurring Fraction NotOccurring Potentially Ps, Pca, Uc Non-native Fw 0% 0 5 10 15 20 25 30 Smax (‰)

Figure 2.2 Species sensitivity distributions for maximum salinity tolerances of native and non-native molluscs of the river Rhine. The data points represent individual species’ tolerances based on Hazen plotting positions (Native: n = 33; α = 0.54, β = 0.25; Non-native: n = 8; α = 0.87, β =0.27). Full species names can be found in Table 2.1.

River Rhine case study and comparison with survey data In the summer of 2003, potential salinity effects were minimal in nearly the entire river Rhine, except for the coastal region where the PNOFs for native as well as non-native species were high (Table 2.2). Temperature data yielded higher PNOFs for the Lower and Middle Rhine sections, whereas for the other sections the potential effects were less pronounced. In addition, the PNOFs found for native species were higher than for non- native species, except in the Alpine Rhine where the occurrence of both species groups appeared not to be limited by maximum water temperature.

Table 2.2 Potentially not occurring fractions (PNOFs; in percentages) of native and non-native mollusc species in different river sections of the river Rhine for the extreme warm and dry year 2003.

Station River section Salinity Temperature Native Non-native Native Non-native Maassluis DR 78.8 49.6 14.9 0.3 Lobith DR/LR 1.8 0.8 61.7 2.7 Koblenz MR 1.4 0.6 69.3 3.8 Lauterborg UR 1.0 0.4 40.2 1.1 Wheil am Rhein UR/HR 0.8 0.3 32.5 0.8 Reckingen HR 0.7 0.3 32.5 0.8 Diepoldsau AR 0.7 0.3 0.1 0.0 Data on temperature and salinity of the river sections from the International Commission for the Protection of the Rhine (ICPR), with the exception of Maassluis (data from Waterbase) and Diepoldsau (data derived from Uehlinger et al. 2009). DR: Delta Rhine; LR: Lower Rhine; MR: Middle Rhine; UR: Upper Rhine; HR: High Rhine; AR: Alpine Rhine. Sensitivity of native and non-native mollusc species

The yearly maximum water temperature of the river Rhine at Lobith increased 2.5 °C over the period 1960-2009 (Figure 2.3). The maximum salinity showed an increase over the period 1960-1985 and a steep decline from 0.6 to 0.4 ‰ since the mid-1980s, as a result of effective water pollution control (i.e. international treaties concerned with a reduction in salt load of the river Rhine in 1976). The PNOFs of native and non-native species with regard to water temperatures significantly increased over the period 1960-2009 (P 37 < 0.01; Table 2.3). For native species however, the total increase was higher due to lower

30 0.9

0.8 25 0.7

20 0.6

0.5 °C 15 ‰ 0.4

10 0.3

0.2 5 Temperature 0.1 Salinity

0 0 1960 1970 1980 1990 2000 2010

Year

Figure 2.3 Maximum water temperature and salinity of the river Rhine at Lobith (salinity measurements for the years 1985-1987 were not available).

Table 2.3 Slope (a), intercept (b), statistical probability (P-value) and explained variance (R2) of trends in potentially not occurring fractions (PNOF) and not occurring fractions (NOF) of native and non-native mollusc species.

Slope (a) Intercept (b) R2 P-value PNOF-temperature Native (1960-2009) 3.29E-03 ns 0.19 P < 0.01 Non-native (1960-2009) 8.65E-05 ns 0.15 P < 0.01 PNOF-salinity Native (1960-1976) 1.43E-04 ns 0.31 P < 0.05 Non-native (1960-1976) 5.39E-04 ns 0.31 P < 0.05 Native (1977-2009) -9.98E-04 6.84E-02 0.65 P < 0.01 Non-native (1977-2009) -3.78E-04 2.68E-02 0.65 P < 0.01 PNOF-temperature and salinity Native (1960-2009) 2.75E-03 8.48E-02 0.15 P < 0.01 Non-native (1960-2009) ns 2.05E-02 0.08 P > 0.05 NOF (field monitoring data) Native (1988-2003) 2.01E-02 6.50E-01 0.65 P < 0.01 Non-native (1988-2003) ns 5.50E-01 0.004 P > 0.05 ns: not significant. Chapter 2

maximum tolerance levels (Figure 2.4A). The trends of the PNOFs for salinity stress include a turning point. After the initiation of international treaties in 1976, the PNOFs of both species groups at Lobith have significantly declined (P < 0.01; Table 2.3), and PNOFs for both native and non-native species are currently lower than in 1960 (Figure 2.4B). As the effects of temperature are considerably stronger than the salinity effects, 38 the trend lines for the combined effects of these stressors largely resemble the trend lines for temperature effects (Figure 2.4C). For native species, a statistically significant increase in PNOF was found (P < 0.01; Table 2.3). For non-native species no significant change was found (P > 0.05; Table 2.3).

8% A B Native 1960-1976 50% Native 7% Non-native 1960-1976 Non-native Native 1977-2009 6% 40% Non-native 1977-2009 5% 30% 4% PNOF PNOF 20% 3% 2% 10% 1% 0% 0% 1960 1970 1980 1990 2000 2010 1960 1970 1980 1990 2000 2010 Year Year

C 50% Native Non-native 40%

30%

PNOF 20%

10%

0% 1960 1970 1980 1990 2000 2010 Year Figure 2.4 Potentially not occurring fraction (PNOF) of native and non-native molluscs at Lobith in relation to yearly maximum water temperature conditions (A), yearly maximum salinity conditions (B) and both stressors combined under the assumption of additive effects (C) for the period 1960-2009.

Monitoring data on macroinvertebrates allowed for trend analysis of the mollusc species richness for the period 1988-2003 in the river Rhine at Lobith. The NOF of non-native species remained fairly constant over this period, while the NOF of native species showed an increase, which indicates a gradual decrease in species richness (P < 0.01; Figure 2.5). These trends agree well with the trends in PNOF for both non-native and native species (Figure 2.4C), although the increase in the PNOF of native mollusc species is less pronounced than the increase in the NOF (Table 2.3). A comparison of the slopes of the regression lines (Table 2.3) suggests that the increase in PNOF accounts on average for 14 per cent of the increase in the NOF. Sensitivity of native and non-native mollusc species

100%

80%

60% 39 NOF 40%

Native 20% Non-native

0%

1988 1990 1992 1994 1996 1998 2000 2002 Year

Figure 2.5 Not occurring fraction (NOF) of native and non-native molluscs at Lobith derived from monitoring data for the period 1988-2003.

Discussion

Species sensitivity distributions Based on field-derived maximum tolerance levels for water temperature and salinity, we constructed SSDs for native and non-native mollusc species in the river Rhine. The species included currently occur in this river, which increases the applicability of our SSDs in site-specific assessments (De Vries et al. 2008). Input data for the SSDs comprised maximum tolerance levels derived from field observations. The use of field observations to derive tolerance levels is open to debate (Von Stackelberg et al. 2002), as it cannot be ruled out that the species included are able to live in warmer or more saline waters than indicated by the field observations. For both temperature and salinity, a comparison of field-based maximum tolerance levels with LC50 values reported from laboratory tests revealed no significant difference. This corresponds with findings in previous studies, where comparisons of laboratory- and field-derived salinity tolerance data revealed that salinities lethal to 50 per cent of individuals (LC50) were correlated with the maximum salinity at which a species had been collected in the field, both at family and species level (Horrigan et al. 2007; Kefford et al. 2004). Moreover, for 15 species the field-based maximum temperature tolerance was derived from occurrence data of surveys that also include water bodies with a wider temperature range (Table 2.1); for maximum salinity this holds for 13 species. This supports that our field-based SSDs indeed reflect maximum temperature and salinity tolerances. Unfortunately, for the remaining species data on temperature and salinity ranges of water bodies were not reported. We chose to accept the limitations of field data for reasons of data availability, as laboratory data for temperature tolerance were available for only six mollusc species and several species groups (e.g. Sphaeriidae and Unionidae) are only rarely the subject Chapter 2

of physiological research. Moreover, other authors suggest that tolerance levels derived from field data may be more environmentally relevant and realistic than reference levels obtained in laboratory tests (Kwok et al. 2008; Leung et al. 2005; Struijs et al. 2011). Our results showed that non-native mollusc species in the river Rhine have a higher maximum temperature tolerance than native species. This agrees with other studies 40 on temperature tolerance of aquatic species. For example, non-native fish species can tolerate higher maximum temperatures than native fish species (Leuven et al. 2007, 2011). Higher tolerance levels for non-native mollusc species also explain their high abundance at sites with elevated temperature (Langford 1971; Müller et al. 2005). The difference between native and non-native species can be explained by the origin of species, as previous studies found significantly higher temperature tolerances for (sub)tropical than for temperate species (De Vries et al. 2008). Salinity tolerances of native and non-native species were not significantly different, which agrees with other recent studies on salinity tolerance of native and non-native macroinvertebrates (Piscart et al. 2011; Van de Meutter et al. 2010). However, our results also show that some non-native species can tolerate considerably higher salinities than native species. Two examples are Corbicula fluminalis and Potamopyrgus antipodarum. These species originate from Asia and New Zealand and started their colonisation in the estuaries and dispersed upstream. Their main vector of intercontinental dispersal is ballast water (Leuven et al. 2009; Nehring 2002), which acts as a strong filter in favour of species with high salinity tolerances. This is, again, consistent with Piscart et al. (2005, 2011), who also found higher tolerance levels for non-native species from outside Eurasia.

River Rhine case study and comparison with survey data Based on the SSDs, we calculated the potentially not occurring fractions (PNOFs) of native and non-native mollusc species corresponding with maximum water temperature and salinity levels recorded in the river Rhine (1) for different river sections in 2003, and (2) at Lobith over the period 1960-2009. Whereas daily measurement data were available for temperature, salinity was measured at two-week intervals, so peak values could have been missed. In comparison with maximum salinity values derived from daily (24h) averaged measurements, which were available for a shorter time span (from 1979 onwards), daily values indeed resulted in maximum salinity values exceeding ours with a maximum of 0.8 ‰. Hence, the PNOFs for maximum salinity conditions calculated in this study are underestimated compared to PNOFs that would be based on daily salinity measurements. However, we preferred the two-week interval data because of the longer time span covered. Moreover, the implications for the overall combined impact of both stressors are minimal in the freshwater sections of the river Rhine, as salinity is a less important stressor than temperature (Table 2.2 and Figure 2.4A-B). As the PNOFs were derived from yearly maximum values obtained from a single measurement location, the resulting patterns and trends should be interpreted with care. Possibly, short term maximum temperature and salinity conditions might be insufficient to induce significant effects on molluscs, indicating that the use of single maximum values may result in overestimated PNOFs. Effects could also be overestimated due to spatial variation in abiotic conditions. In the upper water layer of the main river channel, where measurements are commonly conducted, water temperatures may be higher than Sensitivity of native and non-native mollusc species in deeper water layers that receive inflowing ground water. Indeed, water temperatures measured at the channel floor in the rivers Rhine and Meuse throughout the year were up to 4.5 °C lower than in the upper water layer, confirming that vertical heterogeneity in water temperature may be large (Boderie et al. 2006). Such heterogeneity may create thermal refugia and thus mitigate potential negative temperature effects on organisms. Although it is possible to compare SSDs with actual species richness in a river system 41 (Kefford et al. 2006), validation using species survey data is not straightforward. Our SSD predictions do not account for spatial variability in species richness and additional factors that play a role in determining field species’ distributions (Kefford et al. 2011, 2012). Besides maximum temperature and salinity, other factors may influence the occurrence of mollusc species in the river Rhine, including, for example, wave conditions (Gabel et al. 2011) or minimum temperature (Weitere et al. 2009). In addition, a proper validation requires extensive sampling of species, preferably along an environmental gradient with limited and well documented environmental conditions (Kefford et al. 2006, 2010). As the mollusc survey data used to calculate the NOFs were not specifically obtained for the yearly maximum temperature and salinity values used to calculate the PNOFs, the PNOFs cannot be validated for single years. Yet, although the increase in the PNOF of native mollusc species was less pronounced than the increase in the NOF, our results showed similar temporal trends in empirical and modelled (P)NOF for native as well as non-native mollusc species (Table 2.3). This suggests that comparison with survey data helps to confirm and interpret general trends in species loss predicted with SSDs. Despite the uncertainties associated with the PNOFs, the trends and patterns presented here can be qualitatively evaluated and interpreted. Increasing PNOFs were found in relation to temperature changes from 1960 through 2009, reflecting rising river water temperatures due to thermal pollution and, in particular, global warming (Uehlinger et al. 2009). PNOFs were higher in river sections with higher water temperatures due to large cooling water discharges of power plants and effluents of industrial and communal water treatment facilities, i.e. in the Lower and Middle Rhine (Table 2.2). For salinity, we found a net decrease in PNOF at Lobith for native as well as non-native species, reflecting a reduction of salt water effluents from kali mines following the 1976 Rhine Salt Treaty (Dieperink 2000). In the delta region, however, extreme salinities may occur, which potentially have considerable impact on both native and non-native mollusc species (Table 2.2). Previous research has shown that rising sea water levels and increased evaporation due to climate change may result in higher salinity levels (Bonte and Zwolsman 2010). Therefore, in ecological impact assessments special attention should be paid to areas that are more susceptible to climate change and where effects may be more pronounced. Interpretation of the results from the multiple stressor analysis has to be done carefully. We assumed an additive effect of temperature and salinity, whereas previous research has suggested that the interaction between temperature and salinity is complex (Bradley 1975; Brenko and Calabrese 1969; Verween et al. 2007; Wright et al. 1996). Temperature can either modify the effects of salinity, thereby changing the salinity tolerance range of mollusc species, or vice versa, whereby interactions between salinity and temperature can be species-specific (Browne and Wanigasekera 2000; Kefford et al. 2007). Irrespective of possible interactions, however, effects of salinity in the river Rhine were small relative to temperature effects, reflected by a net increase in PNOF for native species from Chapter 2

1960 to 2009 when both stressors were combined (Figure 2.4C). Combined salinity and temperature changes had no significant effect on non-native species, mainly due to their higher maximum temperature tolerance. Thus, the results of our study indicate that future temperature rise as a result of climate change will disproportionally affect native mollusc species. This corresponds with the findings of Mouthon and Daufresne 42 (2006), who studied the effects of heatwaves on mollusc species. They found that both native species and invaders appear to be struck by heatwaves, but that invaders are able to recover remarkably well. Non-native species like dreissenids and corbiculids are well adapted to unstable habitats, thanks to their high fecundity, fast growth and early maturity allowing rapid (re)colonization (Van der Velde et al. 2010). SSDs based on generic species pools show systematic differences in sensitivity among species from different regions and taxonomic groups (De Vries et al. 2008). By using a river basin specific species pool from one taxonomic group, our SSDs account for these differences. Constructing and applying river basin specific SSDs for native as well as non- native species appeared a promising approach for quantifying and comparing tolerance levels and for assessing separate and combined effects of changing abiotic parameters. In addition to conventional methods for expressing upper tolerance levels of species (i.e. classification of physiological tolerances) our SSD-PNOF approach also allows for prediction of changes in mollusc communities in response to future environmental conditions. More data on species tolerances for various abiotic stressors would facilitate the construction of SSDs, whereas long term surveys of actual species distributions will be helpful to validate the PNOFs. Especially measurements of species richness along environmental gradients and mesocosm studies are required for further validation of PNOFs derived from SSDs.

Acknowledgements We thank associate editor Rob Cowie and two anonymous reviewers for their useful comments on earlier versions of this paper and Frank van Herpen for putting monitoring data of Limnodata Neerlandica (STOWA) at our disposal.

References Aldenberg T, Slob W (1993) Confidence limits for hazardous concentrations based on logistically distributed NOEC toxicity data. Ecotoxicology and Environmental Safety 25:48-63 Aldridge DC (1999) The morphology, growth and reproduction of Unionidae (Bivalvia) in a fenland waterway. Journal of Molluscan Studies 65:47-60 Arbačiauskas K, Semenchenko V, Grabowski M et al. (2008) Assessment of biocontamination of benthic macroinvertebrate communities in European inland waterways. Aquatic Invasions 3:211-230 Berger L, Dzięczkowski A (1979) Północnoamerykański zatoczek Menetus dilatatus (Gould, 1841) (Gastropoda, Planorbidae) w Polsce. Przeglad Zoologiczny 23:34-40 Bernauer D, Jansen W (2006) Recent invasions of alien macroinvertebrates and loss of native species in the upper Rhine River, Germany. Aquatic Invasions 1:55-71 Bij de Vaate A, Jazdzewski K, Ketelaars HAM et al. (2002) Geographical patterns in range extension of Ponto-Caspian macroinvertebrate species in Europe. Canadian Journal of Fisheries and Aquatic Sciences 59:1159-1174 Sensitivity of native and non-native mollusc species

Boderie P, Meijers E, Peñailillo R (2006) Verificatie SOBEK-Landelijk temperatuurmodel. Rapport Q4166. Delft: WL Delft Hydraulics Bonte M, Zwolsman JJG (2010) Climate change induced salinisation of artificial lakes in the Netherlands and consequences for drinking water production. Water Research 44:4411-4424. Bradley BP (1975) Anomalous influence of salinity on temperature tolerances of summer and winter populations of copepod Eurytemora affinis. The Biological Bulletin 148:26-34 43 Brenko MH, Calabrese A (1969) Combined effects of salinity and temperature on larvae of mussel Mytilus edulis. Marine Biology 4:224-226 Britton JC, Morton B (1982) A dissection guide, field and laboratory manual for the introduced bivalve Corbicula fluminea. Malacological Review Supplement 3:1–82 Browne RA, Wanigasekera G (2000) Combined effects of salinity and temperature on survival and reproduction of five species of Artemia. Journal of Experimental Marine Biology and Ecology 244:29-44 Buisson L, Thuiller W, Lek S et al. (2008) Climate change hastens the turnover of stream fish assemblages. Global Change Biology 14:2232-2248 Burgmer T, Hillebrand H, Pfenninger M (2007) Effects of climate-driven temperature changes on the diversity of freshwater macroinvertebrates. Oecologia 151:93-103 Chessman BC (2009) Climatic changes and 13-year trends in stream macroinvertebrate assemblages in New South Wales, Australia. Global Change Biology 15:2791-2802 Chu C, Mandrak NE, Minns CK (2005) Potential impacts of climate change on the distributions of several common and rare freshwater fishes in Canada. Diversity and Distributions 11:299- 310 Connelly NA, O'Neill CR, Knuth BA et al. (2007) Economic impacts of zebra mussels on drinking water treatment and electric power generation facilities. Environmental Management 40:105-112 Costil K, Daguzan J (1995) Comparative life cycle and growth of 2 freshwater gastropod species, Planorbarius corneus (L.) and Planorbis planorbis (L.). Malacologia 37:53-68 Costil K, Dussart GBJ, Daguzan J (2001) Biodiversity of aquatic gastropods in the Mont St-Michel basin (France) in relation to salinity and drying of habitats. Biodiversity and Conservation 10:1-18 Daufresne M, Boet P (2007) Climate change impacts on structure and diversity of fish communities in rivers. Global Change Biology 13:2467-2478 Daufresne M, Roger MC, Capra H et al. (2004) Long-term changes within the invertebrate and fish communities of the Upper Rhone River: effects of climatic factors. Global Change Biology 10:124-140 De Vries P, Tamis JE, Murk AJ et al. (2008) Development and application of a species sensitivity distribution for temperature-induced mortality in the aquatic environment. Environmental Toxicology and Chemistry 27:2591-2598 De Zwart D (2005) Impact of toxicants on species composition of aquatic communities: concordance of predictions and field observations. PhD thesis, University of Amsterdam, The Netherlands Dieperink C (2000) Successes in the international cooperation in the Rhine catchment area. Physics and Chemistry of the Earth B 25:341-347 Dillon RT, Wethington AR, Rhett JM et al. (2002) Populations of the European freshwater pulmonate Physa acuta are not reproductively isolated from American Physa heterostropha or Physa integra. Invertebrate Biology 121:226-234 Directorate-General for Public Works and Water Management (2009) Waterbase. Online source. http://live.waterbase.nl (Accessed February, 16 2010) Dreier H, Tranquilli JA (1981) Reproduction, growth, distribution, and abundance of Corbicula in an Illinois cooling lake. Illinois Natural History Survey Bulletin 32:378-393 Chapter 2

Forcart L (1948) Ueber ein massenhaftes Auftreten von Physa acuta Drap. in den Thermen von Baden, sowie Untersuchungen über die Wärmeresistenz dieser Art. Basteria 12:24-28 Gabel F, Pusch M, Breyer P et al. (2011) Differential effect of wave stress on the physiology and behaviour of native versus non-native benthic invertebrates. Biological Invasions 13:1843- 1853 Gittenberger E, Janssen AW, Kuijper WJ et al. (1998) De Nederlandse zoetwatermollusken: 44 recente en fossiele weekdieren uit zoet en brak water. Nationaal Natuurhistorisch Museum Naturalis, KNNV, EIS Nederland, Leiden Gornitz V (1991) Global coastal hazards from future sea level rise. Global and Planetary Change 89:379-398 Grabowski M, Bacela K, Konopacka A et al. (2009) Salinity-related distribution of alien amphipods in rivers provides refugia for native species. Biological Invasions 11:2107-2117 Hadderingh RH, Van der Velde G, Schnabel PG (1987) The effect of heated effluent on the occurrence and the reproduction of the freshwater limpets Ancylus fluviatilis (Müller, 1774), Ferrissia wautieri (Mirolli, 1960) and Acroloxus lacustris (L., 1758) in two Dutch water bodies. Hydrobiological Bulletin 21:193-205 Heino J, Virkkala R, Toivonen H (2009) Climate change and freshwater biodiversity: detected patterns, future trends and adaptations in northern regions. Biological Reviews 84:39-54 Horrigan N, Dunlop JE, Kefford BJ et al. (2007) Acute toxicity largely reflects the salinity sensitivity of stream macroinvertebrates derived using field distributions. Marine and Freshwater Research 58:178-186 IKSR (2002) Das Makrozoobenthos des Rheins 2000. Internationale Kommission zum Schutz des Rheins, Koblenz IKSR (2011) Gewässergütedaten. Online source: http://maps.wasserblick.net:8080/iksr-zt/ (Accessed January 27, 2011) Jackson DA, Mandrak NE (2002) Changing fish biodiversity: predicting the loss of cyprinid biodiversity due to global climate change. In: McGinn NA (ed) American Fisheries Society Symposium 32. American Fisheries Society, Bethesda, MD, pp. 89-98 Kangas P, Skoog G (1978) Salinity tolerance of Theodoxus fluviatilis (Mollusca, Gastropoda) from freshwater and from different salinity regimes in Baltic Sea. Estuarine and Coastal Marine Science 6:409-416 Karatayev AY, Burlakova LE, Padilla DK (1998) Physical factors that limit the distribution and abundance of Dreissena polymorpha (Pall.). Journal of Shellfish Research 17:1219-1235 Karatayev AY, Burlakova LE, Padilla DK et al. (2009) Invaders are not a random selection of species. Biological Invasions 11:2009-2019 Karatayev AY, Padilla DK, Minchin D et al. (2007) Changes in global economies and trade: the potential spread of exotic freshwater bivalves. Biological Invasions 9:161-180 Kefford BJ, Fields EJ, Claya C et al. (2007) Salinity tolerance of riverine microinvertebrates from the southern Murray-Darling Basin. Marine and Freshwater Research 58:1019-1031 Kefford BJ, Marchant R, Schäfer RB et al. (2011) The definition of species richness used by species sensitivity distributions approximates observed effects of salinity on stream macroinvertebrates. Environmental Pollution 159:302–310 Kefford BJ, Nugegoda D, Metzeling L et al. (2006) Validating species sensitivity distributions using salinity tolerance of riverine macroinvertebrates in the southern Murray-Darling Basin (Victoria, Australia). Canadian Journal of Fisheries and Aquatic Sciences 63: 1865-1877 Kefford BJ, Papas PJ, Metzeling L et al. (2004) Do laboratory salinity tolerances of freshwater animals correspond with their field salinity? Environmental Pollution 129:355-362 Kefford BJ, Schäfer RB, Liess M et al. (2010) A similarity-index based method to estimate chemical concentration limits protective for ecological communities. Environmental Toxicology and Chemistry 29:2123–31 Sensitivity of native and non-native mollusc species

Kefford BJ, Schäfer RB, Metzeling L (2012) Risk assessment of salinity and turbidity in Victoria (Australia) to stream insects' community structure does not always protect functional traits. Science of the Total Environment 415: 61-68 Kinzelbach R (1995) Neozoans in European waters: exemplifying the worldwide process of invasion and species mixing. Experientia 51:526-538 Krkac N (1979) Temperature and reproductive cycle relations in Radix peregra O.F. Müller. Malacologia 18:227-232 45 Kuiper JGJ, Wolff WJ (1970) The Mollusca of the estuarine region of the rivers Rhine, Meuse and Scheldt in relation to the hydrography of the area. III. The genus Pisidium. Basteria 34:1- 42 Kwok KWH, Bjorgesaeter A, Leung KMY et al. (2008) Deriving site-specific sediment quality guidelines for Hong Kong marine environments using field-based species sensitivity distributions. Environmental Toxicology and Chemistry 27:226-234 Langford TE (1971) The biological assessment of thermal effects in some British rivers. Symposium on freshwater biological research and electrical power generation. Central Electricity Research Laboratories, Leatherhead, pp. 35 Lehtonen H (1996) Potential effects of global warming on northern European freshwater fish and fisheries. Fisheries Management and Ecology 3:59-71 Leung KMY, Bjorgesaeter A, Gray JS et al. (2005) Deriving sediment quality guidelines from field-based species sensitivity distributions. Environmental Science & Technology 39:5148- 5156 Leuven RSEW, Slooter N, Snijders J et al. (2007) The influence of global warming and thermal pollution on the occurrence of native and exotic fish species in the river Rhine. In: Van Os AG (ed) NCR-days 2007: a sustainable river system. The Netherlands Centre for River Studies, Delft, pp. 62-63 Leuven RSEW, Van der Velde G, Baijens I et al. (2009) The river Rhine: a global highway for dispersal of aquatic invasive species. Biological Invasions 11:1989-2008 Leuven RSEW, Hendriks AJ, Huijbregts MAJ et al. (2011) Differences in sensitivity of native and exotic fish species to changes in river temperature. Current Zoology 57:852-862 McMahon RF (1996) The physiological ecology of the zebra mussel, Dreissena polymorpha, in North America and Europe. American Zoologist 36:339-363 McMahon RF, Williams CJ (1986) Growth, life cycle, upper thermal limit and downstream colonization rates in a natural population of the freshwater bivalve mollusc, Corbicula fluminea (Mueller) receiving thermal effluents. American Malacological Bulletin Special Edition 2:231- 239 Mihuc TB, Battle JM, Mihuc JR et al. (1999) Zebra mussel (Dreissena polymorpha) seasonal colonization patterns in a sub-tropical floodplain river. Hydrobiologia 392:121-128 Morgan DE, Keser M, Swenarton JT et al. (2003) Population dynamics of the Asiatic clam, Corbicula fluminea (Müller) in the Lower Connecticut River: establishing a foothold in New England. Journal of Shellfish Research 22:193-203 Morton B (1986) Corbicula in Asia: an updated synthesis. American Malacological Bulletin Special Edition 2:113-124 Morton B, Tong KY (1985) The salinity tolerance of Corbicula fluminea (Bivalvia: Corbiculoidea) from Hong Kong. Malacological Review 18:91-95 Mouthon J (2007) Lithoglyphus naticoides (Pfeiffer) (Gastropoda : Prosobranchia): distribution in France, population dynamics and life cycle in the Saone river at Lyon (France). Annales De Limnologie 43:53-59 Mouthon J, Daufresne M (2006) Effects of the 2003 heatwave and climatic warming on mollusc communities of the Saone: a large lowland river and of its two main tributaries (France). Global Change Biology 12:441-449 Chapter 2

Mouthon J, Daufresne M (2008) Population dynamics and life cycle of Pisidium amnicum (Muller) (Bivalvia: Sphaeriidae) and Valvata piscinalis (Muller) (Gastropoda: Prosobranchia) in the Saone river, a nine-year study. Annales De Limnologie 44:241-251 Müller D, Patzner RA (1996) Growth and age structure of the swan mussel Anodonta cygnea (L.) at different depths in lake Mattsee (Salzburg, Austria). Hydrobiologia 341:65-70 Müller R, Anlauf A, Schleuter M (2005) Nachweise der Neozoe Menetus dilatatus (Gould, 1841) 46 in der Oberelbe, Mittelelbe, dem Mittellandkanal und dem Nehmitzsee (Sachsen, Sachsen- Anhalt, Brandenburg) (Gastropoda: Planorbidae). Malakologische Abhandlungen 23:77-85 Nehring S (2002) Biological invasions into German waters: an evaluation of the importance of different human-mediated vectors for nonindigenous macrozoobenthic species. In: Leppäkoski E, Gollasch S (eds) Invasive aquatic species of Europe: distribution, impacts and management. Kluwer Academic Publishers, Dordrecht, pp. 373-383 Orlova MI (2002) Dreissena (D.) polymorpha: evolutionary origin and biological peculiarities as prerequisites of invasion success. In: Leppäkoski E, Gollasch S (eds) Invasive aquatic species of Europe: distribution, impacts and management. Kluwer Academic Publishers, Dordrecht, pp. 127-134 Orlova MI, Therriault TW, Antonov PI et al. (2005) Invasion ecology of quagga mussels (Dreissena rostriformis bugensis): a review of evolutionary and phylogenetic impacts. Aquatic Ecology 39:401-418 Panov VE, Alexandrov B, Arbačiauskas K et al. (2009) Assessing the risks of aquatic species invasions via European inland waterways: the concepts and environmental indicators. Integrated Environmental Assessment and Management 5:110-126 Perez-Quintero JC (2007) Diversity, habitat use and conservation of freshwater molluscs in the lower Guadiana River basin (SW Iberian Peninsula). Aquatic Conservation: Marine and Freshwater Ecosystems 17:485-501 Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52:273-288 Piscart C, Moreteau JC, Beisel JN (2005) Biodiversity and structure of macroinvertebrate communities along a small permanent salinity gradient (Meurthe River, France). Hydrobiologia 551:227-236 Piscart C, Kefford BJ, Beisel JN (2011) Are salinity tolerances of non-native macroinvertebrates in France an indicator of potential for their translocation in a new area? Limnologica 41:107- 112 Posthuma L, Suter GW, Traas TP (2002) Species sensitivity distributions in ecotoxicology. Lewis Publishers, Boca Raton, Florida Rahel FJ, Olden JD (2008) Assessing the effects of climate change on aquatic invasive species. Conservation Biology 22:521-533 Ricken W, Steuber T, Freitag H et al. (2003) Recent and historical discharge of a large European river system: oxygen isotopic composition of river water and skeletal aragonite of Unionidae in the Rhine. Palaeogeography Palaeoclimatology Palaeoecology 193:73-86 Rossetti Y, Rossetti L, Cabanac M (1989) Annual oscillation of preferred temperature in the freshwater snail Lymnaea auricularia: effect of light and temperature. Animal Behaviour 37:897-907 Smit MGD, Holthaus KIE, Trannum HC et al. (2008) Species sensitivity distributions for suspended clays, sediment burial, and grain size change in the marine environment. Environmental Toxicology and Chemistry 27:1006-1012 Strayer DL (2010) Alien species in fresh waters: ecological effects, interactions with other stressors, and prospects for the future. Freshwater Biology 55:152-174 Struijs J, De Zwart D, Posthuma L et al. (2011) Field sensitivity distribution of macroinvertebrates for phosphorus in inland waters. Integrated Environmental Assessment and Management 7:280-286 Sensitivity of native and non-native mollusc species

Traas TP, van de Meent D, Posthuma L et al. (2002) The potentially affected fraction as a measure of ecological risk. In: Posthuma L, Suter II GW, Traas TP (eds) Species sensitivity distributions in ecotoxicology. Lewis Publishers, Boca Raton, Florida, pp. 315 -344 Uehlinger U, Wantzen KM, Leuven RSEW et al. (2009) The Rhine River Basin. In: Tockner K, Robinson CT, Uehlinger U (eds) Rivers of Europe. Elsevier/Academic Press, Oxford, pp. 199-245 Van de Meutter F, Trekels H, Green AJ et al. (2010) Is salinity tolerance the key to success for 47 the invasive water bug Trichocorixa verticalis? Hydrobiologia 649:231-238 Van der Velde G (1991) Population dynamics and population structure of Ferrissia wautieri (Mirolli, 1960) (Gastropoda, Ancylidae) in a pond near Nijmegen (The Netherlands). Hydrobiological Bulletin 24:141-144 Van der Velde G, Rajagopal S, bij de Vaate A (2010) The zebra mussel in Europe. Backhuys, Leiden/Margraf, Weikersheim Van Zelm R, Huijbregts MAJ, van Jaarsveld HA et al. (2007) Time horizon dependent characterization factors for acidification in life-cycle assessment based on forest plant species occurrence in Europe. Environmental Science & Technology 41:922-927 Vanderploeg HA, Nalepa TF, Jude DJ et al. (2002) Dispersal and emerging ecological impacts of Ponto-Caspian species in the Laurentian Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences 59:1209-1228 Verween A, Vincx M, Degraer S (2007) The effect of temperature and salinity on the survival of Mytilopsis leucophaeata larvae (Mollusca, Bivalvia): the search for environmental limits. Journal of Experimental Marine Biology and Ecology 348:111-120 Von Stackelberg K, Menzie CA (2002) A cautionary note on the use of species presence and absence data in deriving sediment criteria. Environmental Toxicology and Chemistry 21:466- 472 Walther AC, Lee T, Burch JB et al. (2006) Confirmation that the North American ancylidFerrissia fragilis (Tryon, 1863) is a cryptic invader of European and East Asian freshwater ecosystems. Journal of Molluscan Studies 72:318-321 Walton WC (1996) Occurrence of zebra mussel (Dreissena polymorpha) in the oligohaline Hudson River, New York. Estuaries 19:612-618 Webb BW (1996) Trends in stream and river temperature. Hydrological Processes 10:205-226 Weitere M, Vohmann A, Schulz N et al. (2009) Linking environmental warming to the fitness of the invasive clam Corbicula fluminea. Global Change Biology 15:2838-2851 Winterbourn MJ (1969) Water temperature as a factor limiting the distribution of Potamopyrgus antipodarum (Gastropoda-Prosobranchia) in the New Zealand thermal regions. New Zealand Journal of Marine Freshwater Research 3:453–458 Wright DA, Setzler-Hamilton EM, Magee JA et al. (1996) Effect of salinity and temperature on survival and development of young zebra (Dreissena polymorpha) and quagga (Dreissena bugensis) mussels. Estuaries 19:619-628 Wulfhorst J (1991) Effects of thermal and organic pollution on macroinvertebrate communities in the river Schwalm, a Northern Hesse hill stream (FRG). Verhandlungen Internationale Vereinigung fur Theoretische und Angewandte Limnologie 24:2149-2155

Chapter 3

Risk classifications of aquatic non-native species: application of contemporary European assessment protocols in different biogeographical settings

Laura Verbrugge, Gerard van der Velde, Jan Hendriks, Hugo Verreycken and Rob Leuven

Aquatic Invasions 7: 49-58, 2012 Chapter 3

Abstract Non-native species can cause negative impacts when they become invasive. This study entails a comparison of risk classifications for 25 aquatic non-native species using various European risk identification protocols. For 72 per cent of the species assessed, risk classifications were dissimilar between countries. The pair-wise comparison of Freshwater Fish Invasiveness Scoring Kit (FISK) scores of in total 28 fish species from the UK, Flanders (Belgium) and Belarus resulted in a higher correlation for scores of Flanders-Belarus than that of Flanders-UK and Belarus-UK. We conclude that different risk classifications may occur due to differences in (1) national assessment protocols, (2) species-environment matches in various biogeographical regions, and (3) data 50 availability and expert judgement. European standardisation of risk assessment protocols, performance of biogeographical region specific risk classifications and further research on key factors for invasiveness of aquatic ecosystems are recommended.

Introduction In the last decades, risk assessment has gained much interest as an instrument to support policy makers in their decisions regarding the need for managing non-native species (Andersen et al. 2004; Byers et al. 2002). Once non-native species are introduced and become invasive, they can cause considerable damage to natural ecosystems, biodiversity, human health, cattle, agriculture, and economy (Pimentel et al. 2005; Oreska and Aldridge 2011). Eradication and control of invasive species are very costly. For instance, recent estimates of environmental, social, and economic costs of 25 invasive non-native species in Europe vary between 12 and 20 billion euro per year for documented and extrapolated costs, respectively (Kettunen et al. 2008). These costs mainly result from damage and control measures. Circa ten per cent of non-native species entering a country or region outside their natural distribution area is able to become highly invasive in marine and freshwater systems (Ricciardi and Kipp 2008). High impacts of non-native fish invaders are limited to about 19 per cent of the total regions they invade (Ricciardi and Kipp 2008). Risk assessment is useful in identifying species that are likely to become invasive and cause significant negative impacts. In order to derive appropriate management options, several European countries (e.g. Austria, Belgium, Germany, Ireland, Switzerland, and United Kingdom) have recently developed national risk assessment protocols to identify low, moderate and high risk species. Risk assessment protocols for non-native species generally contain the main stages of invasion: (1) entry, (2) establishment, (3) spread, and (4) impacts. Because of the large number of non-native species that spread worldwide, there is a particular need for quick screening tools which can help to identify which new coming species have the potential to become invasive. Therefore, risk identification is one of the most important applications in risk assessment of non-native species. In Europe, risk standards and assessment protocols have been developed by the European and Mediterranean Plant Protection Organisation (EPPO). These standards can be used for developing (new) risk assessment protocols, such as in the IMPASSE project on the assessment of environmental impacts of alien species in aquaculture (Copp et al. 2008). However, legislative and regulatory requirements for European Union member states concerning risk assessment and management of (invasive) non-native species are Risk classifications of aquatic non-native species fragmented (Hulme et al. 2009). As a result, different risk classification approaches are being used in Europe and the vast majority of European risk assessment systems are not legally binding, so enforcement of their results in invasive species management is limited (Essl et al. 2011). Genovesi and Shine (2004) stress the importance of risk assessment in European policy on non-native species. They propose the use of a listing system to assign species to a black, white or grey list, depending on the severity of impact and data availability. Although the need for an early warning system for the European Union has recently been acknowledged (Genovesi et al. 2010), legal standards for risk assessment of non-native species are still lacking. Risk assessment of non-native species tend to be of a qualitative or semi-quantitative nature (Dahlstrom et al. 2011; Heikkilä 2011), mainly because data for quantitative 51 assessments are lacking (Kulhanek et al. 2011). However, in qualitative assessments of non-native species, lack of data is also a common problem (e.g. Gasso et al. 2010). As a result, current risk assessments are often based on incomplete data input and may rely heavily on expert opinions and assessors’ interpretations (Maguire 2004; Strubbe et al. 2011). In case of lack of data, available risk classifications from other countries or regions are often used to predict whether or not a non-native species may become invasive. A match of species traits to climate and habitat also helps in predicting invasiveness. According to Wittenberg and Cock (2001), the only factor consistently correlated with invasiveness in a region is invasiveness elsewhere. Although invasiveness elsewhere is usually included as a criterion in risk assessment, there are still remarkable differences between risk protocols worldwide and within Europe (Essl et al. 2011; Heikkilä 2011). These include differences in scope, weighting, scoring and classification methods, assessment criteria and uncertainty analysis. Moreover, there are many examples of non- native species which have become invasive in one region, but not in others (Ricciardi and Kipp 2008), and several species are known to expand to other habitat types once outside their native range (Wittenberg and Cock 2001). The sensitivity of ecosystems and economic impact may also differ between countries. For example, the risks and costs for control of the muskrat Ondatra zibethicus damaging river dikes in lowland regions are much higher than in uplands. Moreover, ecological impacts depend on region-specific habitat characteristics and conservation aims. So, whether risk classifications from one region are useful predictors for other regions is questionable as they only predict their potential impact. Previous studies have reviewed risk protocols available worldwide for assessment of aquatic biosecurity (Dahlstrom et al. 2011) and pests and pathogens (Heikkilä 2011). Other studies have evaluated the use of one assessment tool for different species groups and in different geographic regions (e.g. Weed Risk Assessment (WRA), Gordon and Gantz 2011; Gordon et al. 2008). Within Europe, environmental indicators for introduction and impacts of alien aquatic macroinvertebrate species have been developed and applied to various river systems (Panov et al. 2009). In addition, the accuracy of three risk assessment schemes has been tested in Central Europe for woody species (Krivánek and Pyšek 2006). However, the recently developed national risk assessment tools for non- native species and the multitude of risk classifications available in Europe have not yet been analysed. Altogether, comparative analyses of different risk assessment methods are largely missing in Europe (Essl et al. 2011). Chapter 3

The aim of this paper is to evaluate available risk classifications of non-native aquatic species performed with various risk assessment protocols of European countries and to elucidate factors that may contribute to variability in risk classifications between countries. In order to achieve this goal we performed two types of comparisons between countries, using risk classifications from (1) different protocols, and (2) the same protocol. The implications of our results for risk assessment of non-native species and application of risk classifications will be discussed.

Material and methods

52 Literature search A literature search was conducted to collect available protocols for risk assessment of non-native species in Europe (Verbrugge et al. 2010). In addition, an inventory was made of the outcomes in terms of risk classifications of species. Risk classifications and information about the protocols were obtained via the Internet and scientific publications.

Risk identification protocols This study focused on (trans)nationally developed, generic risk identification protocols from Europe. For the purpose of this study, we included protocols (1) which are currently being used for risk assessment in one (or more) countries and (2) for which risk classifications were available for review. A literature search yielded protocols from Belgium, Germany/Austria, Ireland, and Switzerland. Moreover, two protocols from the United Kingdom (UK) were included: one species-specific tool developed for freshwater fish and invertebrates, and the national GB risk assessment scheme (formerly referred to as the UK risk assessment scheme). Strictly speaking, the latter is beyond a risk identification tool, including a more elaborate risk analysis. We decided to include the GB scheme as well, because this is a good example of a generic protocol that can be used for all taxonomic groups. Moreover, it is the one of the first and the only elaborate scheme used in Europe in a national context. Overall, two different approaches for risk classification are applied in the protocols: (1) classification keys using formalized ‘yes’ or ‘no’ questions to assign high risk species to a Black List, and (2) semi-quantitative scoring methods, using the sum of the scores for various evaluation criteria as indicator for a high, medium or low risk using cut-off thresholds. The protocols are listed below with a short description of their characteristics. Classification keys The scope of the German-Austrian Black List Information System (GABLIS) is limited to ecological effects (Essl et al. 2011; Nehring et al. 2010). Based on five basic criteria species are assigned to the White, Grey or Black list, according to their potential risk. Species with scientifically sound evidence of a significant threat on native biodiversity are assigned to the Black List; species with a less evidence-based reliability of effects are assigned to the Grey List, and species which do not pose a threat to native biodiversity are assigned to the White List. The Black List and Grey List are further divided into sub lists based on the distribution of the species and the availability of eradication measures (Black warning, action and management list) and on the level of certainty of the assessment Risk classifications of aquatic non-native species

(Grey watch and operation list). Six complementary, biological and ecological criteria related to impact are used to decide whether the species should be placed on the Grey (watch) List or the White List. For the comparison of risk classifications with other risk assessment tools we distinguish only between the Black, Grey and White List. The Swiss classification key for neophytes is only applicable to plants and it assesses damage to biodiversity, human health, and economy using a total of ten questions (Weber et al. 2005). Species are then assigned to a Black or Watch List. The Black List includes plants that actually cause damage and the establishment and spread of these species should be prevented. The Watch List includes plants that have the potential to cause damage or are already causing damage in neighbouring countries. Semi-quantitative protocols 53 The Invasive Species Environmental Impact Assessment (ISEIA) from Belgium assesses environmental impact only and has no taxonomic boundaries (Branquart 2007). The assessment consists of four sections matching the last steps of the invasion process: the potential for spread (1), establishment (2), adverse impacts on native species (3) and ecosystems (4). ISEIA is based on 12 questions, the results of which reduce to these four numerical responses with which a species is classified. Species are assigned to a list based on their total score: Black list (high environmental risk), Watch list (moderate environmental risk), and Alert list for potential risk species which are not yet present. The GB risk assessment scheme is based on international risk standards provided by EPPO and can be used for all taxonomic groups. It roughly consists of two parts: (1) a preliminary assessment (14 ‘yes’/ ‘no’ questions) to determine whether a detailed risk assessment is needed, and (2) a detailed risk assessment scheme (51 questions) to assess the potential for entry and establishment, the capacity for spread, and the extent to which economic, environmental or social and human health impacts may occur (Baker et al. 2005, 2008). Answers can be given on a 5-point scale (ranging from very low to very high risk) and include an assessment of uncertainty (low, medium or high). Risks are then summarised in the four categories: entry, establishment, spread, and impact and aggregated to a final high, medium or low risk indication. The Freshwater Fish Invasiveness Scoring Kit (FISK) is an adaptation of the WRA from Pheloung et al. (1999). It is one of the pre-screening tools that can be used to inform the preliminary assessment section of the GB Scheme. It uses 49 questions in eight categories: (1) domestication, (2) climate and distribution, (3) invasive elsewhere, (4) undesirable traits, (5) feeding guild, (6) reproduction, (7) dispersal mechanisms, and (8) persistence attributes. Moreover, it takes into account the confidence (certainty/uncertainty) ranking of the assessors. Scores can range from −11 to 54 and they classify non-native species into low, medium, and high risk categories. Similar invasiveness screening tools have been developed for non-native freshwater invertebrates (Tricarico et al. 2010), marine fish and invertebrates, and amphibians (Cefas 2010). The Invasive Species Ireland Risk Assessment consists of a preliminary and detailed assessment (Invasive Species Ireland 2008). We only included the classifications resulting from the preliminary (i.e. risk identification) assessment in this study (already classifying species as high, medium or low risk). The complementary stage two assessment is only used to be able to rank and prioritize high risk species and therefore not useful for Chapter 3

our comparison. There are separate assessment formats for potential and established species. Invasion history, vectors and pathways, suitability of habitats, propagule pressure, establishment success and spread potential are addressed in a total of ten questions, and ecological, economic, and impacts on human and animal health assessed. Finally, the species are assigned to the high, medium or low risk category based on their summed scores.

Comparison of risk classifications The similarity of risk classifications for aquatic, non-native species was analysed by comparing risk assessment outcomes in two different ways. First of all, national (i.e. original) risk classifications were screened for similar species and this resulted in a table 54 with risk classifications using different protocols in different contexts (or countries). For species that have been subject of risk assessments in three or more countries, the similarity of the risk classifications of protocols applied in different countries was analysed. Owing to the different phrasing in risk classifications, we distinguished three levels of risk: (1) high risk / black list or high risk species not yet introduced (alert list), (2) medium risk / grey list / watch list, and (3) low risk / white list / not invasive. For each included species the classifications were marked to be either equal (classifications from all protocols fall into the same category) or dissimilar (classification from one or more protocols differs from the others). Some countries have adopted risk identification tools from other countries or use adapted schemes (e.g. ISEIA in the UK; see Parrot et al. 2009). However, in this comparison we limit ourselves to the use of protocols in their ‘native’ country. Secondly, mutual comparisons of available risk classifications for a group of non-native fish species occurring in three countries resulting from the same risk assessment protocol (i.e. FISK) were statistically correlated. This approach eliminates differences in risk classifications due to applications of different protocols. FISK originates from the UK and was applied in the UK (Copp et al. 2009), Flanders (Verreycken et al. 2009a, b) and Belarus (Mastitsky et al. 2010) to identify the (potential) risk of non-native fish species. For the UK, minimum, maximum, and mean scores from two assessors were available for each species and we used the mean scores in our study. The scores from Verreycken et al. (2009a, b) are averages of Verreycken et al. (unpublished data) and Vandenbergh (2007). Mastitsky et al. (2010) report single scores only. The scores were converted to risk classifications using thresholds recently calibrated by Copp et al. (2009). Comparisons between two countries were made using risk classifications for mutually assessed species. Correlations were calculated using species that were assessed by all three studies (n = 10).

Results

Comparison of national risk classifications National risk classifications were equal for seven out of 25 species (28%) (Table 3.1). For the remaining species, risk classification of at least one country differed from that of other countries. Comparatively spoken, risk classifications from different countries were more similar for plants than for animal species. Four out of eight plant species were classified equally, although more animal than plant species were assessed. For the Risk classifications of aquatic non-native species

Table 3.1 Comparison of available risk classifications for aquatic plants, fish and crayfish in various countries, where risk assessment protocols in force have been applied in their national context

FISK / BE1 DE2 AT2 UK5 IE6 CH7 FI-ISK Plants Azolla filiculoides Lamarck Watch list n.r. n.r. n.a. High risk High risk n.r. Crassula helmsii A. Berger Black list Grey list Grey list n.a. High risk High risk n.r. Elodea canadensis Michx. Black list Black list Black list n.a. n.r. Medium risk Black list Elodea nuttallii (Planch.) St. John Black list Black list Black list n.a. n.r. High risk Black list Hydrocotyle ranunculoides L. f. Black list Black list Black list n.a. High risk High risk n.r. Lagarosiphon major (Ridl.) Moss Black list n.r. n.r. n.a. High risk High risk n.r. Ludwigia grandiflora (M. Micheli) Black list Black list8 n.r. n.a. High risk High risk Black list Greuter & Burdet 55 Myriophyllum aquaticum (Vell.) Black list n.r. n.r. n.a. High risk Medium risk n.r. Verdc. Crayfish Astacus astacus (Linnaeus, n.r.# n.r.# n.r.# Low risk3 Low risk High risk n.a. 1758) Astacus leptodactylus n.r. n.r. n.r. Medium Low risk High risk n.a. (Eschscholtz, 1823) risk3 Orconectes limosus (Rafinesque, n.r. n.r. n.r. High risk3 Medium High risk n.a. 1817) risk Procambarus clarkii (Girard, n.r. n.r. n.r. High risk3 High risk High risk n.a. 1852) Fish Ameiurus nebulosus (Lesueur, Watch list Black list Grey list High risk4 n.r. Medium risk n.a. 1819) Carassius auratus (Linnaeus, n.r. Grey list Grey list n.r. n.r. Medium risk n.a. 1758) Ctenopharyngodon idella n.r. Black list Black list High risk4 n.r. Medium risk n.a. (Valenciennes in Cuvier and Valenciennes, 1844) Gambusia holbrooki Girard, 1859 n.r. Grey list Grey list High risk4 n.r. Medium risk n.a. Hypophthalmichthys molitrix n.r. Grey list Grey list High risk4 n.r. Medium risk n.a. (Valenciennes in Cuvier and Valenciennes, 1844) Lepomis gibbosus (Linnaeus, Watch list Grey list Grey list High risk4 n.r. n.r. n.a. 1758) Micropterus salmoides n.r. White list White list Medium n.r. Medium risk n.a. (Lacépède, 1802) risk4 * Neogobius melanostomus Alert list Black list Black list High risk4 n.r. Medium risk n.a. (Pallas, 1814) Oncorhynchus kisutch (Walbaum, n.r. White list White list n.r. n.r. Medium risk n.a. 1792) Pseudorasbora parva (Temminck Black list Grey list Grey list High risk4 High risk High risk n.a. and Schlegel, 1846) Perccottus glenii Dybowski, 1877 Alert list Black list Black list High risk4 n.r. n.r. n.a. Salvelinus fontinalis (Mitchill, n.r. Grey list Black list Medium n.r. Medium risk n.a. 1814) risk4 * Umbra pygmaea (DeKay, 1842) Not White list White list High risk4 n.r. n.r. n.a. invasive BE: Belgium, DE: Germany, AT: Austria, UK: United Kingdom, IE: Ireland, CH: Switzerland; n.a.: not applicable because protocol is limited to only one taxonomic group; n.r.: not reviewed; #: not reviewed because indigenous species in this country; *: previous assessment with FISK classified this species as high risk. Species with equal risk classifications are highlighted. 1Harmonia Database (2010); 2Nehring et al. (2010) for fish species and Essl et al. (unpublished data) for plant species (except Ludwigia grandiflora); 3Tricarico et al. (2010); 4Copp et al. (2009); 5Non-native Species Secretariat (2010); 6Invasive Species Ireland (2007); 7Swiss Commission for Wild Plant Conservation (2008); 8Nehring and Kolthoff (2011). Chapter 3

eastern mudminnow Umbra pygmaea, the noble crayfish Astacus astacus, and the Turkish crayfish Astacus leptodactylus risk classifications were most different, including both low and high risk classifications. For Ireland, all but one assessed fish species were classified as medium risk. The risk classifications for the remaining countries show more variability and generally give a higher risk indication.

Crossing borders FISK has recently been applied for 70 non-native fish species in the United Kingdom by Copp et al. (2009). Verreycken et al. (2009a, b) used this tool to assess the potential

A B 56 40 Pg 40 Pg Ppa Ppa Cg Ane Nm Ane Cg Nm 30 30 Cc Pse Om Pse 20 20 FISK BY FISK BY Nf Nf Mp Ci Ci Ng Hm Ng Hm Ip 10 10 Psp Ano Ar Cl 0 0 0 10 20 30 40 0 10 20 30 40 FISK FL FISK UK

C 40

Ane 30 Ppa Am Pg Cg Ppr Sl 20 Lg Nm

FISK FL Nk Nf Up Aa Ng Ci 10 Pse Hn Vv Hm 0 0 10 20 30 40 FISK UK Figure 3.1 Comparisons of risk assessments of exotic fish species with FISK performed in United Kingdom (UK), Belgium (FL, Flanders) and Belarus (BY). Scores can range from −11 to 54 and they classify non-native species into low, medium, and high risk categories (High risk: ≥ 19, 1 ≤ Medium risk < 19, Low risk: < 1). Data: Copp et al. (2009), Mastitsky et al. (2010), and Verreycken et al. (2009a, b) and Vandenbergh (2007). Species depicted with closed symbols were used in regression analysis (n = 10). The abbreviations of species names are as follows: Aa - Aspius aspius, Am - Ameiurus melas, Ane - Ameiurus nebulosus, Ano - Aristichthys nobilis, Ar - Acipenser ruthenus, Cc - Cyprinus carpio, Cg - Carassius gibelio, Ci - Ctenopharyngodon idella, Cl - Coregonus lavaretus maraenoides, Hm - Hypophthalmichthys molitrix, Hn - Hypophthalmichthys nobilis, Ip - Ictalurus punctatus, Lg - Lepomis gibbosus, Mp - Mylopharyngodon piceus, Nf - Neogobius fluviatilis, Ng - Neogobius gymnotrachelus, Nk - Neogobius kessleri, Nm - Neogobius melanostomus, Om - Oncorhynchus mykiss, Pg - Perccottus glenii, Ppa - Pseudorasbora parva, Ppr - Pimephales promelas, Pse - Proterorhinus semilunaris (syn. Proterorhinus marmoratus p.p.), Psp - Polyodon spathula, Sl - Sander lucioperca, Up - Umbra pygmaea, Vv - Vimba vimba. Risk classifications of aquatic non-native species invasiveness of the present and expected non-native fishes in Flanders (Belgium). FISK was also applied by Mastitsky et al. (2010) to assess the invasion potential of introduced fishes in Belarus. Only one out of 12 species assessed in Flanders and Belarus differed in risk classification, whereas 9 out of 19 and 8 out of 16 differed for pair-wise comparisons of Flanders-UK and Belarus-UK, respectively (Figure 3.1A-C). Furthermore, all mean UK scores were consistently higher than the Belgian ones, except that of Ameiurus nebulosus and Pimephales promelas (Figure 3.1C; Verreycken et al. 2009a, b). A higher correlation was found between the scores of non-native fish species (n = 10) assessed in both Flanders and Belarus (R2 = 0.79; P < 0.01) than that of species assessed in Flanders and UK (R2 = 0.41; P < 0.05) or in Belarus and UK (R2 = 0.41; P < 0.05).

57 Discussion When interpreting the outcome of this study, it is important to realize that our results are derived from a limited number of risk protocols. Firstly, development of risk protocols is an iterative process. Therefore, newly developed protocols are often based on existing risk assessment procedures. In some cases, similar questions or criteria are used, for example in the GB risk assessment scheme and the more recent Ireland Risk Assessment. Secondly, the GB risk assessment scheme is a more elaborate protocol than the others and it is not only a risk identification tool but a complete risk analysis. This protocol requires a detailed assessment of 51 questions and therefore needs more data input. In the preliminary assessment pre-screening tools such as FISK can be used. We included both FISK and the GB scheme in our comparison because our aim was to evaluate available risk classifications of non-native aquatic species performed with various risk assessment protocols of European countries to investigate risk classifications from both different countries and different protocols. Moreover, exclusion of the GB scheme would reduce the number of species for comparison (from 25 to 18) but would have produced the same results (72% dissimilar classifications). But when comparing the results of the UK with risk classifications from other countries this second remark has to be taken into account. Thirdly, FISK and its derivatives have been specifically designed to assess invasiveness attributes of freshwater fish, invertebrates etc. The Swiss classification key only focuses on plants, while the remaining protocols include more general criteria which can be applied to all species. Fourthly, because of the novelty of risk assessment of non- native species in Europe, protocols are constantly evaluated and revised. This means that comparisons as conducted in this study must be regularly updated. To our knowledge, the Ireland Risk Assessment and the GB scheme referred to in this study are currently being revised. Moreover, it has also triggered the development of alternative risk assessment procedures in Europe, such as ENSARS, a specific risk assessment for species involved in aquaculture (Copp et al. 2008). Risk classifications for aquatic species show dissimilarities for 18 of the 25 species included in this study when compared between countries (Table 3.1). Owing to the large number of variables included in the comparison we cannot attribute these dissimilarities to a single determining factor. Differences in classifications may be related to the different (number of) criteria in risk protocols as well as variability in national context (i.e. invasibility of ecosystems) and in use of literature by experts (i.e. expert judgement). While invasiveness of species elsewhere appeared to be consistently stronger correlated Chapter 3

to invasiveness (Wittenberg and Cock 2001; Figure 3.1), our study also shows that risk classifications from other (neighbouring) countries should always be applied with caution. For example, the fish speciesUmbra pygmaea is classified both as a non-invasive and a high risk invader within different parts of Europe (Table 3.1 and Figure 3.1). The comparison in this study was limited by the number of completed risk assessments for each country. Taxonomic differences are accounted for by including aquatic plant, vertebrate, and invertebrate species. However, the inclusion of non-aquatic species may alter the results. Differences for species groups have been exposed for the WRA, where risk indications for aquatic plants were more precautionary than for non-aquatic plants because the risk assessment included questions which are not relevant for aquatic plants. (Champion and Clayton 2000; Gordon and Gantz 2011). This would speak in favour of 58 species group-specific risk assessment components (such as FISK, FI-ISK etc.), while generic risk protocols, as applied by some European countries (e.g. Belgium and Ireland), may not have the same accuracy for all species groups. We found that risk assessments for plant species were more consistent than for animal species. Criteria in risk identification also relate to availability of habitat, climate matching, invasion stage, pathways and other region-specific matters. Essl et al. (2011) also recognized the value of regional risk assessment. In a comparison of assessments of freshwater fish in a German and Austrian context (using the same protocol: GABLIS), 10 per cent of the fish species were classified differently for the two countries. According to the authors, these dissimilarities largely reflected differences in current distributions in the two neighbouring countries (Essl et al. 2011). FISK classifications showed a higher correlation for scores of non-native fish species in Flanders and Belarus than for the pair-wise comparisons of Belarus-UK or Flanders- UK. This may be related to (1) the number and expertise of assessors, and (2) the variability in the bio-geographical and ecological setting of continental water systems versus inland waters on islands. Firstly, the comparison of Belarus and UK scores shows large differences for six species (i.e. Coregonus lavaretus maraenoides, Ameiurus nebulosus, Ctenopharyngodon idella, Neogobius gymnotrachelus, Mylopharyngodon piceus and Hypophthalmichthys molitrix). For these species, the Belarus scores were much lower, dismissing a high risk classification. According to Mastitsky et al. (2010), this may be explained by the use of dual independent assessments for each species in the UK (Copp et al. 2009), while in the Belarus study species were assessed by only one assessor. However, multiple experts may also affect variability, for example when experts judge reliability of data differently based on their experience or when they have different perceptions of risks (Maguire 2004). Qualitative risk assessments of non-native species inherently include normative aspects in the valuation of ecological effects. For example, Strubbe et al. (2011) recently showed that evidence of impacts of invasive birds are generally not based on scientific research but on anecdotal observations relating to small areas only. Secondly, when comparing our results with previous literature we have to make a distinction between applicability of the use of risk classifications from other regions and the use of a protocol (in this case FISK) in different regions. Gordon et al. (2008) evaluated the use of the WRA (of which FISK is an adaption) in six countries and found the number of correct rejections of invader species to be consistent across geographical applications. However, this only refers to the accuracy of the WRA in a certain region as the species assessments were compared to Risk classifications of aquatic non-native species a priori classifications for the same region. It does not compare risk classifications from different regions for the same species, as is the case in our study. When a semi-quantitative approach is used (i.e. scoring species for each criterion), the normative cut-off thresholds determine whether a species poses a low, medium or high risk (or is assigned to a certain list). This means that small changes in the assessment (e.g. slightly different judgements of available data) or cut-off thresholds can lead to different risk outcomes. Re-calibration of cut-off thresholds between regions is recommended, but this remains to be examined statistically and it would require justification. For instance, the calibration of FISK relied upon independent, international expertise for the a priori classifications of the species examined (Copp et al. 2009). Normative cut-off thresholds effects on risk classification are particularly relevant when risk assessment protocols have 59 a relative small number of criteria (i.e. ISEIA and Ireland Risk Assessment). Screening tools that are based on a larger number of scores (i.e. ask more questions) are more likely to produce lower variability (in the total score rankings) than those based on a few scores. However, more research on this topic is required as the number of species assessed by risk identification protocols is low and prohibits general conclusions on this matter. Parrot et al. (2009) recently applied the ISEIA protocol as a screening tool to identify potentially invasive non-native animal species in England. In their study, the UK scores from the ISEIA protocol were compared with the FISK scores from Copp et al. (2009) and the Freshwater Invertebrate Invasiveness Scoring Kit (FI-ISK) scores from Tricarico et al. (2010). Of the FISK scores for twelve fish species, eight are within the high risk category. Using the adapted ISEIA scheme, all but four species are classified as low risk. Parrot et al. (2009) explain the underestimation of risk using the ISEIA scheme by stating that the number of questions (i.e. the sample size of interrogation about the species) in the ISEIA protocol is insufficient. However, the FI-ISK and ISEIA assessments are in general agreement. Only one of five species was classified lower by ISEIA than FI-ISK (Parrot et al. 2009). In our study, three out of six species assessed are classified lower by ISEIA than FISK (i.e. Ameiurus nebulosus, Lepomis gibbosus and Umbra pygmaea). Another factor influencing risk assessment is data availability. The absence or scarcity of (literature) data on the invasion and effects of a species requires consultation of experts. One of the species classified as low risk in Belgium, Germany and Austria and as high risk in the UK is Umbra pygmaea. According to Verreycken et al. (2010), the paucity of (peer reviewed) publications on the introduced range and the ecological impact of Umbra pygmaea may explain the differences in outcome of the assessors (UK versus Belgium) and of different assessment tools, as the results are probably mainly based on expert judgement. Another important matter related to data availability is the inconsistency in terminology on the species’ status and classification and in information supply on species richness, intertaxon correlations and the significance of individual drivers of invasion for European databases on invasive species (i.e. DAISY and NOBANIS; Hulme et al. 2011). Both studies and our findings on dissimilarity in risk classifications across countries emphasize the need for transparency in risk assessments, related to data sources as well as limitations of data. The diversity in scoring and classification systems used in risk identification of non- native species in Europe hampers collaboration and the use of available risk assessments across borders. Considering the spread and impacts of invasive species across borders, European standardization of risk assessment protocols is highly recommended. Chapter 3

Conclusions Based on the limited comparisons made in this study, risk classifications of pre-screening tools used in Europe resulted in different outcomes for the majority of the tested species (72%). This may result from differences in scoring, classification, and weighting between the protocols. Application of the same protocol in different countries also resulted in differences in risk classifications of some fish species, indicating that variations in assessment outcomes may stem from other reasons. Important factors affecting the risk classifications are related to regional aspects, such as current distributions, habitat availability, and environmental matching. In addition, lack of data, expert judgement, and the number of assessors may play a role. 60 Our results suggest that risk classifications from one region cannot be applied to other regions without inserting a caveat. In spite of a significant correlation between pair-wise comparisons of risk classifications of non-native fish species in various countries, our results suggest that it would advisable for risk assessments to be performed within a national or even regional context. Research on key factors for invasiveness of species and invasibility of aquatic ecosystems in various biogeographical regions will be required to bridge knowledge gaps in risk assessments and to reduce uncertainties in risk classifications of non-native species. Current evaluations of risk assessment also indicate that the influence of uncertainties and lack of data on expert judgement should be explicitly acknowledged. Finally, European standardisation of risk assessment protocols will contribute to better comparable and transparent risk assessments of non-native species.

Acknowledgements This study was commissioned by the Invasive Alien Species Team, Plant Protection Service (Wageningen) of the Dutch Ministry of Economic Affairs, Food and Consumer Product Safety Authority (TRPCD/2009/3790 and TRPCD/2010/1540). We thank Prof. G. Copp (Centre for Environment, Fisheries and Aquaculture Science, UK), Dr. E. Branquart (Belgian Biodiversity Platform, Belgium), Dr. F. Essl (Federal Environment Agency, Austria), Dr. S. Vanderhoeven (University of Liege, Belgium), Dr. E. Weber (Swiss Federal Institute of Technology, Switzerland), J. Kelly (EnviroCentre Limited, Northern Ireland) and Dr. S. Nehring (Federal Agency for Nature Conservation, Germany) who kindly supported us with information, literature, opinions, and expertise on risk assessment of non-native species. We thank two anonymous reviewers and J.W. Lammers (Invasive Alien Species Team, Plant Protection Service, Wageningen) for critical comments on earlier drafts of this paper. Risk classifications of aquatic non-native species

References Andersen MC, Adams H, Hope B et al. (2004) Risk assessment for invasive species. Risk Analysis 24:787-793 Baker RHA, Black R, Copp GH et al. (2005) UK non-native organism risk assessment scheme user manual, Version 3.3. Online source: https://secure.fera.defra.gov.uk/nonnativespecies/ index.cfm?sectionid=51 (Accessed March 1, 2010) Baker RHA, Black R, Copp GH et al. (2007) The UK risk assessment scheme for all non-native species. In: Rabitsch W, Essl F, Klingenstein F (eds) Biological Invasions: from Ecology to Conservation. Neobiota 7:46-57 Belgian Forum on Invasive Species (2010) Harmonia database. Online source: ias.biodiversity. be/species/all (Accessed March 17, 2010) Branquart E (ed) (2007) Guidelines for environmental impact assessment and list classification 61 of non-native organisms in Belgium. Belgian Biodiversity Platform, Belgium, 4 pp Byers JE, Reichard S, Randall JM et al. (2002) Directing research to reduce the impacts of nonindigenous species. Conservation Biology 16:630-640 Cefas (2010) Decision support tools, identifying potentially invasive non-native marine and freshwater species: fish, invertebrates, amphibians. Online source: http://www.cefas.defra. gov.uk/our-science/ecosystems-and-biodiversity/non-native-species/decision-support- tools.aspx (Accessed April 9, 2010) Champion PD, Clayton JS (2000) Border control for potential aquatic weeds. Stage 1. Weed risk model. Science for conservation 141. Department of Conservation, Wellington, New Zealand. Online source: http://www.doc.govt.nz/upload/documents/science-and- technical/sfc141.pdf (Accessed March 17, 2010) Copp GH, Garthwaite R, Gozlan RE (2005) Risk identification and assessment of non-native freshwater fishes: a summary of concepts and perspectives on protocols for the UK. Journal of Applied Ichthyology 21:371-373 Copp GH, Areikin E, Benabdelmouna A et al. (2008) Review of risk assessment protocols associated with aquaculture, including the environmental, disease, genetic and economic issues of operations concerned with the introduction and translocation of species. Impasse Project No 44142, report to EC, 91 pp Copp GH, Vilizzi L, Mumford J et al. (2009) Calibration of FISK, an invasiveness screening tool for non-native freshwater fishes. Risk Analysis 29:457-467 Dahlstrom A, Hewitt CL, Campbell ML (2011) A review of international, regional and national biosecurity risk assessment frameworks. Marine Policy 35:208–217 Essl F, Nehring S, Klingenstein F et al. (2011) Review of risk assessment systems of IAS in Europe and introducing the German-Austrian black list information system (GABLIS). Journal for Nature Conservation 19:339–350 Gasso N, Basnou C, Vila M (2010) Predicting plant invaders in the Mediterranean through a weed risk assessment system. Biological Invasions 12:463–476 Genovesi P, Shine C (2004) European Strategy on Invasive Alien Species. Council of Europe (Nature and environment) No 137. Council of Europe Publishing, Strasbourg, 66 pp Genovesi P, Scalera R, Brunel S et al. (2010) Towards an early warning and information system for invasive alien species (IAS) threatening biodiversity in Europe. European Environment Agency, Copenhagen, 47 pp Gordon DR, Onderdonk DA, Fox AM et al. (2008) Consistent accuracy of the Australian weed risk assessment system across varied geographies. Diversity and Distributions 14:234-242 Gordon DR, Gantz CA (2011) Risk assessment for invasiveness differs for aquatic and terrestrial plant species. Biological Invasions 13:1829–1842 Heikkilä, J (2011) A review of risk prioritisation schemes of pathogens, pests and weeds: principles and practices. Agricultural and Food Science 20:15-28 Chapter 3

Hulme PE, Pyšek P, Nentwig W et al. (2009) Will threat of biological invasions unite the European Union? Science 324:40-41 Hulme PE, Weser C (2011) Mixed messages from multiple information sources on invasive species: a case of too much of a good thing? Diversity and Distributions 17:1152–1160 Invasive Species Ireland (2007) Invasive Species Database. Online source: http://www. invasivespeciesireland.com/downloads/risk_assessment.asp (Accessed March 17, 2010) Kettunen M, Genovesi P, Gollasch S et al. (2008) Technical support to EU strategy on invasive species (IS) - assessment of the impacts of IS in Europe and the EU (Final module report for the European Commission). Institute for European Environmental Policy (IEEP), Brussels, 44 pp Krivánek M, Pyšek P (2006) Predicting invasions by woody species in a temperate zone: a test of three risk assessment schemes in the Czech Republic (Central Europe). Diversity and 62 Distributions 12:319–327 Kulhanek SA, Ricciardi A, Leung B (2011) Is invasion history a useful tool for predicting the impacts of the world's worst aquatic invasive species? Ecological Applications 21:189-202 Maguire LA (2004) What can decision analysis do for invasive species management? Risk Analysis 24:859-868 Mastitsky SE, Karatayev AY, Burlakova LE et al. (2010) Non-native fishes of Belarus: diversity, distribution, and risk classification using the Fish Invasiveness Screening Kit (FISK). Aquatic Invasions 5:103-114 Nehring S, Essl F, Klingenstein F et al. (2010) Schwarze Liste invasiver Arten: Kriteriensystem und Schwarze Listen invasiver Fische für Deutschland und für Österreich. Bundesamt für Naturschutz, BfN-Skripten 285, Bonn-Bad Godesberg, 185 pp Nehring S, Kolthoff D (2011) The invasive water primrose Ludwigia grandiflora (Michaux) Greuter & Burdet (Spermatophyta: Onagraceae) in Germany: first record and ecological risk assessment. Aquatic Invasions 6:83–89 Non-native Species Secretariat (2010) Risk assessments. Online source: https://secure.fera. defra.gov.uk/nonnativespecies/index.cfm?pageid=216 (Accessed March 17, 2010) Oreska MPJ, Aldridge DC (2011) Estimating the financial costs of freshwater invasive species in Great Britain: a standardized approach to invasive species costing. Biological Invasions 13:305-319 Panov VE, Alexandrov B, Arbačiauskas K et al. (2009) Assessing the risks of aquatic species invasions via European inland waterways: from concepts to environmental indicators. Integrated Environmental Assessment and Management 5:110-126 Parrott D, Roy S, Baker R et al. (2009) Horizon scanning for new invasive non-native species in England. Research Report, Natural England, Peterborough, 111 pp Pheloung PC, Williams PA, Halloy SR (1999) A weed risk assessment model for use as a biosecurity tool evaluating plant introductions. Journal of Environmental Management 57:239-251 Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52:273- 288 Ricciardi A, Kipp R (2008) Predicting the number of ecologically harmful exotic species in an aquatic system. Diversity and Distributions 14:374-380 Strubbe D, Shwartz A, Chiron F (2011) Concerns regarding the scientific evidence informing impact risk assessment and management recommendations for invasive birds. Biological Conservation 144:2112–2118 Swiss Commission for Wild Plant Conservation (2008) Invasive alien plants Black and Watch List. Online source: http://www.cpsskew.ch/english/black_list.htm (Accessed March 17, 2010). Risk classifications of aquatic non-native species

Tricarico E, Vilizzi L, Gherardi F et al. (2010) Calibration of FI-ISK, an invasiveness screening tool for non-native freshwater invertebrates. Risk Analysis 30:285-292 Vandenbergh K (2007) Risicoanalyse voor uitheemse vissoorten in Vlaanderen. Licentiaatsverhandeling, Departement Biologie, Katholieke Universiteit Leuven, Leuven, 96 pp Verbrugge LNH, Leuven RSEW, Van der Velde G (2010) Evaluation of international risk assessment protocols for exotic species. Department of Environmental Science, Report 352. Radboud University Nijmegen, Nijmegen, 54 pp Verreycken H, van Thuyne G, Belpaire C (2009a) Non-indigenous freshwater fishes in Flanders: status, trends and risk assessment. In: Segers H, Branquart E (eds) Proceedings of a scientific meeting on Invasive Alien Species - Science Facing Aliens. Belgian Biodiversity Platform, Brussels, pp 71-75 Verreycken H, Van Thuyne G, Belpaire C (2009b) Non-indigenous freshwater fishes in Flanders: 63 status, trends and risk assessment. PowerPoint presentation, Science Facing Aliens, 2nd Belgian conference on biological invasions. Online source: http://ias.biodiversity.be/ meetings/200905_science_facing_aliens/session3_02.pdf (Accessed February 23, 2010) Verreycken H, Geeraerts C, Duvivier C et al. (2010) Present status of the North American Umbra pygmaea (DeKay, 1842) (eastern mudminnow) in Flanders (Belgium) and in Europe. Aquatic Invasions 5:83-96 Weber E, Köhler B, Gelpke G et al. (2005) Schlüssel zur Einteilung von Neophyten in der Schweiz in die Schwarze Liste oder die Watch-Liste. Botanica Helvetica 115:169-194 Wittenberg R, Cock MJW (eds) (2001) Invasive alien species: A toolkit of best prevention and management practices. CAB International, Wallingford, 228 pp

Chapter 4

Metaphors in invasion science: implications for risk assessment and management of biological invasions

Laura Verbrugge, Hub Zwart and Rob Leuven

Submitted Chapter 4

Abstract Metaphors for describing the introduction, impacts and management of non-native species are numerous and often quite outspoken (e.g. ‘invasional meltdown’, ‘elimination’, ‘explosive growth’). The adequacy of these metaphors is increasingly disputed. Policy makers have adopted metaphorical terms from scientific discourse that are now under dispute. We discuss the implications of the use of (strong) metaphors in risk assessment policies for invasive species. We argue that, rather than trying to erase all instances of value-laden language, the acknowledgement of value choices, commitments and narratives conveyed by these metaphors (or ‘responsible metaphor management’) is of major importance for implementation of effective policy.

Introduction Non-native species, also referred to as neobiota, alien, foreign, exotic, introduced or non- indigenous, are generally described as species introduced in areas outside their natural geographical range and whose presence is intentionally or unintentionally facilitated 66 by humans. Invasion biology is a relatively young scientific discipline which studies the causes, effects and management of non-native species introductions (Carlton 1999). One of the striking features of this field is the terminology that is used, in scientific as well as in public and policy domains. The use of overtly militaristic terms, such as ‘invasive species’, ‘fighting invaders’ and ‘explosive growth’ has been increasingly criticized (Larson 2005). First of all by philosophers and social scientists who have challenged the current vernacular by pointing out possible links between xenophobia and nativism, drawing parallels with immigration policy and accusing invasion biologists of taking a xenophobic stance towards non-native species (e.g. O’Brien, 2006). The linguistic problems in the field are further aggravated by the fact that multiple interpretations of key terms such as ‘non-native species’ and ‘invasive species’ are employed. The distinction between native and non-native species is criticized because of the lack of objective criteria in defining what is ‘native’ and ‘non-native’ (Warren 2007; Webber and Scott 2012; Woods and Moriarty 2001). Furthermore, different understandings of the term ‘invasive species’ can be identified within science, and between the scientific, policy and management domain (Boonman-Berson et al. 2014). In the past years, a vigorous and polarized debate on the use of (strong) metaphors and value-laden language in this particular field has emerged. It has come to the point where scientists are advocating for the ‘end of invasion biology’ based on its perceived xenophobic stance, the ambiguity of definitions and lack of foundation as such (Valéry et al. 2013). Ecologists and biologists take a pragmatic stance and stress the valuable outcomes of invasion biology in predicting and managing disrupting and costly biological invasions (Blondel et al. 2013; Richardson and Ricciardi 2013; Simberloff and Vitule 2014). The debate has reached a state where the search has begun for a middle-ground, for example by Shackelford et al. (2013) who outline a framework with different perspectives for different invasion stages; thus in prevention oriented measures the non-native status of the species plays an important role, while for an established species this is less relevant and impact should be the leading part. How diverging the existing perspectives may be, there is a common goal in place: to gain new insights needed to provide more valuable knowledge for the management of invasive species. Both sides advocate for a broader Metaphors in invasion science scope by engaging more disciplines in the so-called ‘invasion science’. However, in spite of the recent attempts for reconciliation, there is little evidence for movement on either side. This may be exemplary for these kind of debates, but it may also have unexpected or even unwanted effects, perhaps even moving them away from their (mutual) goal. The polysemic nature of terms used in invasion science is increasingly recognized. Misunderstandings arise from different understandings or interpretations of vocabularies. For example, recent literature has shown that the terms ‘non-native species’ and ‘invasive species’ have different meanings amongst ecologists and landscape scientists (Humair et al. 2013). The inclusion of more scientific disciplines will only add to the existing pool of interpretations. The ambiguity of terms extends into other domains as well, as does the importance that is attached to criteria that form these categorizations. A recent comparison of existing definitions of the terms ‘(non-)native species’ and ‘invasive species’ has identified origin as a major determinant in the science domain, while in policy and management other criteria are more important (i.e. impact and behaviour, respectively) (Boonman-Berson et al. 2014). In our paper, we follow the definition of the Convention of Biological Diversity (http://www.cbd.int/invasive/) that “invasive alien (or non-native) species are species whose introduction and/or spread outside their natural past or present 67 distribution threatens biological diversity ”, although we are aware of the fact that this is one possible definition among others. The existence of multiple interpretations shows that the struggle over nomenclature is by no means merely an academic or semantic issue, as it may create hurdles for implementing research findings into policy as well (Shaw et al. 2010; Young and Larson 2011). We believe there is a lack of knowledge on the implications of current vocabularies in the policy domain. Current debates concerning terminology used to describe biological invasions mainly address conceptual issues that are not directly useful for policymakers and managers. This especially holds for the field of risk assessment where science provides tools for policymakers to prioritize and effectively manage invasions. In this paper, we focus on the implications of the use of strong metaphors in describing biological invasions for effective risk management of invasive species. First, we analyse how terminological controversies in invasion biology are spilling over into the policy domain. Next, we assess the benefits and pitfalls of using strong metaphors in reporting scientific findings and apply the concept of responsible metaphor management on current risk assessment practices to identify potentially invasive species. Finally, we highlight opportunities to deal with the existence of multiple narratives on invasive species in the policy domain.

Metaphors and invasive species policy On global, European and national levels, governmental organizations and institutions have adopted tools and frameworks for effective management of invasive species. These tools usually include a formal procedure to assess and prioritize risks to the natural environment, human health or the economy. These risk outcomes then form the basis for management decisions, for example by allowing prioritization and ranking of species in terms of invasiveness or by linking invasion stage to feasible interventions. Reviews of international risk assessment frameworks have shown that they are inconsistent in scope and terminology (BIO Intelligence Service 2011; Dahlstrom et al. 2011; Essl et al. 2011). Thus, the quandaries of invasion biology have entered (if not ‘pervaded’) the Chapter 4

realm of environmental policy as well. It has been argued that the use of value-laden terms endangers the credibility of policy (Warren 2011) as well as the consistency of the decision making process (Hulme 2012). So far, unlike among scientists, discussions among policy experts on terminology and metaphors have been rare. As a rule, policy makers seem to focus on what is to be done rather than on terminology disputes among experts. They tend to focus on responsible management of invasive species, rather than on ‘responsible management of metaphors’. The problems involved are not so easy to solve. Whereas in the case of scientists awareness of the complexities and intricacies of the terminologies involved is part of their trade, policy experts tend to work with a relatively compact set of concepts that can be easily used to inform decision making. To the extent that the academic idiom becomes more sophisticated and nuanced, it may become increasingly difficult to translate research findings into clear-cut policy recommendations or guiding principles for nature management. Woods and Moriarty (2001) argue that policy should acknowledge the complexities of the issue by including relevant values such as naturalness, animal welfare, and economic and aesthetic values in framing its management aims. The question, then, 68 becomes: how can invasive species policy acknowledge that current discourse concerning non-native species implicitly or explicitly involves the use of value-laden concepts, and still develop consistent and effective species management (which often requires clear cut choices on the basis of unambiguous standards)? This issue is also addressed by Keulartz and Van der Weele (2008) who likewise point to the chronic debate between two diametrically opposed extremes, namely 'nativism' (taking sides with native species at the expense of newcomers) and 'cosmopolitism' (embracing and diversification). They argue that time has now come to address this academic stalemate in terms of concrete management practices, based on specific framings of the native versus non-native species issue in practical contexts.

Responsible metaphor management Two relevant perspectives on the use of metaphors in invasion biology were developed by Larsson (2011) and Hattingh (2001, 2010). A comprehensive survey of metaphor use in ecology, and in invasion biology in particular, has been published by Larson (2011). In his view, ecologists often have the tendency to overlook the value-dimension of the terms they use (p. ix). Rather than trying to rid ecology of metaphors and value-laden language, however, Larson argues that we should become more aware of this dimension, so that we can make conscious and responsible metaphoric choices (p. xi). Invasion biology is described as a rather extreme example. Although as a biologist Larson (2011) understands the concerns about invasive species, he is nonetheless critical about how these species have been ‘vilified’, also in scientific discourse (p. 162). His basic contention is that, in the case of invasive biology, the metaphors used by scientists have often contributed to a climate of fear and that “they have not shied away from advocating on behalf of native species and against invasive ones, despite recent concerns in the scientific community about whether such advocacy is appropriate ”(p. 162). The term ‘invasional meltdown’, employed by Simberloff (2006) in the journal Biological Invasions, is explicitly mentioned as an example in this context (p. 165). Again, the idea is not to cleanse the discourse from metaphors altogether. Rather, Larson (2011) argues that our metaphoric choices in sustainability and biodiversity discourse Metaphors in invasion science should be responsible and, indeed, ‘sustainable’, both from a scientific and from a societal and policy point of view. The question is, however, how to do this. Another constructive approach has been outlined by Hattingh (2001, 2010). He argues that conceptual oppositions frequently used in the debate on invasive species (such as native versus non-native, natural versus unnatural, and pristine versus disrupted) quickly lose their meaning in a post-modern society that is characterized by globalization and mobility. In a globalizing world, the integrity and authenticity of ecosystems are under pressure more or less by definition. Controversies arise simply because such dichotomies can no longer be upheld as an undisputed, consensual vocabulary. In policy debates, as well as in science, multiple narratives are interacting with one another. Therefore, according to Hattingh (2001), we cannot escape the narrative dimensions of these concepts. Neutrality is no option, but we can strengthen our awareness and sensitivity to the linguistic intricacies involved. He argues that, rather than opting for one particular (allegedly ‘neutral’) interpretation, we should be aware of the strengths and weaknesses (or relative value) of the various terminologies available, and be open to alternative narratives that might be more effective in articulating concerns about non-native species in the policy or public realm. In other words, we can no longer afford to base our decisions for 69 species management on particular vocabularies and leave the responsibility for developing and choosing this vocabulary to others. Both scientists and policy makers have to become consciously involved in how conceptual and linguistic disputes affect invasive species policy. The most basic question is whether we know in which narrative we operate when we debate the problem of invasive species in these terms, and whether we can live with its assumptions, implications and consequences. Building on these two approaches, we will try to make this idea of ‘responsible metaphor management’ more concrete by focusing on the implications of metaphorical language in invasive species policy and management practices. Can an ethic of responsibility, or more precisely: an ethic of ‘responsible metaphor management’, allow policy makers to address conceptual issues outlined above? We will use two important facets of invasive species policy: (1) the issue of developing different standards for native and non-native species, and (2) ecological impact assessment, as examples to flesh out more concretely what responsible metaphor management in policy would mean.

Applying an ‘ethic of responsibility’ to policy frameworks The native-non-native dichotomy is an important distinction in environmental policy and has led to the development of special screening procedures for non-native species. This first of all suggests that it is possible to make a clear distinction between both categories. Subsequently, to the extent that it is possible to make this distinction, the implications for policy are far from obvious. In Europe, decisions are usually based on the assumption that non-native species will not cause harm unless sufficient evidence indicates otherwise, while on other continents the opposite principle (the so-called ‘guilty until proven innocent’) is applied (Dahlstrom et al. 2011). This trend, where non-natives are regarded as (potentially) invasive prior to actual assessments, enhances the image of introduced species as dangerous invaders, while in fact only a small portion of the introduced species become invasive (Ricciardi and Kipp 2008; Williamson 1996). If we Chapter 4

apply the ethic of responsibility to invasive species policy, these assumptions must be reconsidered (see also Richardson and Ricciardi 2013). First of all, the number of introductions of non-native species has increased tremendously over the past decades (Leuven et al. 2009; Liebhold et al. 2012) and in a number cases immediate action seems warranted in order to forego severe ecological or socioeconomic impacts (Pejchar and Mooney 2009). To ´discriminate´ between native and non-native species is not without reason, as non-native species are more likely to become a pest (Paolucci et al. 2013), due to factors such as high dispersal ability and broad tolerance ranges, absence of natural enemies and the unpredictable nature of their population development and spread (Richardson et al. 2008). Therefore, to a certain extent, it seems reasonable to develop risk assessment tools and policies especially for them. Another aspect which acts as a selective bias to managing introduced species is our role as humans in the ‘unnatural’ spread and introduction of species. Because of the devastating impact that humans have (had) on nature we feel responsible for actions which facilitate the spread of non-native species and want to correct our mistakes and interference by means of prevention, eradication and control. The fact that non-native species are 70 sometimes addressed as biopollution serves as a good example (Elliott 2003; Panov et al. 2009). Both previous arguments, species’ harmfulness and human responsibility for its spread, are key arguments in shaping both ecologists and lay public perceptions of non- native species (Selge et al. 2011). On the basis of various regulatory frameworks, many countries have developed lists of (potential) invasive species in a national context. This is the core of invasive species policy, allowing differentiation between potential harmful species from harmless ones, as is also common in phytosanitary measures (FAO 2013). Assuming that the native – non-native dichotomy is a feasible one, and that non-native species indeed are potentially more invasive than native ones, it has often been argued that prevention is in principle the most (cost) effective strategy in invasive species management. There is increasing policy recognition that preventive measures are more adequate than selective targeted action (European Commission 2013), despite practical difficulties such as international agreements on trade (Hulme et al. 2008) and lack of control of individual actions that facilitate spread. However, current policies are mainly concerned with impact assessment of species that are already introduced, while only minor attention is paid to identifying pathways, vectors and species introductions (Leung et al. 2012). Already introduced species are the most urgent and the most visible and therefore receive more policy attention. In all those lines of argument, we must be aware of the fact that we frame a particular situation in terms of a particular narrative, one which allows us to focus attention on the management perspective. It is not a purely objective account, but a way of assuming responsibility for our actions.

Complexity of policy frameworks Although the concepts of nativeness and invasiveness provide a practical basis for policy frameworks, there are also limitations to this approach. In the case of invasive species, managers must decide on the basis of complex ecological, socioeconomic and ethical arguments. Indeed, one might refer to it as a ‘wicked problem’ (Rittel and Webber 1973) Metaphors in invasion science which involves many stakeholders holding different values and perceptions. We must consider that these perceptions of characteristics such as harm, invasiveness or nativeness are not a constant but dynamic and determined by various factors. Firstly, countries differ in (political) history, cultural identity and previous encounters with non-native species which may lead to variability in risk perception and eradication policies. For example, cultural differences as well as differences in the interpretation of available data may affect the consistency of risk classifications (Verreycken et al. 2010). Also, biological invasions may create paradoxal situations in which a species is regarded as invasive in one region and endangered or protected elsewhere in the world (Garzón-Machado et al. 2012). Moreover, it is important to realize that perception of non-native species not only differs on spatial scales but that this also fluctuates on a timescale. In other words, our narratives are sensitive to both space and time. We must keep in mind, for instance, that in the nineteenth century, introduced plants were at first perceived positively as migrating and adventurous cosmopolitans, then negatively as a weed, followed again by a positive attitude towards all common, ‘close to home’ species, regardless of their origin (Dresen 2011). Until the risks of non-native species became apparent, plant forms were regarded as ‘common heritage of mankind’ (Heywood 2005). Recent examples of changing 71 perceptions are the tamarisk (Stromberg et al. 2009), American jack-knife (Dekker and Beukema 2012), and zebra mussel (Leuven et al. 2009), for which also positive effects are now increasingly recognized. When taking a long term view, one may argue that the appreciation of non-native species is likely to increase because they are experienced as part of the local flora and fauna by future generations who grow up surrounded by them (Genovart et al. 2013). Finally, the various uses of the term ‘invasive species’ also reflect different narratives and this should not be overlooked. Labelling a species as invasive can have a much more profound meaning in the policy and public domain than in academic circles (e.g. Qvenild 2013). Overexposure to alarming messages can contribute to a negative image of non- native species in general (not only harmful ones). It may also adversely affect public support for species management as scientific views may conflict with public values. Especially for mammals, aesthetic or animal welfare values may feed public opposition, causing delay of eradication projects, and giving the population a chance to spread, as was the case with the grey squirrel in Italy (Genovesi and Bertolino 2001).

A closer look at ecological impact assessment Risk assessment is further complicated by uncertainties regarding potential impacts and the difficulty of quantifying ecological damage of invasive species. The assuring and definite tone of (inter)national risk classifications in fact sharply contrasts with the many uncertainties and complexities in the risk assessment processes (Liu et al. 2011; McGeoch et al. 2012) and with the variability in risk classifications between countries (Verbrugge et al. 2012). The effectiveness and usefulness of risk assessment procedures have been questioned by Hulme (2012) who states that many lack consistent hazard identification and that risk assessors should be trained to limit cognitive biases. Risk protocols in force are of qualitative or semi-quantitative nature (translating qualitative data into numbers) (Leung et al. 2012). Lack of data is a common problem and risk assessments often rely on expert judgements and anecdotal knowledge (Bayliss et al. 2012). Moreover, language can Chapter 4

be considered as a source of uncertainty itself (Carey and Burgman 2008). For example, in the assessment of predation impacts of bird species experts have to state whether there is a decline of several or many native species (Strubbe et al. 2011). The connotation of impact then becomes problematic because in assessments of harm, value judgements always play a role. A proposal to make subjectivity in value judgements explicit in ecological assessments has been made by Colautti and Richardson (2009). They argue that we should distinguish between motivational and methodological questions. An example of a methodological question is: “what affects the rate of population growth in introduced species and does it differ from natives? ” Such a question, they argue, should be answered as objectively as possible, based on the data at hand. Interpretations among experts may differ, and a certain level of subjectivity and flexibility, referred to as ‘methodological subjectivity’, may be involved. These questions should be distinguished from motivational ones, however, which are related to societal impact in terms of biodiversity, ecosystem management and human welfare, for example: “why should we be concerned about invasive species and what constitutes a negative impact? ” Besides interpretations of the available data, such questions involve value 72 judgements as well. This type of subjectivity they refer to as ‘motivational subjectivity’. It is much less constrained by established scientific methods than methodological subjectivity and therefore allows for much more flexibility among experts. Colautti and Richardson (2009) argue that, in order to clarify the confusion, both types of subjectivity, although legitimate in themselves, should be clearly distinguished. The main criteria in ecological impact assessments for non-native species tend to build to a large extent on the definitions and concepts that were developed in the academic domain. As a rule, the focus is on the adverse impacts of new-comers on native species communities (through predation, habitat modification, competition for food or habitat, parasitism, transition of disease vectors or hybridization) and on changes in ecosystem functioning. Although such criteria may function as effective guidelines in risk assessment, they do not always incorporate clear, ‘objective’ or noncontroversial definitions on what significant or undesirable damage to the environment is. Rather, they often reflect societal values relating to nature or biodiversity. For example, protecting native species can be substantiated by the desire to preserve biodiversity and to counter the homogenization of the world’s biota. This is a plausible narrative that will be supported by many, although it is a narrative which articulates a clear value commitment. On a smaller scale, keeping out non-native species may be needed to protect scarce and vulnerable ecosystems that society values because they are relatively natural and authentic (Hettinger 2001; Throop 2000). Again, this is a responsible way of framing the issue, as long as we are aware of the fact that a value judgement (in favour of relatively unique and vulnerable native ecosystems) is involved. We must be aware of the fact, however, that some drawbacks are involved in this. The fact that both main criteria in risk assessment (i.e. ‘harm to native species’ and in particular ‘changes in ecosystems functions’) at present are poorly specified raises concerns about their practicality. Notably, the question rises whether it is at all possible for any newly introduced species to be categorized as ‘not threatening’. Would it really be possible for a species to establish itself in a new area without changing its surroundings or competing with the species already present? The key question is: “how can we distinguish between changing Metaphors in invasion science and damaging ecosystems ” (Hulme 2012)? Where do we draw the line between acceptable and disruptive ecological impact without excluding all introduced species a priori? The present number of non-native species with ecological impacts is likely to be an underestimation (Pysek and Richardson 2010; Simberloff 2011) and with an increasing number of introductions and intensified research efforts, more impacts will be documented. This implies that current procedures will create longer lists of potential harmful species and will not provide feasible goals for invasive species management. To the extent that impact assessment not only involves methodological issues but also motivational ones, as Colautti and Richardson (2009) have argued, the responsibility for evaluating this ecological impact and translating it into policy objectives should not lie with the scientific community but should also be based on societal values (see also Carolan 2006).

Future perspectives In this paper, we discussed the implications of debates on value-laden terminology in invasive species research for decision making frameworks. Based on an ‘ethic of responsibility’ we argued that the acknowledgement of value choices is of major importance for the implementation of effective policy which is, in fact, determined by 73 numerous factors such as public support, feasibility of the aims, and the consistency and efficiency of proposed measures. Metaphorical language is not likely to be abandoned in invasive species policy as long as it is an integral part of science and regarded as necessary to create a sense of urgency (Young and Larson 2011). However, understanding and awareness of the different possible narratives and metaphorical alternatives that exist in the context of non-native species management is critical. This implies that we accept that there are multiple stories available and that we have to take responsibility for the choices and assumptions we make (in choosing one particular story rather than others) as well as for the consequences of our actions arising from those choices. Based on previous observations in risk assessment frameworks, the following recommendations have been drawn. One difficult challenge in ‘responsible metaphor management’ is that policies frame non- native species in a national context. Natural systems, such as rivers and mountains, tend to cross (artificial) institutional boundaries. Especially in Europe, the use of bioregions may provide more accurate predictions and provide a solid base for prevention and eradication programs. In addition, it may also prove useful in dealing with future prospects of global climate change. However, every country has its own (historic and cultural) values, norms and language. This exacerbates current difficulties in creating uniform policies or legislation and therefore may hamper international cooperation. Thus, the existence of multiple narratives on invasive species in a particular area, for example Europe, has to be acknowledged before a comprehensive ‘bioregion’ approach can be established. The challenge lies in recognizing and valuing these different perceptions of non-native species. Values and norms originate from society, from people. As a result, we argue that ‘narrative’ flexibility can only be improved by incorporating stakeholder participation in the decision making process. In that way different perceptions and narratives can be taken into account while still providing a useful risk outcome to support management (Falk-Peterson forthcoming; Kapler et al. 2012). The incorporation of multiple narratives and perceptions may obviously also give rise to conflicts and differences of opinion Chapter 4

in defining assessment criteria and scaling issues (Binimelis et al. 2007). However, this should not be used as an argument against public participation because it adds a new dimension that science alone simply cannot offer. Early involvement of stakeholders is important to avoid or at least reduce conflicts. In addition, we would argue, that merely ecological impact assessment will not suffice and that incorporation in a broader decision making framework is recommended. This inevitably requires invasive species policy to take a broader perspective, for instance by recognizing the possibility that impacts of non-native species also include positive effects. The qualitative nature of risk assessment allows for processes of framing in accordance with normative value judgements. This often meets the need of policy makers for concise interpretations resulting in clear recommendations for action, but the scientific validity of moving from fact to interpretation may nonetheless be questioned. We propose to tackle this issue from two sides. On the one hand we encourage ongoing efforts to develop more quantitative and objective risk assessments. However, these outputs (in the form of numbers or maps) have to interpreted and presented nonetheless. In the end value judgements will inevitably play a role. Therefore, we argue that academic researchers and 74 risk assessors should become more aware that their interpretation of research results (their ‘motivational subjectivity’) will have a significant influence on risk assessment outcomes and eventually also on policy objectives. Values and uncertainties in science should be made explicit, as well as the implications for the results, notably for policy makers to make informed decisions. Many environmental and ecological issues are complex (‘wicked’) problems beset with uncertainties, so that factual (objective) knowledge alone will not lead to clear cut results and value judgement will always play a role. Efforts to translate expert information into policy will always involve interpretation on the basis of the narratives we use. Whether these narratives, and the metaphors supporting them, are feasible, allowing us to assume responsibility in the face of uncertainty and under determination of purely factual accounts is to be considered carefully. We have shown that responsible metaphor management is especially important in impact assessments. Currently, risk protocols often lack a clear reference to what ecological damage is. Tools to make assessment criteria operational can be obtained from existing legal frameworks for nature conservation. Nature conservation aims are part of nature protection laws or plans and violation of these laws (e.g. European Union Habitats Directive, Birds Directive and Water Framework Directive) can serve as base lines for evaluating harmful effects of non-native species (De Nooij et al. 2008). In order to provide sufficient guiding, these criteria should at least include a reference to reversible and irreversible damage and spatial scale of the effects. Thus, frameworks can be improved by providing sufficient guidance to avoid misinterpretations as much as possible, however, these cannot be ruled out entirely. Therefore, we stress the importance of reducing bias by increasing the transparency of the risk assessment process and by setting requirements for the assessment procedure (e.g. number and expertise of assessors and quality assurance of data reviews). Finally, policy makers are increasingly confronted with new types of ecosystems for which traditional restoration and conservation norms are difficult to uphold. If a non- native species has successfully established in a certain region, this inevitably conflicts with flora or fauna compositions based on historical references. Climate change, shifts Metaphors in invasion science in land use and other consequences of human activities further complicate our relation with the environment. Better insights into visions of nature (Van den Born et al. 2001) will also help to evaluate non-native species policy in terms of values attributed to nature by institutions, professionals and the public. Altogether, this will aid the development of more sustainable and realistic goals for management of non-native species.

Acknowledgements We thank J.W. Lammers (Invasive Alien Species Team, Netherlands Food and Consumer Product Safety Authority, Wageningen) and Dr. Riyan van den Born (Department of Philosophy and Science Studies, Institute for Science, Innovation and Society, Radboud University Nijmegen) for their comments on an earlier draft of this paper.

References Bayliss HR, Wilcox A, Stewart GB et al. (2012) Does research information meet the needs of stakeholders? Exploring evidence selection in the global management of invasive species. Evidence & Policy: A Journal of Research, Debate and Practice 8:37-56. 75 Binimelis R, Monterroso I, Rodriguez-Labajos B (2007) A social analysis of the bioinvasions of Dreissena polymorpha in Spain and Hydrilla verticillata in Guatemala. Environmental Management 40:555-566. BIO Intelligence Service. (2011). A comparative assessment of existing policies on invasive species in the EU Member States and in selected OECD countries. Commissioned by EU Commission DG ENV, Paris Blondel J, Hoffmann B, Courchamp F (2013) The end of invasion biology: intellectual debate does not equate to nonsensical science. Biological Invasions16:977-979 Boonman-Berson S, Turnhout E, Van Tatenhove J (2014) Invasive species: the categorization of wildlife in science, policy, and wildlife management. Land Use Policy 38:204-212 Carey JM, Burgman MA (2008) Linguistic uncertainty in qualitative risk analysis and how to minimize it. Annals of the New York Academy of Sciences 1128:13-17 Carlton JT (1999) A journal of biological invasions. Biological Invasions 1:1-1 Carolan MS (2006) The values and vulnerabilities of metaphors within the environmental sciences. Society & Natural Resources 19:921-930 Colautti RI, Richardson DM (2009) Subjectivity and flexibility in invasion terminology: too much of a good thing? Biological Invasions 11:1225-1229 Dahlstrom A, Hewitt CL, Campbell ML (2011) A review of international, regional and national biosecurity risk assessment frameworks. Marine Policy 35:208-217 De Nooij RJW, Leuven RSEW, Lenders HJR et al. (2008) Relating the ecological and legal frameworks for nature conservation in Europe. Journal of International Wildlife Law & Policy 11:63-95 Dekker R, Beukema JJ (2012) Long-term dynamics and productivity of a successful invader: the first three decades of the bivalve Ensis directus in the western Wadden Sea. Journal of Sea Research 71:31-40 Dresen, L (2011) De waardering voor kosmopolitisme van planten en dieren in de Nederlandse natuurjournalistiek, 1850-1910. De Negentiende Eeuw 35:34-58 (in Dutch) Elliott M (2003) Biological pollutants and biological pollution: an increasing cause for concern. Marine Pollution Bulletin 46:275-280 Chapter 4

Essl F, Nehring S, Klingenstein F et al. (2011) Review of risk assessment systems of IAS in Europe and introducing the German–Austrian Black List Information System (GABLIS). Journal for Nature Conservation 19:339-350 European Commission (2013) Proposal for a regulation of the European parliament and of the council on the prevention and management of the introduction and spread of invasive alien species. COM/2013/0620, Brussels, Belgium, pp. 36 Falk-Petersen, J (forthcoming) Alien invasive species management: stakeholder perceptions of the Barents Sea King Crab. Environmental Values. FAO (2013) Pest risk analysis for quarantine pests. International Standards for Phytosanitary Measures Publication No. 11. Food and Agriculture Organization of the United Nations (FAO), Rome Garzón-Machado V, del-Arco-Aguilar MJ, Pérez-de-Paz PL (2012) Threat or threatened species? A paradox in conservation biology. Journal for Nature Conservation 20:228-230 Genovart M, Tavecchia G, Enseñat JJ et al. (2013) Holding up a mirror to the society: children recognize exotic species much more than local ones. Biological Conservation 159:484-489 Genovesi P, Bertolino S (2001) Human dimension aspects in invasive alien species issues: the case of the failure of the grey squirrel eradication project in Italy. In: McNeely JA (ed) The great reshuffling: human dimensions of invasive alien species. IUCN, Gland, Switzerland 76 and Cambridge, UK, pp. 113-120 Hattingh J (2001) Human dimensions of invasive alien species in philosophical perspective: towards an ethic of conceptual responsibility. In: McNeely JA (ed) The great reshuffling: human dimensions of invasive alien species. IUCN, Gland, Switzerland and Cambridge, UK, pp. 183-194 Hattingh J (2010) Conceptual clarity, scientific rigour and ‘The Stories We Are’: engaging with two challenges to the objectivity of invasion biology. In: Richardson DM (ed) Fifty years of invasion ecology. Wiley-Blackwell, Oxford, UK, pp. 359-375 Hettinger N (2001) Defining and evaluating exotic species: issues for Yellowstone Park policy. Western North American Naturalist 61:257-260 Heywood, V (2005) Changing attitudes to plant introductions and invasives. In: Proceedings of the EPPO conference ‘Invasive plant in the Mediterranean type of regions of the world’ pp.119-128 Hulme PE (2012) Weed risk assessment: a way forward or a waste of time? Journal of Applied Ecology 49:10-19 Hulme PE, Bacher S, Kenis M et al. (2008) Grasping at the routes of biological invasions: a framework for integrating pathways into policy. Journal of Applied Ecology 45:403-414 Humair F, Edwards PJ, Siegrist M et al. (2014) Understanding misunderstandings in invasion science: why experts don’t agree on common concepts and risk assessments. NeoBiota 20:1- 30 Kapler EJ, Thompson JR, Widrlechner MP (2012) Assessing stakeholder perspectives on invasive plants to inform risk analysis. Invasive Plant Science and Management 5:194-208 Keulartz J, Van der Weele C (2008) Framing and reframing in invasion biology. Configurations 16:93-115 Larson BMH (2005) The war of the roses: demilitarizing invasion biology. Frontiers in Ecology and the Environment 3:495-500 Larson, BMH (2011) Metaphors for environmental sustainability: redefining our relationship with nature. Yale University Press, New Haven Leung B, Roura-Pascual N, Bacher S et al. (2012) TEASIng apart alien species risk assessments: a framework for best practices. Ecology Letters 15:1475-1493 Leuven RSEW, Velde G, Baijens I et al. (2009) The river Rhine: a global highway for dispersal of aquatic invasive species. Biological Invasions 11:1989-2008 Metaphors in invasion science

Liebhold AM, Brockerhoff EG, Garrett LJ et al. (2012) Live plant imports: the major pathway for forest insect and pathogen invasions of the US. Frontiers in Ecology and the Environment 10:135-143 Liu S, Sheppard A, Kriticos D et al. (2011) Incorporating uncertainty and social values in managing invasive alien species: a deliberative multi-criteria evaluation approach. Biological Invasions 13:2323-2337 McGeoch MA, Spear D, Kleynhans EJ et al. (2012) Uncertainty in invasive alien species listing. Ecological Applications 22:959-971 O’Brien W (2006) Exotic invasions, nativism, and ecological restoration: on the persistence of a contentious debate. Ethics, Place & Environment 9:63-77 Panov VE, Alexandrov B, Arbaciauskas K et al. (2009) Assessing the risks of aquatic species invasions via European inland waterways: from concepts to environmental indicators. Integrated Environmental Assessment and Management 5:110-126 Paolucci EM, MacIsaac HJ, Ricciardi A (2013) Origin matters: alien consumers inflict greater damage on prey populations than do native consumers. Diversity and Distributions 19:988- 995 Pejchar L, Mooney HA (2009) Invasive species, ecosystem services and human well-being. Trends in Ecology & Evolution 24:497-504 Pysek P, Richardson DM (2010) Invasive species, environmental change and management, and 77 health. In: Gadgil ALDM (ed) Annual Review of Environment and Resources 35:25-55 Qvenild M (2013) Wanted and unwanted nature: landscape development at Fornebu, Norway. Journal of Environmental Policy & Planning 16:183-200 Ricciardi A, Kipp R (2008) Predicting the number of ecologically harmful exotic species in an aquatic system. Diversity and Distributions 14:374-380 Richardson DM, Pysek P, Simberloff D et al. (2008) Biological invasions - the widening debate: a response to Charles Warren. Progress in Human Geography 32:295-298 Richardson DM, Ricciardi A (2013) Misleading criticisms of invasion science: a field guide. Diversity and Distributions 19:1461-1467 Rittel HWJ, Webber MM (1973) Dilemmas in a general theory of planning. Policy Sciences 4:155-169 Selge S, Fischer A, Van der Wal R (2011) Public and professional views on invasive non-native species: a qualitative social scientific investigation. Biological Conservation 144:3089-3097 Shackelford N, Hobbs RJ, Heller NE et al. (2013) Finding a middle-ground: the native/non- native debate. Biological Conservation 158:55-62 Shaw J, Wilson J, Richardson D (2010) Initiating dialogue between scientists and managers of biological invasions. Biological Invasions 12:4077-4083 Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecology Letters 9:912-919 Simberloff D (2011) How common are invasion-induced ecosystem impacts? Biological Invasions 13:1255-1268 Simberloff D, Vitule JRS (2014) A call for an end to calls for the end of invasion biology. Oikos 123:408-413 Stromberg JC, Chew MK, Nagler PL et al. (2009) Changing perceptions of change: the role of scientists in Tamarix and river management. Restoration Ecology 17:177-186 Strubbe D, Chiron F, Shwartz A (2011) Reply to Kumschick and Nentwig (2010, 2011): promoting a robust cost-benefit approach for conducting impact risk assessments of invasive species. Biological Conservation 144:2748 Throop W (2000) Eradicating the aliens: restoration and exotic species. In: Throop W (ed) Environmental restoration: ethics, theory and practice. Humanity Books, New York, pp. 179-191 Chapter 4

Valéry L, Fritz H, Lefeuvre J-C (2013) Another call for the end of invasion biology. Oikos 122:1143-1146 Van den Born RJG, Lenders HJR, De Groot WT et al. (2001) The new biophilia: an exploration of visions of nature in Western countries. Environmental Conservation 28:65-75 Verbrugge LNH, Van der Velde G, Hendriks AJ et al. (2012) Risk classifications of aquatic non- native species: Application of contemporary European assessment protocols in different biogeographical settings. Aquatic Invasions 7:49–58 Verreycken H, Geeraerts C, Duvivier C et al. (2010) Present status of the North American Umbra pygmaea (DeKay, 1842) (eastern mudminnow) in Flanders (Belgium) and in Europe. Aquatic Invasions 5:83-96 Warren CR (2007) Perspectives on the 'alien' versus 'native' species debate: a critique of concepts, language and practice. Progress in Human Geography 31:427-446 Warren CR (2011) Nativeness and nationhood: what species belong in post-devolution Scotland? In: Rotherham ID and Lambert RA (eds) Invasive and introduced plants and animals: human perceptions, attitudes and approaches to management. Earthscan, London, UK, pp. 67-79 Webber BL, Scott JK (2012) Rapid global change: implications for defining natives and aliens. Global Ecology and Biogeography 21:305-311 Williamson MH (1996) Biological Invasions. Chapman and Hall, London, UK 78 Woods M, Moriarty PV (2001) Strangers in a strange land: the problem of exotic species. Environmental Values 10:163-191 Young AM, Larson BMH (2011) Clarifying debates in invasion biology: a survey of invasion biologists. Environmental Research 111:893-8

Chapter 5

Exploring public perception of non-native species from a visions of nature perspective

Laura Verbrugge, Riyan van den Born and Rob Lenders

Environmental Management 52:1562-1573, 2013 Chapter 5

Abstract Not much is known about lay public perceptions of non-native species and their underlying values. Public awareness and engagement, however, are important aspects in invasive species management. In this study, we examined the relations between the lay public’s visions of nature, their knowledge about non-native species, and their perceptions of non-native species and invasive species management with a survey administered in the Netherlands. Within this framework, we identified three measures for perception of non- native species: perceived risk, control and engagement. In general, respondents scored moderate values for perceived risk and personal engagement. However, in case of potential ecological or human health risks, control measures were supported. Respondents’ images of the human-nature relationship proved to be relevant in engagement in problems caused by invasive species and in recognizing the need for control, while images of nature appeared to be most important in perceiving risks to the environment. We also found that eradication of non-native species was predominantly opposed for species with a high cuddliness factor such as mammals and bird species. We conclude that lay public perceptions of non-native species have to be put in a wider context of visions of nature, and we discuss the implications for public support for invasive species management.

Introduction

General introduction 82 Public support is an increasingly relevant issue in current nature and wildlife management (Vaske et al. 2011; Sijtsma et al. 2012). In this respect, it is vital to have a good understanding of the public’s view and underlying values of nature and nature management (Teel and Manfredo 2010). Public attitudes may also have large implications for invasive species management in terms of prevention, early warning, and eradication success (Burt et al. 2007; Cohen et al. 2007; Crall et al. 2010; Genovesi and Bertolino 2001). Biological invasions are recognised as a potentially major threat to biodiversity, and may have considerable economic and social effects (European Environment Agency 2012; Pejchar and Mooney 2009; Pimentel et al. 2005). Consequently, they have become an important issue in environmental policy and management (Essl et al. 2011; Verbrugge et al. 2012). Although attention for the role of stakeholders groups in relation to management and impacts has increased in the past decade (Andreu et al. 2009; Bardsley and Edwards-Jones 2006; Binimelis et al. 2007; Vanderhoeven et al. 2011), only limited knowledge about lay public perception of non-native species exists. A recent survey among European citizens showed that biodiversity management that is strongly focused on nativeness might not always tally with public interests (Fischer et al. 2011). This may indicate that policy foci should entail a broader basis than merely the distinction between native and non-native species. However, a recent study has shown that the origin of a species does matter when predicting ecological impacts (Paolucci et al. 2013). Altogether, the human-mediated introduction of non-native species, their rate of spread, and their impacts may evoke feelings that these species do not naturally belong in an area (Ridder 2007). Exploring public perception of non-native species

Sharp et al. (2011) have shown that environmental attitudes can be used as indicators of support for non-native species management. For example, the belief that all living things have a right to coexist appears to result in a preference for hands-off management, while people who feel that some degree of human intervention in nature is necessary were more supportive of on-site management and eradication of non-native species. Recently, a study on an invasive plant species, tree mallow (Lavatera arborea), indicated that safeguarding a state of balance and naturalness (defined as untouched by humans) were significant predictors for preferred management options for this species (Fischer and Van der Wal 2007). In addition, Bremner and Park (2007) found that respondents with prior knowledge of control and eradication programmes and members of conservation organisations showed higher levels of support for eradication of invasive species. They also found that species appeal influenced levels of support (Bremner and Park 2007). However, further insights in the relationship between lay public perception of non-native species and nature are currently lacking. A better understanding of the underlying values in non-native species perception can help elucidate current difficulties in invasive species management. This type of information is relevant for making decisions on the feasibility of management actions and for informing the public about non-native species control and involvement in prevention oriented measures (Andreu et al. 2009). Our study entails an exploration of perceptions of nature as predictors for non-native species perception and support of invasive species management.

Theory on visions of nature Lay people’s perceptions of nature are captured in the visions of nature concept (Van den 83 Born et al. 2001). This research tradition has its roots in western countries and comprises three different components: (1) images of nature (what is nature?) including images of the type of balance in nature, (2) values of nature (why is nature important?), and (3) images of the human-nature relationship (how should people relate to nature?). The first component, images of nature, addresses people’s understanding of what nature is. Aspects shaping lay people’s images of nature unfolded in previous studies are the absence or presence of humans, autonomy of natural processes, and degree of wildness (Buijs 2009a; De Groot 2012; De Groot and De Groot 2009; Van den Born 2008). To our knowledge, no previous studies have investigated possible relationships between the lay public’s images of nature and their perceptions of non-native species and invasive species management. Vanderhoeven et al. (2011) did show that horticultural professionals and nature reserve managers with different perceptions (or images) of nature had different levels of concern for non-native species. Images of nature also comprise images of balance in nature; i.e. beliefs regarding how fragile or how robust nature is. Thompson et al. (1990) described four myths of nature (i.e. unstable, with thresholds, stable, and indifferent) based on cultural theory of risk. In this theory, followers of each myth have an accompanying view regarding the management of nature (Thompson et al. 1990). Recent applications to environmental risk perception have proved it to be a useful concept in understanding environmental beliefs and nature perception (Grendstad and Selle 2000; Steg and Sievers 2000; Storch 2011). A study that linked myths of nature and perception of risks related to water management showed that respondents who thought of nature as stable were, in general, less concerned about non-native species than respondents with Chapter 5

an unstable and thresholds view (Fath and Beck 2005). However, non-native species were ranked low relative to the other risks included in the study. The second component, values of nature, is the reason why nature is perceived to be important. Prevailing concepts are those of instrumental (or functional) values and the intrinsic value of nature (the value nature has irrespective of its utility) (Van den Born et al. 2001). For example, people who value nature because of its functionality for humans may have a different perspective on non-native species than people who highly value the authenticity of nature (Van den Born and De Groot 2009). The final component is images of the human-nature relationship. Early attempts by philosophers such as Passmore (1974) and Barbour (1980) to classify images of relationships between humans and nature date back to the 1970s and 1980s. In the last decades, this has evolved into a qualitative and quantitative research field discerning between four classifications of human-nature relationships (De Groot et al. 2011; De Groot 1992; Kockelkoren 1993; Van den Born 2008): 1. Mastery over nature: humans stand above nature and are allowed to maximize exploitation of nature to benefit human society as detrimental effects of human actions can easily be overcome by economic growth and technology; 2. Stewardship of nature: humans stand above nature but have a responsibility towards future generations or God to take care of nature; 3. Partnership with nature: there is an equal relationship between nature and humans who 84 work together in a dynamic process of interaction and mutual development; 4. Participant in nature: humans are part of nature, not just biologically, but also with a sense of (spiritual) belonging. In two previous studies, these images of the relationship between humans and nature were found to act as predictors for preferred river management styles, with the Master being positively correlated with technical measures, and the more ecocentric views (i.e. Steward and Participant) rejecting drastic technological interventions (De Groot 2012; De Groot and De Groot 2009). The question of how to respond to biological invasions also addresses images of the relationship between humans and nature; therefore, visions of nature are relevant in understanding perceptions of non-native species and support for invasive species management.

Research aims In this study, we aim to explore the relationships between the lay public’s visions of nature (i.e. the meanings people attribute to nature based on experience and knowledge), their knowledge about non-native species, and their perceptions of non-native species and invasive species management in the Netherlands. Based on the previously discussed literature, the following research objectives were formulated. Figure 5.1 presents the coherence of the research objectives which are depicted by the numbered arrows: 1. to examine the relationship between the lay public’s visions of nature and perception of non-native species; Exploring public perception of non-native species

2. to examine the relationship between the lay public’s level of knowledge about non- native species and perception of non-native species; 3. to examine the predictive value of non-native species perceptions in support for invasive species management.

A. Visions of nature • Image of nature • Values of nature • Human-nature relationship

1 Non-native species

D. Support B. Level of 2 C. Perception 3 for knowledge management

Figure 5.1 Graphical representation of the coherence of research objectives of this study (numbers in the arrows correspond with the research objectives).

85 Material and methods

Survey population In order to examine the lay public’s perception of nature and non-native species, postal questionnaires were distributed in three municipalities in the Netherlands: (1) the city of Arnhem (population 150,000) located in a relatively green urban area in the centre of the Netherlands, (2) the village of Renkum (population 30,000) located about 10 km from Arnhem in a rural area, and (3) the village of Boskoop (population 15,000) located in the more urbanised western part of the Netherlands and well-known for its horticultural sector. In Boskoop, inhabitants were recently confronted with a situation that called for eradication of the non-native citrus longhorned beetle (Anoplophora chinensis) in their immediate surroundings. We included the inhabitants of this village in our study in order to investigate how their personal experiences with invasive species control influenced their perception of non-native species and management. Demographics of different parts of the Arnhem and Renkum municipalities (age, gender, income, and ethnicity in 2009) were compared with national numbers using StatLine from Statistics Netherlands (CBS 2010) to select similar households. Data were collected in the period November 2010 through February 2011, and included household members aged 18 years or older. Respondents had two options for completing the survey: a hardcopy could be returned in the pre-paid envelope we enclosed, or an identical questionnaire could be filled in online. In total, 1800 questionnaires were distributed and an overall response rate of 22.1 per cent yielded 398 filled-in questionnaires Chapter 5

which provided a sufficient number for analysis. Five respondents did not register their postal code, so their place of residence was unknown; these were excluded in analyses where location was entered as a parameter, but included in the overall analyses.

Survey design The survey consisted of four major components corresponding to the four boxes in Figure 5.1. These are visions of nature (A), level of knowledge about non-native species (B), non-native species perception (C), and acceptability of invasive species management (D). Demographics included were gender, educational level, and postal code. Membership of a nature protection organisation and frequency of visits to nature reserves were previously identified as relevant variables in the context of non-native species and visions of nature (Bremner and Park 2007; De Groot and De Groot 2009; Williams et al. 1992) and, therefore, added to the questionnaire. A translation of the questionnaire is available in Appendix 1. Question numbers given in the headings of the sub paragraphs correspond with the numbers in the questionnaire. Visions of nature (Q1, Q2 and Q6) To examine the lay public’s visions of nature, the previously discussed theories were operationalized. Values of nature and views on the human-nature relationship were measured using the Human and Nature (HaN) scale (De Groot and Van den Born 2003). This instrument measures ideas people have regarding the relationship between humans and nature, and has been tested worldwide (Fliervoet et al. 2013; De Groot 2012; De Groot and De Groot 2009; De Groot and van den Born 2007; Hunka et al. 2009). 86 This scale includes statements that fit four classifications of human-nature relationships (Appendix 2). Each category is represented by five statements to which respondents could react on a five-point scale from ‘strongly disagree’ to ‘strongly agree’. To obtain information on the general image people have of nature, we included three statements on what represents nature in relation to human intervention, autonomy, and wildness. Respondents could react to the statements on the same five-point scale. By calculating the average for each person, responses to these three statements were aggregated to a single score. Respondents with a high averaged score appear to hold a more pristine image of nature, while a low score indicates a broader representation of nature, which may also include city parks. In addition, respondents were categorized into one of four representations of balance in nature based on a one-item measure. The respondent had to choose one out of four different descriptions of the balance in nature, either (1) indifferent, (2) with thresholds, (3) unstable, or (4) stable. We modified the descriptions to match the ability of nature to deal with introductions of non-native species (Appendix 1). Level of knowledge (Q3-Q5) Questions about respondents’ knowledge of non-native species included definitions and examples of particular species. Correct identification of examples of species was checked for each respondent and only species names that are currently listed as non-native in the Dutch Species Catalogue (www.nederlandsesoorten.nl) were categorized as correct examples. The variable ‘knowledge’ then consisted of three categories: Exploring public perception of non-native species

1. people who were either not or mostly not familiar with the definition of non-native species and could not name a correct example (low level of knowledge). 2. people who were either mostly or completely familiar with the definition of non-native species or less familiar but could name at least one correct example (intermediate level of knowledge) 3. people who were either mostly or completely familiar with the definition and could name at least one correct example (high level of knowledge). Whether or not respondents had prior knowledge of management of particular non- native species in the Netherlands was addressed later in the questionnaire and used as a separate variable. Non-native species perception (Q7) Perception of non-native species was measured with 15 statements on: nature values in relation to non-native species (n = 4), perceived risks and benefits (n = 4), perceived need for management of invasive species (n = 5), and personal concern and engagement (n = 2). These statements were developed based on previous literature and form the basis for a new scale to measure non-native species perception (hereafter the NNS scale). Statements were measured on a five-point scale. However, if a certain level of knowledge about non-native species was required, a ‘don’t know’ option was included to obtain valid answers. These answers were recoded as neutral (as 0) in further analyses. Acceptability of management options (Q8) Eight illustrated examples of non-native species were given with a short introduction to 87 their origin and impacts in the Netherlands. The selection of species was based on their impact (i.e. economic, ecological, or health-related) and the species’ appeal defined by cuddliness, aesthetic value, and relatedness to humans. Recently introduced species tend to be more recognizable as non-native to the public than species which were introduced a long time ago (García-Llorente et al. 2008). Therefore, all species’ examples included in this study are recent introductions or ones that have recently become problematic. Three vertebrates with a high level of appeal and impact on biodiversity were selected: grey squirrel (Sciurus carolinensis ), ringnecked parakeet (Psittacula krameri ), and pumpkinseed sunfish Lepomis ( gibbosus). Furthermore, two plant species were chosen: the terrestrial common ragweed (Ambrosia artemisiifolia ) and the aquatic water pennywort (Hydrocotyle ranunculoides ) to represent species with an intermediate level of appeal and with human health and economic impact, respectively. Finally, three invertebrates with low levels of appeal were selected: red swamp crayfish (Procambarus clarkii ), citrus long horned beetle (Anoplophora chinensis ), and Asian tiger mosquito (Aedes albopictus ) to represent major impacts on biodiversity, economy, and human health, respectively. For each species, we asked whether it (1) should be accepted, (2) should be controlled to prevent further spread, or (3) should be eradicated. Also, for each species three management options were presented (e.g. use of pesticides, reproduction control, catching and shooting); the respondent could tick them if he or she deemed the measures acceptable for management of these species. A fourth option was ‘none of the above’. We created a dummy variable for each option to test whether the response differed per species (0 = not acceptable, 1 = acceptable). Analysis of variance (ANOVA) was used to detect dissimilarities between species. Chapter 5

Data analysis All five-point scale statements were recoded into a range from -2 to 2. The statements of the HaN and NNS scale were analysed using two rotated factor analyses. This method groups statements into factors based on similar answers of respondents. These factors then represent a coherent set of ideas respondents have. We used an oblique rotation method (Promax with Kaiser Normalization) to account for potential relationships between factors. The number of factors was determined using the scree plot, Kaiser’s criterion, and interpretation skills. Items with factor loadings above .350 were included in a factor. Respondents for which one or more answers were missing were excluded from the analysis. For each respondent, the average score of the items included in one factor was calculated. These scores could then be used as dependent variables in regression analyses. We controlled for the effects of living in Boskoop, where inhabitants were confronted with invasive species eradication, by creating two dummy variables using Boskoop residence as a baseline. Chi-square tests were used to compare the level of acceptance between species (i.e. to accept, control, or eradicate). We also calculated a cumulative score for level of acceptance per respondent by combining scores for all species. Cumulative scores range from 8 (accept all species) to 24 (eradicate all species) and were used as dependent variables in regression analyses with perception of non-native species as the predictor variable. All analyses were carried out using SPSS 19.0.

88 Results

Descriptive results Chi-squared tests were used to compare the sample composition of the three locations. Considerably more respondents from Arnhem (78%) had a polytechnical or university degree than respondents from Renkum (60%) and especially Boskoop (34%) (χ2 = 42.93, df = 2, P < 0.01). Respondents from Boskoop included more women (62%) compared to Arnhem (52%) and Renkum (44%) (χ2 = 6.82, df = 2, P < 0.05). In addition, they were less often a member of a nature protection organisation (46%) compared to 72 per cent and 61 per cent from Renkum and Arnhem respectively (χ2 = 15.09, df = 2, P < 0.01). Respondents’ visions of nature (A) The factors from principal axis factoring corresponded well with the original classifications from the HaN scale, and factors are composed solely of statements belonging to each group (Appendix 2). Cronbachs’s α for the factors were: Participant 0.73, Master 0.68, Partner 0.72, and Steward 0.64 which are reasonable values considering the small number of items per factor. The factors accounted for 37 per cent of the variance. Levels of adherence show that most respondents reject the Master image (-0.65). Participant and Partner both received a positive score (0.31 and 0.56, respectively), but respondents agreed most with the Steward image (1.46). For the Participant factor, the item about spending a week in the forest had a negative score, while all others were positive. This statement apparently depicts something most people do not feel comfortable with (independent of their vision of nature) and, therefore, scored negatively. Exploring public perception of non-native species

Respondents held divergent views on what represents nature. About 47 per cent of the respondents did not see wildness or absence of humans as requirements for real nature, in contrast to 24 and 29 per cent, respectively, who did think so. Half of the respondents did agree that nature is something that functions autonomously (50%). A vast majority of respondents (76%) agreed with a representation of balance in nature as long as certain threshold limits are not crossed. Second most popular was the representation of unstable nature (19%). Both the stable and indifferent views were chosen by only a small number of respondents (2% and 3%, respectively). Respondents’ level of knowledge (B) Level of knowledge on non-native species among the respondents was high, as 80 per cent reported being completely or mostly acquainted with the definition of non-native species. About half of the respondents (52%) could name a correct example, and an additional 97 respondents claimed they could give an example, but listed none or gave an incorrect example. Most cited species were the American bullfrog (Rana catesbeiana), citrus longhorned beetle (Anoplophora chinensis), red swamp crayfish (Procambarus clarkii), and black cherry (Prunus serotina). Furthermore, 72 per cent of the respondents reported prior knowledge of invasive species control in the Netherlands (but only 43% could name a species example here). Respondents’ perception of non-native species (C) Principal axis factoring revealed three factors from the NNS scale which accounted for 34 per cent of the variance (Appendix 2). The first factor grouped six items that relate to the perception of non-native species threathening nature values and human health (labelled 89 as perceived risk; Cronbach’s α = 0.72). High scores for this factor should be interpreted as a perception of high risk of non-native species, and a low score viewed as perceiving them to represent no significant ecological or human health hazard. The second factor consisted of five items that addressed non-native species control (labelled as control; Cronbach’s α = 0.71). Respondents with a high averaged score for this factor believe that non-native species that pose a risk to human health, biodiversity, or the economy, have to be controlled. This view is strenghtened by the negative score for the reversed phrased statement (i.e. “it does not matter if non-native species cause harm, they should always be allowed to stay”). The final cluster of items, calledengagement , grouped two statements on concern and engagement regarding problems with non-native species (Cronbach’s α = 0.60). A high score indicates more engagement in and concerns for problems with non- native species while a low score indicates less engagement and concern. For our sample, the total level of adherence to the factors of perceived risk (-0.04) and engagement (-0.05) showed impartiality on a scale from -2 to 2. This indicates there is no distinct high or low risk perception of non-native species, and that respondents had little concern for the presence of non-native species in the Netherlands. The score for control is quite high (1.05) indicating that respondents recognize the need for invasive species management. Support for management (D) Support for management strategies differed per species (χ2 = 1503.03, df = 14, P < 0.01) (Figure 5.2). The number of respondents in favour of accepting was highest for the appealing ringnecked parakeet, grey squirrel, and to a lesser extent, the pumpkinseed Chapter 5

tiger mosquito

citrus long horned beetle

water pennywort

common ragweed

red swamp crayfish

pumkinseed sunfish

grey squirrel

ringnecked parakeet

0% 20% 40% 60% 80% 100% 90 Accept Control Eradicate Missing (no answer)

Figure 5.2 Percentage of respondents who agreed on proposed management strategies (to accept, control or eradicate) for the eight species included in this study.

sunfish; while lowest for the tiger mosquito and the citrus longhorned beetle (both insect species). For eradication, the opposite pattern was found, with decreasing scores for increasing level of appeal. Proposed measures for control and eradication differed per species, but could be compared between species (Figure 5.3). Compared to the other species, the ‘none of the above’ option was more popular for the ringnecked parakeet and grey squirrel (P < 0.01). Scores for management of the ringnecked parakeet by shooting were lower than for the grey squirrel (P < 0.05). Overall, results also showed respondents rejected the use of pesticides (especially for animals living in an aquatic environment). An exception was made for the two insect species for which scores were significantly higher (P < 0.01).

Interrelations between visions of nature and perception of non-native species All variables were entered into three regression analyses with aggregated scores for perceived risk, control, and engagement as dependent variables. Although the models can explain only a small fraction of non-native species perception, the results show some interesting relations between visions of nature and non-native species perception (Table 5.1). A significant positive relationship exists between the most popular image of the human-nature relationship (i.e. steward) and control, which indicates that stewards are Exploring public perception of non-native species

A 1 B 1 c d 0.8 0.8 a b a-d 0.6 0.6 * 0.4 0.4 *

0.2 * 0.2

0 0

C 1 D 1

0.8 0.8

0.6 0.6

0.4 0.4 a 0.2 0.2 a

0 0

E 1 F 1 b c a,d a b-d 0.8 0.8 † 0.6 0.6 †

0.4 0.4 # # 0.2 0.2 * * 91 0 0

grey squirrel grey squirrel tiger mosquito tiger mosquito water pennywort water pennywort common ragweed common ragweed red swamp crayfish red swamp crayfish ringnecked parakeet pumpkinseed sunfish ringnecked parakeet pumpkinseed sunfish citrus longhorned beetle citrus longhorned beetle

Figure 5.3 Average scores and 95% confidence intervals for acceptance of several control methods for the eight species included in this study: A: No measures, B: Species removal, C: Reproduction control, D: Shooting, E: Natural enemy, F: Use of pesticides. Significance tests computed with one-way ANOVA (Games Howell posthoc procedure for unequal variances). Similar letters indicate significant differences between species for a particular intervention (P < 0.05). * significantly different from all other species (P < 0.01). #, † significantly different from all other species except those with similar symbol (P < 0.05). more associated with invasive species control than non-stewards (P < 0.01). Participants, on the other hand, are suggested to be more engaged than non-participants (P < 0.01), perhaps because people who adhere to this image are more connected to nature in general. Respondents with a pristine image of nature perceived risks of non-native species as more severe than respondents with a broader image of nature (P < 0.01). Finally, respondents who regarded balance in nature as unstable, perceived more risks of non-native species (P < 0.01), were more associated with control (P < 0.05), and were more engaged (P < 0.01) than respondents who depict balance in nature as a threshold system. Level of knowledge was identified as an important factor in predictingengagement of respondents. Compared to respondents with a high level of knowledge, respondents with a low or intermediate level were less engaged. Prior knowledge of invasive species Chapter 5

control also positively influenced engagement. Contrary to our expectations, place of residence did not have any predictive power. Regression analysis (P < 0.01) with cumulative management scores (ranging from 8 to 24) as dependent variable showed that the NNS perception variables perceived risk, control, and engagement are significant predictors (P < 0.01) explaining 28.5 per cent of the variance.

Table 5.1 Linear regression analyses for three variables measuring the perception of non-native species including names and descriptions of independent variablesa.

Independent variables Dependent variables Perceived risk Control Engagement Visions of nature Description beta beta beta Master Level of adherence to Master -0.025 0.103 0.001 (-2 lowest and 2 highest) Steward Level of adherence to Steward 0.037 0.156* -0.045 (-2 lowest and 2 highest) Partner Level of adherence to Partner 0.051 0.018 0.011 (-2 lowest and 2 highest) Participant Level of adherence to Participant 0.055 -0.008 0.201* (-2 lowest and 2 highest) Image of nature Averaged score -2 (broad image) 0.151* -0.007 0.040 and 2 (pristine image) B values B values B values Balance in nature Stable 0.016 -0.399 0.052 (compared to "thresholds") Unstable 0.343* 0.152** 0.311* 92 Indifferent 0.027 -0.129 0.412 Membership nature (0 = no, 1 = yes) -0.102 -0.088 0.232* protection organization Frequency nature visits Twice a month -0.070 0.021 0.026 (compared to "once a Monthly -0.014 0.037 0.235 week") Few times a year 0.157 0.038 0.178 Less than once a year 0.242 0.057 0.127 Knowledge and experience Level of knowledge Low -0.075 -0.155 -0.398* (compared to "high") Intermediate -0.034 -0.110 -0.332* Knowledge of actual control (0 = no, 1 = yes) 0.067 0.054 0.242** Place of residence Arnhem -0.095 -0.152 0.055 (compared to "Boskoop") Renkum 0.033 -0.104 0.055 Explained variance (including 14.5% 10.4% 24.3% demographic variables: gender, age and education) ANOVA P < 0.01 P < 0.05 P < 0.01 a Aggregated data show an approximately normal distribution with skew ≤ |.406| and kurtosis ≤ |.523|, with exception of the Steward with higher, but still moderate, values for skew ≤ |1.314| and kurtosis ≤ |2.184|. * P < 0.01 (2-tailed) and ** P < 0.05 (2-tailed). Exploring public perception of non-native species

Discussion

Survey and representativeness The purpose of this study was to explore relationships between the lay public’s visions of nature, their knowledge about non-native species, and their perceptions of non-native species and invasive species management in the Netherlands. Response rate and number of returned questionnaires were similar compared to other studies on nature perceptions in the Netherlands (Vaske et al. 2011). However, our approach to data collection (limited to three municipalities) and the inclusion of a village in which inhabitants were informed by the government about invasive species control may cause the sample to deviate from the Dutch population. Therefore, the results of this study should be interpreted as a case study within the Netherlands that provides useful information on non-native species perception in relation to visions of nature and level of knowledge about non- native species. In view of the main subject of the questionnaire, it is possible that people with an interest in nature are overrepresented in the sample. In the Netherlands, public support for nature protection is generally high, which is also reflected in frequent membership of nature protection organizations. Actual data about membership are not available, and therefore, could not be compared to our sample (in which 62% were members). Higher educated people tend to be more supportive of nature protection organisations, which may explain the high percentages of both groups in our sample. Despite the above- mentioned limitations, the results from the HaN scale are very similar to representative studies in the Netherlands (De Groot and De Groot 2009; Van den Born 2006) with a 93 high level of adherence to the steward and firm rejection of the master. In our study, the level of respondents’ knowledge of non-native species of was high; this may be partly explained by the large number of respondents who are members of a nature protection organisation (who also had more knowledge on non-native species, P < 0.01), self-selection, and the choice in locations. It is not surprising that the citrus longhorned beetle was one of the most cited species, as inhabitants of the municipality of Boskoop were informed about management of this invasive species in their surroundings.

Perception of non-native species Perception of non-native species was measured with 15 newly developed statements that were grouped based on similar answers by respondents using factor analyses. The resulting factors regarding non-native species control and personal engagement displayed a coherent set of items. However, the perceived risk factor included items on nature values as well as on risks and benefits and requires closer examination. All items but one (related to human health risk) addressed ecological impacts or threats to nature values. Our interpretation is the respondents may regard non-native species as an unnatural element in nature posing an ecological risk. Both perceived risk and control were moderately correlated with engagement (0.585 and 0.416, respectively), indicating that respondents who perceive more risks or are more in favour of invasive species control are also more engaged and concerned. Chapter 5

Overall results showed that respondents were impartial and not particularly concerned about non-native species in the Netherlands, but that they recognized the need for invasive species management when they pose a threat to nature, economy, or human health. However, many invasive species management programmes involve early eradications or preventive measures (e.g. making areas less susceptible for invasions). In such cases, threats are less apparent to the lay public and may reduce support for invasive species management. This may also be the case when other values come into play (e.g. related to place attachment). Other studies have shown that expert views of appropriate management of a natural area may deviate from those of other stakeholders (such as volunteers or frequent users), which may result in conflicts (Buijs 2009b; Ryan 2005). Knowledge was found to be an important factor in predicting personal engagement with problems caused by non-native species. Whether solving a possible knowledge deficit will also result in more support for invasive species control is a more difficult question. Other studies associated higher levels of knowledge with increased support levels for management options (Bremner and Park 2007; Ryan 2005). Based on their previous experiences, it was expected that perceptions of inhabitants from Boskoop might differ from the other two locations. Although scores indicated a higher preference for control in Boskoop, it did not significantly differ from the other groups.

Interrelations between visions of nature and perception of non-native species Although the predictive values of the regression analyses were low (Table 5.1), it did show that visions of nature variables had the highest unique contribution, and were 94 the most important predictors of non-native species perception. In congruence with Fischer and Van der Wal (2007) we found that perception of balance and naturalness are important in non-native species perception. Respondents who thought nature was not capable of dealing with non-native species and still maintain equilibrium were associated with increased perception of risk, need for management, and personal engagement. We acknowledge that concepts such as balance and equilibrium are disputed in the ecological sciences (Gunderson and Pritchard 2002). However, lay people’s perceptions of balance in nature are much less charged in that sense, simply because they are not aware of this discussion and their perceptions are based on their own observations and experiences in nature. Although a trend from an equilibrium paradigm to a more dynamic paradigm has become apparent in conservation biology, our result supports the view that this has not yet fully entered the public domain (Ladle and Gillson 2009; Wallington et al. 2005). Fath and Beck (2005) also found that respondents who thought of nature as unstable were in general more concerned about non-native species than respondents holding a stable or threshold view of nature. In our study, respondents had a strong preference for the unstable and threshold images of balance in nature, limiting comparability.

Support for non-native species management Categories of proposed management for species used in the survey (i.e. to accept, control, or eradicate) were similar to those in previous studies (Sharp et al. 2011). Even though the possibility for eradication of species was strongly formulated (i.e. to exterminate or extirpate), it did not restrain respondents from choosing this option. The high levels of support for management of non-native species in the Netherlands can be explained by the Exploring public perception of non-native species adherence of most respondents to a stewardship image in which human intervention is regarded as just. Dutch citizens have a cultural background in managing resources, spatial planning, and development of nature, coherent with the mind set of stewardship. Also, our species examples described hypothetical situations, and did not consider personal connections with an area such as place attachment. Previous research on ecological risk perception showed that controllable hazards were more often rated as needing stricter regulation (McDaniels et al. 1997). Written comments received in this study indicated that respondents not only considered acceptability purely based on humaneness of the measures, but also the feasibility of the proposed measures. As we did not specify on what terms it was to be acceptable, but aimed for general acceptability of the measures, the answers should be interpreted in that way as well. Even if general support for elimination of a species exists, there may be concerns about the type of measures used to achieve this goal (Ryan 2005). Our results, indicating different levels of support for measures per species, support this view. Acceptability of measures also differed greatly among species and reflected aesthetic motivations. The scores of acceptance for the ringnecked parakeet were remarkably higher than for all other species, and only very few respondents thought this species had to be eradicated (Figure 5.2). These results are similar to previous studies, which found that larger and companion species were most accepted by the public (Fitzgerald 2007), and that measures for control of bird species were the least supported (Bremner and Park 2007). By comparing the scores of the three perception variables (perceived risk, control and engagement) derived from factor analyses with the cumulative scores for actual species 95 management, we were able to investigate the predictive value of perception of non-native species in preference for species-specific management strategies. It proved that all three variables were important, and that, as expected, control was the most important predictor. This implies that variables derived from the NNS scale are meaningful and useful indicators for support of invasive species management. However, the overall predictive value was low, indicating the need for further research on predictors for support of non- native species management.

Concluding remarks In this paper we examined the relations between the lay public’s level of knowledge on non-native species, visions of nature, and attitudes towards non-native species. Overall, we conclude that lay public perceptions of non-native species have to be put in a wider context of visions of nature. Images of the human-nature relationship proved to be relevant in personal engagement in problems caused by invasive species, and in recognizing the need for control. Perhaps this reflects a feeling of responsibility for our actions that resulted in the introduction of non-native species. Images of nature appear to be most important in perceiving risks of non-native species to the environment. We found the level of knowledge was related to personal engagement in problems with invasive species. Considering the high level of knowledge of the respondents included in this study, we believe the general public is likely most served by species-specific information in a regional context. Public support for invasive species management depends on a multitude of factors that include risk perception and the type of species to be managed. We found that the perception of non-native species connects with more deep-lying and profound Chapter 5

visions of nature. Because these visions are often firmly anchored and difficult to change, they create challenges for policy makers and managers. Early stakeholder participation and risk communication are effective strategies to incorporate public values into policy, and thereby minimize conflicts.

Acknowledgements We thank Wiebe Lammers (Invasive Alien Species Team, Netherlands Food and Consumer Safety Authority, Wageningen) and Dr. Rob Leuven (Institute for Water and Wetland Research, Radboud University Nijmegen) for their comments on early survey drafts and data analyses, Drs. Chris Visscher (Department of Social Science Research Methodology, Faculty of Social Sciences, Radboud University Nijmegen) for statistical advice, Dr. Mirjam de Groot (Forest and Nature Conservation Policy, Wageningen University and Research Centre) for her advice on survey design and statistical analyses, and Jon Matthews (Institute for Water and Wetland Research, Radboud University Nijmegen) for his help with translating the questionnaire.

References Andreu J, Vilà M, Hulme PE (2009) An assessment of stakeholder perceptions and management of noxious alien plants in Spain. Environmental Management 43:1244-1255 Barbour IG (1980) Technology, environment, and human values. Preager Publishers, New York Bardsley D, Edwards-Jones G (2006) Stakeholders’ perceptions of the impacts of invasive exotic 96 plant species in the Mediterranean region. GeoJournal 65:199-210 Binimelis R, Monterroso I, Rodriguez-Labajos B (2007) A social analysis of the bioinvasions of Dreissena polymorpha in Spain and Hydrilla verticillata in Guatemala. Environmental Management 40:555-566 Bremner A, Park K (2007) Public attitudes to the management of invasive non-native species in Scotland. Biological Conservation 139:306-314 Buijs AE (2009a) Lay people's images of nature: comprehensive frameworks of values, beliefs, and value orientations. Society & Natural Resources 22:417-432 Buijs AE (2009b) Public support for river restoration. A mixed-method study into local residents' support for and framing of river management and ecological restoration in the Dutch floodplains. Journal of Environmental Management 90:2680-2689 Burt J, Muir A, Piovia-Scott J et al. (2007) Preventing horticultural introductions of invasive plants: potential efficacy of voluntary initiatives. Biological Invasions 9:909-923 CBS (2010) Statline. Statistics Netherlands. Online source: http://statline.cbs.nl/statweb/ (Accessed August 7, 2011) Cohen J, Mirotchnick N, Leung B (2007) Thousands introduced annually: the aquarium pathway for non-indigenous plants to the St Lawrence Seaway. Frontiers in Ecology and the Environment 5:528-532 Crall A, Newman G, Jarnevich C et al. (2010) Improving and integrating data on invasive species collected by citizen scientists. Biological Invasions 12:3419-3428 De Groot M (2012) Exploring the relationship between public environmental ethics and river flood policies in Western Europe. Journal of Environmental Management 93:1-9 De Groot M, De Groot WT (2009) "Room for river" measures and public visions in the Netherlands: a survey on river perceptions among riverside residents. Water Resources Research 45 (7):W07403 Exploring public perception of non-native species

De Groot M, Drenthen M, De Groot WT (2011) Public visions of the human/nature relationship and their implications for environmental ethics. Environmental Ethics 33:25-44 De Groot M, Van den Born RJG (2007) Humans, nature and god: exploring images of their interrelationships in Victoria, Canada. World Views: Environment, Culture, Religion 11:324- 351 De Groot WT (1992) Environmental science theory: concepts and methods in a problem- oriented, one-world paradigm. Studies in Environmental Science 52. Elsevier Science Publishers, Amsterdam De Groot WT, Van den Born RJG (2003) Visions of nature and landscape type preferences: an exploration in The Netherlands. Landscape and Urban Planning 63:127-138 Essl F, Nehring S, Klingenstein F et al. (2011) Review of risk assessment systems of IAS in Europe and introducing the German–Austrian Black List Information System (GABLIS). Journal for Nature Conservation 19 (6):339-350 European Environment Agency (2012) The impacts of invasive alien species in Europe. EEA Technical report No 16/2012. European Environment Agency, Copenhagen Fath BD, Beck MB (2005) Elucidating public perceptions of environmental behavior: a case study of Lake Lanier. Environmental Modelling and Software 20:485-498 Fischer A, Bednar-Friedl B, Langers F et al. (2011) Universal criteria for species conservation priorities? Findings from a survey of public views across Europe. Biological Conservation 144:998-1007 Fischer A, Van der Wal R (2007) Invasive plant suppresses charismatic seabird: the construction of attitudes towards biodiversity management options. Biological Conservation 135:256-267 Fitzgerald G (2007) Public attitudes towards invasive animals and their impacts. A summary and review of Australasian and selected international research. Invasive Animals Cooperative Research Centre, Canberra 97 Fliervoet JM, Van den Born RJG, Smits AJM et al. (2013) Combining safety and nature: a multi- stakeholder perspective on integrated floodplain management. Journal of Environmental Management 128 :1033-1042 García-Llorente M, Martín-López B, González JA et al. (2008) Social perceptions of the impacts and benefits of invasive alien species: Implications for management. Biological Conservation 141:2969-2983 Genovesi P, Bertolino S (2001) Human dimension aspects in invasive alien species issues: the case of the failure of the grey squirrel eradication project in Italy. In: McNeely JA (ed) The great reshuffling: human dimensions of invasive alien species. IUCN, Gland, Switzerland and Cambridge, UK, pp 113-120 Grendstad G, Selle P (2000) Cultural myths of human and physical nature: integrated or separated? Risk Analysis 20:27-40 Gunderson LH, Pritchard L (eds) (2002) Resilience and the behavior of large-scale systems. Island Press, Washington DC Hunka AD, De Groot WT, Biela A (2009) Visions of nature in Eastern Europe: a Polish example. Environmental Values 18:429-452 Kockelkoren PJH (1993) De vernieuwing van Nederland. Locus seminar:11-16 (in Dutch) Ladle RJ, Gillson L (2009) The (im)balance of nature: a public perception time-lag? Public Understanding of Science 18:229-242 McDaniels TL, Axelrod LJ, Cavanagh NS et al. (1997) Perception of ecological risk to water environments. Risk Analysis 17:341-352 Paolucci EM, MacIsaac HJ, Ricciardi A (2013) Origin matters: alien consumers inflict greater damage on prey populations than do native consumers. Diversity and Distributions 19:988- 995 Chapter 5

Passmore J (1974) Man’s responsibility for nature. Ecological problems and Western traditions. Duckworth, London Pejchar L, Mooney HA (2009) Invasive species, ecosystem services and human well-being. Trends in Ecology & Evolution 24:497-504 Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52:273-288 Ridder B (2007) An exploration of the value of naturalness and wild nature. Journal of Agricultural and Environmental Ethics 20:195-213 Ryan RL (2005) Exploring the effects of environmental experience on attachment to urban natural areas. Environment and Behaviour 37:3-42 Sharp RL, Larson LR, Green GT (2011) Factors influencing public preferences for invasive alien species management. Biological Conservation 144:2097-2104 Sijtsma MTJ, Vaske JJ, Jacobs MH (2012) Acceptability of lethal control of wildlife that damage agriculture in the Netherlands. Society & Natural Resources 12:1308-1323 Steg L, Sievers I (2000) Cultural Theory and individual perceptions of environmental risks. Environment and Behaviour 32:250-269 Storch S (2011) Forestry professionalism overrides gender: a case study of nature perception in Germany. Forest Policy and Economics 13:171-175 Teel TL, Manfredo MJ (2010) Understanding the diversity of public interests in wildlife conservation. Conservation Biology 24:128-139 Thompson M, Ellis R, Wildavsky A (1990) Cultural Theory. Westview Press, Oxford Van den Born RJG (2006) Implicit philosophy: images of the people-nature relationship in the Dutch population. In: Van den Born RJG, Lenders HJR, De Groot WT (eds) Visions of nature, a scientific exploration of people’s implicit philosophies. Berlin, lit-verlag, pp 61-84 98 Van den Born RJG (2008) Rethinking nature: public visions in the Netherlands. Environmental Values 17:83-109 Van den Born RJG, De Groot WT (2009) The authenticity of nature: an exploration of lay people's interpretations in the Netherlands. In: Drenthen M, Keulartz J, Proctor J (eds) New visions of nature: complexity and authenticity. Springer, Dordrecht, pp 47-66 Van den Born RJG, Lenders RHJ, De Groot WT et al. (2001) The new biophilia: an exploration of visions of nature in Western countries. Environmental Conservation 28:65-75 Vanderhoeven S, Piqueray J, Halford M et al. (2011) Perception and understanding of invasive alien species issues by nature conservation and horticulture professionals in Belgium. Environmental Management 47:425-442 Vaske J, Jacobs M, Sijtsma M (2011) Wildlife value orientations and demographics in The Netherlands. European Journal of Wildlife Research 57:1179-1187 Verbrugge LNH, Van der Velde G, Hendriks AJ et al. (2012) Risk classifications of aquatic non-native species: application of contemporary European assessment protocols in different biogeographical settings. Aquatic Invasions 7:49–58 Wallington TJ, Hobbs RJ, Moore SA (2005) Implications of current ecological thinking for biodiversity conservation: a review of the salient issues. Ecology and Society 10:15 Williams DR, Patterson ME, Roggenbuck JW et al. (1992) Beyond the commodity metaphor: examining emotional and symbolic attachment to place. Leisure Sciences 14:29-46

Chapter 6

Evaluating stakeholder awareness and involvement in risk prevention of aquatic invasive plant species by a national code of conduct

Laura Verbrugge, Rob Leuven, Johan van Valkenburg and Riyan van den Born

Aquatic Invasions 9(3): 369-381, 2014 Chapter 6

Abstract In 2010, Dutch stakeholders signed a code of conduct to prevent the introduction and spread of aquatic invasive plant species. This voluntary agreement between the government and horticulture sector (i.e. plant nurseries and retailers) has the objective to ban the sale of invasive species and to increase public awareness and stakeholder involvement in measures to prevent new introductions of potential invaders. Public outreach campaigns included flyers and posters displayed in stores and labelling of non- native plant species with warning logos and messages on harmful effects and appropriate disposal. We evaluated several measures issued in the Dutch code of conduct by performing ex ante and ex posterior surveys and interviews with relevant stakeholder groups. Compliance of retailers and producers concerning species on sale and proper labelling was monitored annually by the Netherlands Food and Consumer Product Safety Authority. Interviews with aquarists and water gardeners provided the first quantitative evidence in the Netherlands that 2-3 per cent of these hobbyists deliberately introduced non-native aquatic plants in surface water. A survey of retail professionals identified limited availability of information and lack of salesman’s knowledge on the species lists issued in the code of conduct as major impediments for their engagement. Furthermore, low frequency of meetings and lack of guidance were major obstacles identified by the partners assembled in the code of conduct. Overall, compliance to species bans showed promising results, however, problems were identified with correct labelling of species. We conclude by listing opportunities to improve voluntary regulations for preventing non- native species introductions.

Introduction The horticulture and ornamental trade are important pathways for the introduction and spread of non-native aquatic plants (Dehnen-Schmutz et al. 2007; Padilla and Williams 2004; Reichard and White 2001). Plants that ‘escape’ can cause severe ecological and 102 economic impacts in the recipient area. The number of recorded introductions of non- native plant species appears to be significantly correlated with human related variables such as population size or proximity to urban areas (Dehnen-Schmutz et al. 2007; Hussner et al. 2010). The introduction of Pumpkinseed sunfish (Lepomis gibbosus) in isolated pools and lakes in the Netherlands was traced back to public accessibility of these water bodies (Van Kleef et al. 2008). Thus, (intentional or unintentional) release of ornamental species into the environment creates new pathways for non-native species to spread. However, actual numbers of potential releases in relation to new species introductions in Europe are currently lacking, as well as information on potential groups of ‘releasers’ and their motivations. In 2008, the European Union stressed the importance of codes of conduct, which they defined as voluntary agreements developed to enlist the cooperation of the horticultural trade and associated professionals in reducing and controlling possible introductions of non-native invasive species (Heywood and Brunel 2008). Codes of conduct for the horticulture sector have become a popular policy instrument worldwide (Baskin 2002; Evaluating stakeholder awareness and involvement in risk prevention

Burt et al. 2007; Defra 2011, Halford et al. 2013, Kelly 2012, Peters et al. 2006), but assessments of their effectiveness are often lacking. Currently, decision makers have a specific need for this type of information to evaluate and improve policies on management of invasive species. The Netherlands is one of the biggest plant importing countries in Europe (Brunel 2009) and has populations of at least 24 non-native aquatic plant species in various types of water bodies (Hussner 2012). Many of these species are listed as (potentially) invasive in Europe (www.eppo.org) and their multitude of ecological and socioeconomic impacts (e.g. obstruction of water discharge and navigation) were counteracted by costly management programs (Pot 2002). In 2010, stakeholders agreed on a code of conduct to reduce the introduction and spread of aquatic invasive plant species in the Netherlands (Anonymous 2010). This code of conduct develops partnerships between the government and the horticulture sector. It was initiated by the Ministry of Economic Affairs (Office for Risk Assessment and Research, Netherlands Food and Consumer Product Safety Authority) and the Association of Regional Water Authorities. The representatives from the horticulture sector include three national trade associations for garden centres, pet stores and plant nurseries, respectively. The number of aquatic plant nurseries in the Netherlands is limited and all of them were asked to join the code of conduct. The current participants account for more than 95 per cent of the Dutch trade volume in aquatic plants. Two major agreements were made in the Dutch code of conduct. The first led to the compilation of two species lists. List 1 contains species that are banned from sale (i.e. Crassula helmsii, Hydrilla verticillata, Hydrocotyle ranunculoides, Ludwigia grandiflora, Ludwigia peploides, Myriophyllum aquaticum and Myriophyllum heterophyllum). List 2 species are allowed to be sold but only when additional information is provided for on a label. This warning label informs customers about the risks associated with plant invasiveness and instructions for ownership designed to reduce the risk of release of the plant to the environment (i.e. Azolla sp., Cabomba caroliniana, Eichhornia crassipes, Egeria densa, Lagarosiphon major, Pistia stratiotes and Salvinia molesta). The code of conduct became effective February 2011. The 103 partners also agreed to inform the general public about the harmful effects of the invasive plants listed, and how to dispose of plant waste. In 2010 and 2011, the government launched public outreach campaigns which included flyers and posters that were sent to all garden centres and pet stores in the Netherlands. The objectives of this study are to evaluate the following measures issued in the Dutch code of conduct for aquatic invasive plants: (1) the effectiveness of public awareness campaigns developed to inform aquarists and water gardeners, (2) the effectiveness of awareness campaigns developed to inform retail professionals, (3) the commitment of code of conduct partners, and (4) sector compliance with species lists. Finally, options to improve voluntary regulations developed to prevent non-native species introductions are discussed. Chapter 6

Material and methods

Data collection In order to fulfil our research aims, we performed ex ante and ex posterior surveys and interviews with relevant stakeholder groups (Table 6.1). Data were collected and analysed conform research guidelines and ensured anonymity of the respondents. Aquarists and water gardeners Aquarists and water gardeners were interviewed at garden centres and pet stores randomly distributed over the country. The selection of locations was based on the size of the store (in case of garden centres) and whether they were specialized in the sale of aquatic plants (in case of pet stores), and we requested permission from owners to interview people at their stores. In 2010, 13 locations in 7 provinces were visited, including 12 garden centres and one three-day aquaria event in a large pet store. In 2012, 15 locations were visited in 9 provinces, including 10 garden centres, 3 pet stores and the same three-day aquaria event. In order to effectively reach our target group, the first question addressed ownership of an aquarium or water garden, and if this was the case, the interview was continued. All questions were open ended, meaning that no answering categories were given, except for three statements with fixed categories. Data were collected in the months November and December of 2010 and 2012. The number of aquarists and water garden hobbyists interviewed was similar in both years (230 and 239 respondents, respectively). Questions for aquarists and water gardeners addressed their purchasing strategies (e.g. how often do they make a new purchase, where do they purchase aquatic plants, and what do they consider important plant characteristics), ways of disposal of plant waste, level of knowledge about non-native species and possible impacts, and their attitudes towards non-native species and impacts. Special attention was paid to their motivations for displaying certain behaviour or opinions. Demographics included date of birth, gender and level of education. Additional questions in the 2012 interviews addressed 104 their familiarity with warning labels and the governmental campaign. To avoid socially acceptable responses, the first part of the questionnaire consisted of general questions about their purchasing and disposal behaviour, before entering in the discussion of potentially invasive plants. An English translation of the questionnaire for aquarists and water gardeners is available in Appendix 3.

Table 6.1 Operationalization of research aims, including a reference to the actor(s) involved, methods and variables used. Number of Research aim Actor Method Variables respondents 1. Effectiveness of Aquarists and water Structured 5-minute 2010: n = 230 Level of knowledge public awareness gardeners interviews 2012: n = 239 Level of awareness campaigns Reported behaviour 2. Effectiveness of Retail professionals Postal questionnaires 2010: n = 164 Level of knowledge awareness campaigns 2012: n = 207 Level of awareness Corporate responsibility 3. Stakeholder Code of conduct Semi-structured 2010: n = 5 Commitment engagement and partners interviews 2012: n = 5 Division of tasks involvement Communication 4. Compliance with Plant nurseries and Site visits and 2010: n = 133 Compliance restricted sale species lists retail professionals sampling 2011: n = 107 Compliance labelling 2012: n = 76 Evaluating stakeholder awareness and involvement in risk prevention

Retail professionals In December 2010, postal questionnaires were sent to 600 garden centres using an extensive address list provided by the Netherlands Food and Consumer Product Safety Authority (NVWA). The number of pet stores in the Netherlands is about 1800, but these also include many stores that do not sell aquatic plants. First, all non-relevant pet stores were removed from the list, followed by a search with relevant key words which selected the most relevant ones (i.e. ‘aqua(rium)’, ‘fish’, ‘water’, ‘koi’ and ‘water garden’ or ‘pond’). Of the remainder of the list each fifth company was selected for a total of 300. Incorrect addresses were removed following the 2010 questionnaire and in 2012 the list was updated with newly opened stores. As a result, more questionnaires were sent in November 2012: 618 to garden centres and 313 to pet shops (total of 931). The first part of the questionnaire for retail professionals included questions about their business (type of store, whether they sold water garden or aquarium plants (or both) and membership of a trade organization), their level of knowledge about non-native (plant) species and attitudes towards non-native species and their impacts. The second part addressed engagement in and compliance to the code of conduct and questions on corporate social responsibility. Finally, we inquired input on possible improvements that could be made to the code of conduct. Identical questionnaires were used in both years, however, in 2012 we added questions on general support for the measures in the code of conduct and their knowledge of the species lists and warning labels. An English translation of the questionnaire for retail professionals is available in Appendix 4. All respondents from this group were either the owner, director or a member of the permanent staff. Response rates of 18 and 22 per cent yielded 164 and 207 correctly filled in questionnaires from retail professionals that actually sold aquatic plants for 2010 and 2012, respectively. Code of conduct partners Face-to-face interviews were held with representatives from the five organizations comprising the code of conduct, i.e. the Dutch Ministry of Economic Affairs, the 105 Association of Regional Water Authorities, and the three national trade associations for garden centres (Tuinbranche Nederland http://www.tuinbranche.nl/), pet stores (Dibevo http://www.dibevo.nl/) and plant nurseries (Cultuurgroep Vasteplantenkwekers http://www.nbvb.nl/). Two interviews were held with each respondent, the first in the year the code of conduct was signed and the second two years later. The interviews took place in the office of the interviewee, lasted approximately one hour and were recorded. An interview guide was developed listing the themes to be addressed in the interviews. The first interviews took place in the period November 2010 – January 2011 and included the following themes: personal engagement in problems with invasive aquatic plants, motivations for joining the code of conduct, expectations, division of tasks (or roles) and communication between partners. Themes addressed in the second interviews, held between November 2012 and January 2013, were public support for the measures, positive and negative developments, perceived effectiveness of the measures, and, again, division of tasks (or roles) and communication between partners. During the second interview the interviewees were also asked to respond to four statements about the effectiveness of the code of conduct (1) in general, (2) compared to a legal ban, (3) in changing behaviour of aquarists and water gardeners, and (4) regarding the warning labels specifically. Answering categories were: ‘strongly agree’, ‘agree’, ‘neutral’, ‘disagree’, ‘strongly disagree’. Chapter 6

Monitoring compliance with species lists In 2010, prior to the date the code of conduct became effective, a survey was conducted to access the availability of the species covered by the code of conduct. Based on the address list of the NVWA, used for general phytosanitary surveys, a random selection of 700 addresses was compiled. The site visits were performed by phytosanitary inspectors of the NVWA. In total 133 addresses selling aquarium or pond plants were visited, including garden centres, pet stores (especially aquarium shops) and production facilities distributed throughout the Netherlands. More locations were visited in densely populated areas than in less densely populated areas. The actual survey was conducted between July 10th and August 10th 2010, which is still considered low season for pond plants. During the first survey, species on sale were recorded as well as the use of the correct name for a given species. If the identity of a plant was in question, a sample was sent to the National Reference Centre of the NVWA for verification by experts. In 2011, 107 addresses were visited from January till June. These included 6 production facilities, 2 wholesalers, 98 garden centres and 1 aquarium shop. In 2012 data from 76 visits were available for analysis (1 production facility, 74 garden centres, and 1 florist). During the 2011 and 2012 surveys, records were made of the species on sale, the use of the correct name for a given species and the use of a label warning consumers not to dispose of the plants unwisely.

Data analyses Quantitative data from the surveys for hobbyists and retail professionals were analysed with SPSS 19.0. Answers to open-ended questions were categorized and grouped for easy interpretation and representation. Independent samples t-tests were used to compare the results between both years or between groups (e.g. aquarists and water gardeners). Chi- square tests were used to compare the results between groups for categorical variables. A significance level of P < 0.05 was used to determine differences between the samples. Interview recordings were transcribed and analysed qualitatively, based on the themes 106 outlined above. The NVWA records on compliance of production facilities and retail professionals with the species lists and labelling were analysed quantitatively using MS Excel.

Results

Aquarists and water gardeners In both years, the majority of the respondents was male (2010: 68% and 2012: 65%) and aged 40 years or older (2010: 80% and 2012: 68%). The percentage with a polytechnical or university degree was 36% and 41% for both years, respectively. In 2012, more aquarists (49%) than water gardeners (37%) were interviewed while the opposite was true for 2010 (30% aquarists and 56% water gardeners). There was no change in the percentage of respondents owning both an aquarium and water garden (2010: 14% and 2012: 13%). Aquarists and water gardeners differed in purchasing strategies, with over 80 per cent of the water gardeners buying only once a year or less and usually in garden centres, compared to aquarium owners who buy more frequently and usually in pet or specialist Evaluating stakeholder awareness and involvement in risk prevention stores (Table 6.2). When making a purchase, both groups reported priorities based upon plant aesthetics, type of plant (e.g. floating or submersed) and functional aspects. In general, water gardeners more often considered the function of the plant, while aquarists paid special attention to plant quality, size and personnel advice. Origin of the plant was mentioned to be decisive for buying by less than 3 per cent of the respondents with no difference between the two groups. Disposal methods reported by the respondents could be categorized in ‘waste’ and ‘re- use’ (Figure 6.1). Of the total group of respondents, the majority stated that they throw away surplus plants in the organic waste (2010: 61% and 2012: 67%) or regular waste (2010: 8% and 2012: 15%). Compost was also mentioned (2010: 11% and 2012: 9%). Exchanging plants with relatives or friends (2010: 23% and 2012: 22%) and relocating the plant to another pond or aquarium (2010: 3% and 2012: 4%) were popular ways to re-use a plant. In 2010 and 2012, 2 and 3 per cent of the respondents reported to release plants into open water in the environment, respectively. In 2010, this percentage consisted exclusively of water gardeners while in 2012 this also included people who owned both a water garden and an aquarium (Figure 6.1). Motivations for intentional release were related to respect for living things (e.g. “it is a waste to throw away living plants ”), aesthetics (e.g. “I think it is nice to see beautiful plants and flowers in the ditch ”) or practicality (e.g. “it does not smell bad ” or “it is easier ”).

Table 6.2 Purchasing behaviour of the total number of respondents who participated in the 2010 and 2012 survey and owned either an aquarium or water garden (in percentages). Results for respondents who owned both (n = 64) were excluded from the analyses.

Aquarium (n = 187) Water garden (n = 216) Type of storea Garden centre** 36.9 86.6 Pet store** 42.2 6.0 Specialist store** 33.2 8.3 Plant nursery 2.7 1.8 Internet** 3.7 0.0 107 Does not buy 1.6 3.7 Other** 1.6 5.5 Important plant characteristicsa Aesthetics 57.2 59.2 Function** 27.8 49.5 Type* 16.6 24.8 Quality** 18.7 8.7 Size* 11.8 6.0 Advice** 6.4 0.0 Price 7.5 4.1 Origin 2.1 1.8 Other** 22.0 14.2 Frequency < 1 per year** 15.0 43.1 Once a year** 16.6 38.9 Few times a year** 54.5 15.3 Every month** 13.9 0.5 a multiple answers allowed. *P < 0.05 and **P < 0.01. Significance tests computed with independent samples t-tests. Chapter 6

100% Aquarium Water garden Both 80%

60%

40%

20%

0% 20102012 2010 20122010 2012 2010 2012 2010 2012 2010 2012 2010 2012 organic exchange regular compost relocation intentional other waste or trade waste release

Figure 6.1 Methods of disposal reported by respondents who owned an aquarium, water garden or both in the 2010 and 2012 survey (multiple answers allowed). The percentage of respondents that were able to give a correct definition of non-native species (either referring to the species being non-indigenous or not originally from or 108 present in a country) was low (2010: 15% and 2012: 20%). The notion of the role of humans in the introduction of non-native species was generally lacking from the given definition. Many respondents thought that non-native species were species from ‘abroad’ or ‘warm or tropical areas’. We found an increase in the level of awareness of the origin of the species sold in garden centres and pet stores from 28 to 37 per cent over the period 2010-2012 (P < 0.05). In 2010 and 2012, 21 and 17 per cent of the respondents gave a correct example of a non-native species name, respectively. Most often named species (summed up for both years) were the common carp or koi (Cyprinus carpio), American bullfrog (Rana catesbeiana), elodea (Egeria densa) and floating pennywort (Hydrocotyle ranunculoides). In both years, seven out of ten respondents (2010: 70% and 2012: 72%) could give examples of impacts of aquatic invasive plants. The most cited impacts were proliferate plant growth, loss of native species, ecological damage, risk of carrying diseases and disturbance of balance of nature, with only very few respondents mentioning economic impacts or obstruction of waterways (Figure 6.2A). Hobbyists’ attitudes towards ecological impacts of aquatic invasive plants were similar in both years (Table 6.3). The majority reported to care either much or very much about the loss of a native species (2010: 66% and 2012: 72%) or the loss of diversity in an area (2010: Evaluating stakeholder awareness and involvement in risk prevention

A weed or proliferate growth

ecological damage *

outcompeting native species *

carrying diseases

other answers

disturbance of balance

obstruction of water ways

economical damage

0% 20% 40% 60% 80% 100%

B outcompeting native species

obstruction of water ways

weed or proliferate growth

disturbance of balance

negative influence on oxygen conditions 109 other answers

economical damage

0% 20% 40% 60% 80% 100%

Figure 6.2 Known impacts of non-native aquatic plants reported by Dutch aquarists and water gardeners (A) and retail professionals (B) in the 2010 (open bars) and 2012 (filled bars) survey. * significantly different between years (P < 0.05). Significance tests computed with independent samples t-tests.

84% and 2012: 87%) due to the introduction of a non-native species. Their motivations revealed that they considered (1) that conservation of native species and nature values are important, (2) that non-native species do not belong here or (3) that the balance in a natural system will be disturbed. An increase was found in the self-reported level of engagement of respondents (Table 6.3), however, levels of engagement remained low with an average score of 3.1 on a five-point scale. In 2012, 39 per cent of the respondents reported not to be engaged, mainly because they do not think about the effects of aquatic invasive plants in their daily lives or because they do not think they personally play a role Chapter 6

Table 6.3 Response of aquarists and water gardeners to statements on potential ecological impacts of non-native species and their personal level of engagement in 2010 and 2012, including number of respondents (n), average scores, standard deviation (SD) and P-values.

Average score Year n SD P-valueb (scale 1-5)a What if a native species would disappear as the result 2010 230 2.36 0.98 of the introduction of a non-native species. To what 0.248 degree would you care about that? 2012 238 2.25 1.05 What if a non-native species would grow so fast that 2010 228 1.90 0.92 it would reduce the variation of species in an area. To 0.717 what degree would you care about that? 2012 238 1.93 0.82 To what extent do you consider yourself to be 2010 229 3.47 1.25 personally engaged in problems caused by invasive 0.005* species? 2012 238 3.14 1.26 a: score 1-5: very much – not at all. b: independent samples t-test (*significant atP < 0.05).

and therefore have no responsibilities. Other reasons were that they did not know about it or that they did not think they could do anything about it (i.e. no influence). Hobbyists’ familiarity with warning labels and the governmental campaign (only measured in 2012) was found to be low. Of the total group, 16 per cent recognized the campaign slogan and 12 per cent the warning logo for appropriate disposal of invasive species. For the latter, there was a difference between respondents who owned an aquarium or a water garden (P < 0.05), with aquarists being less informed (9% recognized the logo) compared to water gardeners (18% recognized the logo). In both surveys (2010 and 2012) only 4 per cent of the respondents claimed to have been informed about potential invasiveness when purchasing a new plant.

Retail professionals In both years about two thirds of the retail professionals that were surveyed worked at a garden centre (2010: 65% and 2012: 60%). The other respondents owned or worked at a pet store (2010: 32% and 2012: 26%), specialist store (2010: 1% and 2012: 8%) or 110 other businesses such as wholesale or a combination of a garden centre with professional gardening or flower shops. Stock size of aquarium and aquatic plants were similar in both samples. In both years, eight out of ten respondents was a member of a trade association (2010: 80% and 2012: 81%). In general, garden centres reported membership of Tuinbranche Nederland (tailored to the needs of garden centres) and pet and specialist stores were a member of Dibevo (an association for businesses that are concerned with selling pets). The level of knowledge about the definition of non-native species among retail professionals was high, as nine out of ten reported to be either completely or largely familiar in 2010 (95%) and 2012 (96%). In 2012, 73 per cent could name examples of impacts of non-native aquatic plants compared to 78 per cent in 2010. The three most cited impacts were impacts on native species, weed or proliferate growth and obstruction of water ways (Figure 6.2B). Similar attitudes of retail professionals towards ecological impacts of invasive species were found for both years (Table 6.4). The scores reflected recognition of declining nature values and other risks associated with non-native species. While in 2012 about half of the respondents (47%) reported to be personally engaged in the topic of invasive Evaluating stakeholder awareness and involvement in risk prevention plant species, only one out of four (23%) claimed it to be an important topic within the company. For these two variables, no differences were found between 2010 and 2012 (Table 6 4). The percentage of retail professionals that reported to limit invasive plants in their stock increased over the two-year period from 55 to 61 per cent (P < 0.05). In 2012, we asked retail professionals specific questions concerning their knowledge about the code of conduct. Only five per cent of the respondents considered him or her well informed about the agreements that were made in the code of conduct. About half of the respondents from garden centres (51%) reported to be reasonably informed while six per cent reported to have no knowledge about it. For pet stores, only 25 per cent was reasonably informed, while one in three respondents (32%) reported to have no knowledge about the code of conduct. We asked the respondents who reported to be well or reasonably informed about the code of conduct additional questions about their compliance and support. A small number (16%) reported to have experienced troubles with compliance in the beginning but on the whole this was not considered a problem and the majority claimed to support the code of conduct. In 2012, about 35 per cent of the respondents reported that the employees in their store were (largely) familiar with the species lists. This differed for garden centres and pet stores (χ2 = 23.92, df = 3, P < 0.01), with lower reported levels of knowledge for employees of pet stores (Table 6.5). With respect to warning labels, 41 per cent of the respondents stated that their employees were familiar with the these labels. For this variable, no statistical differences were found between garden centres and pet stores, however, the results indicate that employees of pet stores tend to be less familiar with warning labels than employees of garden centres (Table 6.5).

Table 6.4 Response of retail professionals to statements on ecological impacts of non-native species and their personal level of engagement in 2010 and 2012, including number of respondents (n), average scores, standard deviation (SD) and P-values.

Average score Year n SD P-valued 111 (scale 1-5)

Non-native species pose a threat to biodiversity in the 2010 163 3.76a 1.01 0.580 Netherlands 2012 205 3.82a 1.02 Presence of non-native species makes a nature area 2010 163 3.36a 1.14 0.367 less valuable 2012 200 3.47a 1.12 Non-native species complement biodiversity in the 2010 161 2.50a 1.14 0.515 Netherlands 2012 203 2.42a 1.13

a Animals and plants that came to the Netherlands only 2010 163 3.62 1.16 0.395 because humans facilitated it, do not really belong here 2012 205 3.52a 1.14

Non-native species that spread quickly and compete 2010 163 4.22a 0.94 0.909 with other species must always be controlled 2012 205 4.21aa 0.91 Extent of personal engagement concerning the topic of 2010 163 2.58b 1.12 0.256 non-native species 2012 206 2.71b 1.10 Relative importance of the topic of invasive aquatic 2010 162 3.30c 1.11 0.666 plants in operational store management 2012 206 3.25c 1.05 a: score 1-5: strongly disagree – disagree – neutral – agree – strongly agree; b: scores 1-5: high interest - moderate interest - neutral - little interest - no interest; c: scores 1-5: very important - important - neutral - little important - not important; d: independent t-test (significant atP < 0.05). Chapter 6

Table 6.5 Familiarity of employees of garden centres and pet stores with the species lists and warning labels as reported by the retail professionals who participated in our study (2012 survey; numbers are percentages).

Garden centres (n = 130) Pet stores (n = 68) Familiarity with species lists Completely 2.3 2.9 Largely familiar 40.8 20.6 Largely unfamiliar 42.3 30.9 Unfamiliar 14.6 45.6 Familiarity with warning labels Yes 45.0 32.4 No 28.2 51.5 Do not know 26.7 16.2

In the 2012 survey, one in three (33%) of the retail professionals made suggestions for improving communication about the code of conduct. The three most cited improvements were (1) repetition of the message at the start of the season, (2) clear and more targeted communication about the species lists, and (3) use of visual aids in explaining impacts.

Code of conduct partners Interviews with the five major partners involved in the code of conduct were qualitatively analysed with a focus on their opinions on the effectiveness of the measures, future perspectives and suggestions for improvement. By signing the code of conduct, all partners acknowledged that preventive measures are needed to stop the spread of invasive aquatic plants and made a commitment to take part in these measures. Their cooperation was founded on mutual recognition of the problems caused by invasive aquatic plants. In 2012, all partners agreed with the statement that “the code of conduct contributes to tackling problems caused by invasive aquatic plants ”. From the interviews it became clear that the topic of invasive aquatic plants is framed as part of a ‘bigger picture’. The governmental parties consider it a species-specific measure in their policy strategy for invasive species. For 112 the trade associations and production facilities it fits in the concept of corporate social responsibility to take environmental aspects of their products into account. The role the interviewees assign to the other partners and themselves is closely related to their tasks prescribed in the code of conduct. The trade associations are seen as ‘communicators’ and their main duty is to defend the stakes of their members (i.e. garden centres, pet stores and plant nurseries) and to inform them about the measures issued in the code of conduct. The Association for Regional Water Authorities (which represents the 24 water boards in the Netherlands) is regarded as the partner who has the most to gain. The water boards maintain the Dutch water ways and have a role in communicating with the public. The umbrella organization has to make sure that all water boards are informed about the communication strategy. The views on the role of the national government were most divergent, including both facilitating and leading roles. In general, the majority of the other partners agreed that both roles were insufficiently supported and spoke up for a more visible and accessible leading partner. This was, for example, the case when new partners wanted to sign the code of conduct but did not know about any procedure to do so. Another example was the lack of communication with and between the partners apart from a yearly meeting to discuss developments. While two partners Evaluating stakeholder awareness and involvement in risk prevention did not find this problematic, the others thought it would positively contribute to the engagement of the partners throughout the year. To measure the effects of the code of conduct it is important to evaluate which actions have been taken by the partners and whether these match their intentions. The second interviews showed that the intensity of efforts from all partners decreased between 2010 and 2012. Main reasons that were given were lack of time and man-hours, lack of a sense of urgency and the fact that certain actions needed to be done only once (e.g. label production for list 2 species). Overall, the partners remained supportive of the measures in the code of conduct, and this was also deemed to be the case for the members of the trade associations. There seemed to be no severe financial consequences for the production facilities and retail professionals, partly because of the one year intervening period to sell existing stocks, but also because there were enough alternatives for list 1 species. The impression of the representatives from the trade associations is that the lists are well-known within the production facilities but that this is not the case for salesmen at garden centres and pet stores. Four out of the five interviewees agreed with the statement thatwarning “ messages on labels will increase public awareness ”. One partner disagreed stating that there are already too many labels fighting for attention and that the message may be too complex to depict. The majority of the interviewees did agree that increased public awareness will result in more responsible ways of disposal, but they note that this change will come slowly. One interviewee voted neutral for the statement that “increasing public awareness about the impacts of invasive aquatic plants will automatically lead to a behavioural change ”. On the one hand gardeners and aquarium hobbyists were depicted as a ‘willing’ public and receptive of the message, but on the other hand they may be reluctant to throw away living materials out of respect for nature. A legal ban can be considered as an alternative to a code of conduct if it proves to be unsuccessful. All partners recognized this option but they did not see a legal ban as the ultimate solution. The partners from trade would lose the opportunity to have a say in the 113 matter, and the government would have to invest in legal enforcement. Two interviewees agreed to the statement that “a legal ban is more effective than a voluntary agreement ”. However, they explained that this is only the case if there is proper enforcement and that they remain supportive of the code of conduct when it yields positive results. In any case, external influences that impede the effectiveness of any measure must be ruled out before any changes are considered. Therefore, all partners stressed the importance of an evaluation after four years.

Compliance with species ban and labelling The number of list 1 species found at plant nurseries and retail professionals in the Netherlands decreased tremendously and were found only incidentally in 2011 and 2012 (Table 6.6). We did not find any changes in the detection of list 2 species, of which more than 200 findings were reported each year. In 2011, 31 per cent of the list 2 species were correctly labelled with a warning. In the following year, this was the case for 45 per cent of list 2 species. Oxygenating plants, such as Cabomba caroliniana and Egeria densa, are often sold in bunches containing several species. In 2011, C. caroliniana or E. densa were found in Chapter 6

oxygenating plant bunches at 36 sites. At only 5 of these 36 sites, bunches were correctly labelled for presence of C. caroliniana, and E. densa. In 2012, the number of sites where C. caroliniana or E. densa were found as part of oxygenating plant bunches was 43 and 40, respectively (44 sites in total). Of these 18 per cent were correctly labelled.

Table 6.6 Number of batches of code of conduct species found and number of sites where bunches of oxygenating plants were on sale during surveys of the National Food and Consumer Product Safety Authority (NVWA) in the period 2010-2012. Numbers between brackets indicate the number of batches of list 2 species found that were correctly labelled with a warning message or sites where oxygenating plant bunches were properly labelled.

Number of sites selling oxygenating plant bunches Regular (single) species sales (in batches) (containing Cabomba caroliniana or Egeria densa) List 1 species List 2 species C. caroliniana E. densa 2010 96 262 (n.a.) n.a. n.a. 2011 2 222 (69) 36 (5) 25 (2) 2012 3 261 (118) 43 (8) 40 (7) n.a.: not applicable

Discussion In this study, we evaluated several measures issued in the Dutch code of conduct for aquatic plants by performing ex ante and ex posterior surveys and interviews with relevant stakeholder groups. We used a three-tiered research approach in which quantitative analyses of survey data are combined with monitoring data and qualitative data from interviews. This is a common approach in evaluation studies since it provides valuable data on the effectiveness of a policy instrument as well as on the process of reaching these goals (Rowe and Frewer 2004). Because aquatic plants are sold seasonally, timing of surveys may influence the results. In this respect it was of vital importance to conduct 114 both surveys in the same time period. Aquarists and water gardeners were surveyed in the winter period. Although off season regarding the sale of pond plants, this was a convenient time to yield a high response because of high visitor rates for garden centres. We interviewed 230 and 239 aquarists and water gardeners in 2010 and 2012, respectively, at garden centres and pet stores randomly distributed over the country. Whether these samples are sufficient to make general statements about aquarists and water gardeners in the Netherlands is difficult to determine because of a lack of knowledge on the number of people that constitute this group and their population characteristics. The numbers of hobbyists interviewed are high compared to other studies (Gertzen et al. 2008; Halford et al. 2013; Martin and Coetzee 2011). The response rates for the retail professionals (16 and 22%) were similar to other studies about attitudes towards invasive plants in the horticultural sector (Burt et al. 2007; Halford et al. 2011; Peters et al. 2006).

Level of awareness among hobbyists Empirical data on the modes and number of species introductions provide direct targets for policy intervention aimed at prevention of new introductions of invasive species. In this study, aquarists and water gardeners were identified as playing a significant role in Evaluating stakeholder awareness and involvement in risk prevention the introduction and spread of invasive aquatic plants into natural water bodies (Figure 6.1). Studies conducted in North America reported similar modes of plant disposal, including waste, re-use and intentional release (Cohen et al. 2007; Marson et al. 2009a, 2009b). Intentional release by aquarists found in other studies ranged between 3 per cent for aquatic plants (personal comm. Dr. B. Leung March 19, 2011) and 7 per cent for ornamental fish (Gertzen et al. 2008; Strecker et al. 2011). However, plants, fragments or seeds may also be introduced unintentionally into the environment when complete contents of aquaria are emptied into water bodies (Duggan 2010; Van Kleef et al. 2008) or by composting of plant material (Duggan 2010; Rusterholz et al. 2012). Increasing public awareness concerning their role in species introductions was expected to result in more responsible ways of handling plants and animals. One of the objectives of this study was to evaluate the effectiveness of public outreach campaigns in increasing public knowledge and awareness on invasive aquatic plants. In congruence with other studies, we found that the level of reported knowledge about the definition of non-native species was lower for the general public compared to professionals (Halford et al. 2013), and especially lacked the notion of the role of humans in introductions (Verbrugge et al. 2013). Compared to the level of factual knowledge, impacts of aquatic invasive plants were better known but were limited to ecological effects. Low levels of personal engagement found in this study contrasted somewhat with the high percentages of the respondents that reported to regret the loss of native species (> 65%) or the loss of diversity in an area (> 80%) resulting from the introduction of non-native species. Probably, the question design played a role here, and may have triggered socially acceptable responses. As a result, the respondents may, in fact, be less concerned about the effects of invasive aquatic plants than is indicated by the results. The level of awareness of the origin of plants sold in garden centres and pet stores among aquarists and water gardeners increased to just over one-third of the respondents over the period 2010-2012. Overall, only limited effects of the campaign on public knowledge and awareness were found in this study. This implies that education of the public is not straightforward (see also Halford et al. 2013). Possible explanations reported by the code of conduct 115 partners interviewed in this study include the fact that educating the public is a long term process, especially if it concerns behavioural change, and the low visibility of flyers and warning labels. Analyses of purchasing behaviour of aquarists and water gardeners also pointed out some valuable considerations for the development of communication strategies, for example in terms of frequency and location of plant purchase. Generally, we can conclude that only informing the public at the time of purchase will not be sufficient to reach the target group. In order to reach non-frequent buyers, a more general strategy with a wider scope is needed. Recent studies expressed their concerns about increasing internet sales (Giltrap et al. 2009; Kay and Hoyle 2001; Martin and Coetzee 2011; Matthews et al. 2012). The internet was not a popular medium to purchase aquatic plants among the respondents included in our study (Table 6.2). However, this may be an underestimation due to our recruitment of respondents at garden centres and pet stores, creating a bias towards people who buy at stores. Chapter 6

Level of awareness among retail professionals Several studies identified insufficient knowledge and awareness among crucial stakeholders, such as retail professionals, as major impediments for successful risk prevention (Burt et al. 2007; Chang et al. 2009; Cohen et al. 2007). We found that store owners were quite well informed about the general topic and potential adverse effects of invasive species and supported the idea of responsible use of their products. Compared to the group of aquarists and water gardeners, retail professionals were more aware of socioeconomic impacts of invasive aquatic plants (Figure 6.2), which may be explained by the information package that was sent to all garden centres and pet stores by the government. Moreover, self-selection among respondents may have resulted in an overestimation of the level of awareness and knowledge. However, the results from this study also showed that, despite their general knowledge on the effects of non-native species, specific knowledge about the code of conduct, species lists and warning labels was limited among retail professionals. This is particularly noted among employees of pet stores. Furthermore, less than five per cent of the aquarists and water gardeners that were interviewed in this study claimed to have been informed by employees when purchasing a plant. Thus, in order to maximize the use of seller-buyer interactions as a means for educating the public, more efforts are needed to increase the level of knowledge about the species lists and agreements in the code of conduct at the salesmen level. No changes were found in personal engagement of respondents in retail and, in both years, only one out of four reported that potential invasiveness of plant species was an important topic within the company. The fact that more than half of the retail professionals included in this study reported to reduce invasive plants in their stock (with an increase between 2010 and 2012) then suggests that the availability at plant nurseries is a decisive factor here. Thus, in this case of restricted sale, cooperation of plant nurseries and wholesale businesses appears to be a more effective strategy than targeting individual stores.

116 Commitment of code of conduct partners The role of ornamental species trade in the spread of non-native species represents a multi-stakeholder problem with different perceptions and interests. Therefore, the success of a code of conduct depends on many factors, such as participation of all relevant stakeholders and compliance to the proposed measures. The interviews held with the partners showed that they continually recognize the need for the code of conduct. However, their efforts have decreased over time which has had a negative effect on the output and efficiency of its application. Explanations given by the respondents regarding their self-observed decrease in commitment included poor communication between partners, infrequent meetings and discrepancies about the roles and tasks assigned to each partner. General concerns about voluntary policy instruments, also expressed by the interviewees in this study, relate to its permissiveness and lack of sanctions. A commonly considered solution is a trading ban for invasive species to reduce the risk of further entry (Drew et al. 2010). In Europe, free trade within the European Union and a lack of uniformity of invasive species policies are major barriers in effective policy and legislation (Brunel et al. 2013; Hulme 2010). This explains the recommended use of codes of conduct Evaluating stakeholder awareness and involvement in risk prevention for self-regulation in the sector (Heywood and Brunel 2008). Currently, EU legislation is prepared for a limited number of species, including some invasive aquatic weeds (European Commission 2013). Our results show that, even though some partners may have preferred a ban initially, they are all supportive of the code of conduct. However, they stress the importance of performing an evaluation to measure its effectiveness.

Compliance with species lists Involvement of the major producers and three national trade organizations representing 95 per cent of the trade volume has proven to be an effective strategy for restricted sale. Monitoring of compliance with species lists showed that list 1 species were found incidentally in 2011 and 2012 (Table 6.6) and in most cases these concerned companies that were not signatory of the code of conduct or plants that originated from old stock. The second list contained species which were allowed to be sold but only with a warning label. This strategy proved to be less effective as less than half of the plants that were found during the monitoring in 2011 en 2012 were correctly labelled. Differences were also found between pond and aquarium plants. Often not only list 2 species but all non-native pond plants were provided with a warning label, explaining the customer to dispose of excess material wisely in bins for organic waste and not to spread in public water bodies. Labelling of aquarium plants remains problematic, partly due to the smaller size of the product, and the extra costs involved in providing the labels, as is the case with plant bunches. Mislabelling is a well-recognized problem in trade of ornamental species. This, in combination with limited taxonomic expertise of retail professionals, may result in the selling of a species for which trade is banned (Thum et al. 2012). Often, mislabelling of plants is justified using the argument that the customer is familiar with a particular name or that the correct name is too difficult. Salvinia molesta is consistently mislabelled as Salvinia natans and likewise Cabomba caroliniana as Cabomba aquatica (Brunel 2009). The high level of import of C. caroliniana under the name C. aquatica and possible confusion between the two species by hobbyists may result in its continued use in aquaria and 117 ponds and potential disposal to the freshwater network, despite attempts by Dutch nature organizations and water boards to educate the public (Matthews et al. 2013). Proper labelling of Myriophyllum species requires a combination of morphological and molecular work of which first results can be found in the interactive identification key and molecular data available on Q-bank (http://www.q-bank.eu/Plants/) (Ghahramanzadeh et al. 2013; Van Valkenburg et al. 2013).

Concluding remarks Voluntary policy instruments such as codes of conduct have gained popularity in invasive species management. This study evaluated the effectiveness of the Dutch code of conduct for aquatic invasive plants. The results show that aquarium and water garden hobbyists facilitate the introduction and spread of invasive aquatic plants into natural water bodies which demonstrates the need for increasing public awareness. Of the four measures evaluated in this study, the compliance with restricted sale of list 1 species was found to be most effective. For the other measures (including public outreach campaigns and labelling of list 2 species) the results are less univocal and stress the need for long term evaluation studies. Chapter 6

Acknowledgements This study was commissioned by the Netherlands Food and Consumer Product Safety Authority of the Dutch Ministry of Economic Affairs (TRPCD/2010/2351). The authors thank Jon Matthews, Frank Collas, Remon Koopman for additional data on internet sales in the Netherlands, and Wiebe Lammers, José Vos and Maarten Steeghs for critical comments on earlier results of our study. Finally, we thank all interviewees and stakeholders contributing to surveys.

References Anonymous (2010) Convenant waterplanten. Staatscourant 11341, dd. 21- 7 - 2010, pp. 6 (in Dutch) Baskin Y (2002) The greening of horticulture: new codes of conduct aim to curb plant invasions. Bioscience 52:464-471 Brunel S (2009) Pathway analysis: aquatic plants imported in 10 EPPO countries. EPPO Bulletin 39:201-213 Brunel S, Fernández-Galiano E, Genovesi P et al.(2013) Invasive alien species: a growing but neglected threat? In: Late lessons from early warnings: science, precaution, innovation. European Environmental Agency, pp. 518-540 Burt JW, Muir AA, Piovia-Scott J et al. (2007) Preventing horticultural introductions of invasive plants: potential efficacy of voluntary initiatives. Biological Invasions 9:909-923 Chang AL, Grossman JD, Spezio TS et al. (2009) Tackling aquatic invasions: risks and opportunities for the aquarium fish industry. Biological Invasions 11:773-785 Cohen J, Mirotchnick N, Leung B (2007) Thousands introduced annually: the aquarium pathway for non-indigenous plants to the St Lawrence Seaway. Frontiers in Ecology and the Environment 5:528-532 Defra (2011) Helping to prevent the spread of invasive non-native species: horticultural code of practice. Department for Environment, Food and Rural Affairs (Defra), London, pp. 9 Dehnen-Schmutz K, Touza J, Perrings C, et al. (2007) The horticultural trade and ornamental 118 plant invasions in Britain. Conservation Biology 21:224-231 Drew J, Anderson N, Andow D (2010) Conundrums of a complex vector for invasive species control: a detailed examination of the horticultural industry. Biological Invasions 12:2837- 2851 Duggan I (2010) The freshwater aquarium trade as a vector for incidental invertebrate fauna. Biological Invasions 12:3757-3770 European Commission (2013) Proposal for a regulation of the European parliament and of the council on the prevention and management of the introduction and spread of invasive alien species. COM/2013/0620, Brussels, Belgium, pp. 36 Gertzen E, Familiar O, Leung B (2008) Quantifying invasion pathways: fish introductions from the aquarium trade. Canadian Journal of Fisheries and Aquatic Sciences 65:1265-1273 Ghahramanzadeh R, Esselink G, Kodde LP et al. (2013) Efficient distinction of invasive aquatic plant species from non-invasive related species using DNA barcoding. Molecular Ecology Resources 13:21-31 Giltrap N, Eyre D, Reed P (2009) Internet sales of plants for planting: an increasing trend and threat? EPPO Bulletin 39:168-170 Halford M, Heemers L, Mathys S et al. (2011) Socio-economic survey on invasive plants and ornamental horticulture in Belgium. University of Liège Gembloux Agro Bio-Tech, pp. 29 Evaluating stakeholder awareness and involvement in risk prevention

Halford M, Heemers L, Dierickx M et al. (2013) Perception of invasive alien plants by the horticultural sector in Belgium: the AlterIAS project and the changes of attitudes after four years of awareness-raising. University of Liège Gembloux Agro Bio-Tech, pp. 31 Heywood V, Brunel S (2008) Code of conduct on horticulture and invasive alien plants. Convention on the conservation of European wildlife and natural habitats, Standing Committee, 28th meeting Strasbourg, 24-27 November 2008, pp. 35 Hulme PE (2010) Biosecurity: the changing face of invasion biology. In: Richardson DM (ed) Fifty years of invasion ecology. Wiley-Blackwell, Oxford, UK, pp. 301-314 Hussner A (2012) Alien aquatic plant species in European countries. Weed Research 52:297-306 Hussner A, Van De Weyer K, Gross EM et al. (2010) Comments on increasing number and abundance of non-indigenous aquatic macrophyte species in Germany. Weed Research 50:519-526 Kay SH, Hoyle ST (2001) Mail order, the internet, and invasive aquatic weeds. Journal of Aquatic Plant Management 39:88-91 Kelly J (2012) Horticulture code of good practice to prevent the introduction and spread of invasive non-native species. V2.0. Prepared as part of Invasive Species Ireland, pp 16 Marson D, Cudmore B, Drake DAR et al. (2009a) Summary of a survey of aquarium owners in Canada. Canadian Manuscript Report of Fisheries and Aquatic Sciences 2905, Fisheries and Oceans Canada, Burlington, 20 p Marson D, Cudmore B, Drake DAR et al. (2009b) Summary of a survey of water garden owners in Canada. Canadian Manuscript Report of Fisheries and Aquatic Sciences 2906, Fisheries and Oceans Canada, Burlington, 23 p Martin GD, Coetzee JA (2011) Pet stores, aquarists and the internet trade as modes of introduction and spread of invasive macrophytes in South Africa. Water SA 37:371-380 Matthews J, Beringen R, Collas FPL et al. (2012) Knowledge document for risk analysis of the non-native Curly Waterweed (Lagarosiphon major) in the Netherlands. Reports Environmental Science 414, Radboud University, Nijmegen, pp. 43 Matthews J, Beringen R, Lamers LPM et al. (2013) Knowledge document for risk analysis of the non-native Fanwort (Cabomba caroliniana) in the Netherlands. Reports Environmental Science 443, Radboud University Nijmegen, pp. 60 Padilla DK, Williams SL (2004) Beyond ballast water: aquarium and ornamental trades as sources of invasive species in aquatic ecosystems. Frontiers in Ecology and the Environment 2:131- 119 138 Peters W, Meyer M, Anderson N (2006) Minnesota horticultural industry survey on invasive plants. Euphytica 148:75-86 Pot R (2002) Invasion and management of Floating Pennywort (Hydrocotyle ranunculoides L.f.) and some other species in the Netherlands. In: Dutartre A, Montel M et al. (eds) Proceedings of the 11th EWRS International Symposium on Aquatic Weeds. Moliets et Maa (France), pp. 435-438 Reichard SH, White P (2001) Horticulture as a pathway of invasive plant introductions in the United States. Bioscience 51:103-113 Rowe G, Frewer LJ (2004) Evaluating public-participation exercises: a research agenda. Science, Technology & Human Values 29:512-556 Rusterholz HP, Wirz D, Baur B (2012) Garden waste deposits as a source for non-native plants in mixed deciduous forests. Applied Vegetation Science 15:329-337 Strecker AL, Campbell PM, Olden JD (2011) The aquarium trade as an invasion pathway in the Pacific Northwest. Fisheries 36:74-85 Thum R, Mercer A, Wcisel D (2012) Loopholes in the regulation of invasive species: genetic identifications identify mislabeling of prohibited aquarium plants. Biological Invasions 14:929-937 Chapter 6

Van Kleef H, Van der Velde G, Leuven RSEW et al. (2008) Pumpkinseed sunfish (Lepomis gibbosus) invasions facilitated by introductions and nature management strongly reduce macroinvertebrate abundance in isolated water bodies. Biological Invasions 10:1481-1490 Van Valkenburg JLCH, Duistermaat H, Boer E (2013) Image-driven electronic identification keys for invasive plant species in the Netherlands. EPPO Bulletin 43:250-254. Verbrugge LNH, Van den Born RJG, Lenders HJR (2013) Exploring public perception of non- native species from a visions of nature perspective. Environmental Management 52:1562- 1573

120

Chapter 7

Synthesis

Laura Verbrugge Chapter 7

Introduction Globalization has changed species distributions worldwide. Some argue that these changes are inevitable in the ‘Anthropocene’ era and may in fact increase biodiversity in most places (Thomas 2013). However, the dominant view on biological invasions is that they have the potential to severely impact the environment and society which make it necessary to prevent new introductions whenever possible as well as to mitigate the impacts of harmful species (Simberloff 2011). Risk analysis plays an important role in prevention, in predicting and prioritizing impacts, and in control of biological invasions (Andersen et al. 2004). Risk analyses are comprised of three components, i.e. risk assessment, risk management and risk communication. All three components have a technical, objective dimension but also include perceptions, values, best practices and other normative aspects which complicate risk analyses considerably. The aim of this thesis was twofold. The first aim was to analyse the scientific, societal and policy considerations in risk analysis of biological invasions. The second aim was to evaluate how environmental science and social science may be combined to enhance the understanding of policy practices concerning invasive species management. In the following sections of this synthesis, I will first discuss the major conclusions of each chapter. The sub sections correspond with the five research questions that were presented in the first chapter of this thesis. Next, I will reflect on issues related to interdisciplinarity and the integration of social and natural sciences to enhance our understanding of managing biological invasions. Finally, I will provide an overview of the recommendations for further research and management.

General conclusions

Role of science in predicting and assessing impacts of biological invasions A combination of anthropogenic stressors played a role in the introduction and spread of aquatic non-native species in western European rivers. The construction of the Main- Danube canal in 1992 has facilitated the rapid spread of non-native species into the river Rhine (Leuven et al. 2009). Increased shipping activities accelerated the spread as ships served as transport vehicle for many species that hitched a ride. Recent estimates have shown that introductions of non-native species account for more than half of the 124 freshwater ecosystem impacts of inland shipping when compared to other commonly assessed environmental stressors, such as eutrophication, ecotoxicity, greenhouse gases and water consumption (Hanafiah et al. 2013). Finally, climate change and other human- induced stressors (e.g. pollution) induced changes in water temperature and salinity regimes in rivers. In turn, these abiotic changes influence the biotic diversity in riverine ecosystems (Rahel and Olden 2008). The aim of Chapter 2 was to study the influence of changes in water temperature and salinity on native and non-native mollusc species in the river Rhine. The results of this chapter are relevant in two ways. On the one hand, these data are useful for risk analysis of non-native molluscs, as they provide insights in environmental tolerances of non- native species and possible management options to mitigate their effects. On the other hand, they can also be used to study the role of science in assessing and communicating Synthesis impacts of non-native species. Such an analysis requires the integration of results from several chapters of this thesis (Chapters 2-4). This will be done separately in the following section, in which the possibilities for integrating social and natural sciences are discussed. The following paragraphs will wrap up the general conclusions from Chapter 2 in terms of its value for predicting and managing biological invasions of mollusc species. Two main conclusions from this chapter are that (1) non-native species can tolerate higher temperatures than native species, and (2) increasing river water temperatures have a much larger influence on mollusc species occurrence than changes in salinity levels. These findings indicate that a further increase in water temperature by global warming and thermal discharges will affect a higher percentage of native mollusc species than non- native ones. Other studies also identified temperature tolerance as an important species trait and similarly found that non-native species in aquatic ecosystems were less negatively affected by increases in water temperature than co-occurring native species (Bates et al. 2013; Sorte et al. 2013). Therefore, reducing thermal pollution may mitigate loss of native biodiversity and species replacements in the river Rhine. Other management interventions to protect native species may focus on creating suitable (cold water) refugia in restoration projects. The construction and application of species sensitivity distributions (SSD) proved to be useful approach in addressing the separate and combined effects of changing abiotic conditions on regional native and non-native species pools. As such, it may be very suitable for underpinning analyses on species-environment match. This approach can be applied to other types of ecosystems or taxa, as well as other types of abiotic stressors in river systems, such as pollution, discharge levels or oxygen availability (Collas et al. 2014; Elshout et al. 2013; Fedorenkova et al. 2013; Leuven et al. 2011). The advantage of the SSD approach is that it accounts for interactions of non-native species with abiotic stressors, providing more realistic estimations of impacts and feasible management options.

In summary, • Increasing water temperatures in the river Rhine, resulting from climate change and thermal pollution, will disproportionally affect native mollusc communities when compared to non-native mollusc communities. • Species sensitivity distributions are a useful approach to analyse the species-environment match and to assess the combined effects of multiple anthropogenic stressors on native and non-native species assemblages in river systems. 125 Evaluation of risk protocols and risk classifications According to Groves et al. (2001), the ideal (weed) risk assessment system would be “predictive, transparent, quantitative, rapid, generic, equitable, defensible, practicable and should minimize the occurrence of both ‘false positives’ (plants being evaluated as being weeds that would not become so) and ‘false negatives’ (plants assessed as having low weed risk that could become weeds)” (p. 236). Evaluations of existing risk protocols for biological invasions worldwide (for examples see Chapter 3) have shown that they vary in scope, scoring method and complexity (Leung et al. 2012; Verbrugge et al. 2010). A number of general findings can be distilled from the available evaluation studies. First, the majority of the protocols that were evaluated address impacts only. Thus, by assuming that either the species has already been introduced or is likely to do so, the likelihood of introduction and establishment (e.g. Chapter 7

species-environment match) are disregarded. Second, the scope of impacts assessments is either limited to ecological impacts only, or also includes damage to the economy or human health. Third, different scoring systems are used (i.e. a semi-quantitative approach which sums up scores or a purely qualitative classification key), with different number of questions or criteria to assess impacts, and different approaches in scoring uncertainty. Finally, the protocols used alternative ways for classification of species, including Black Lists, prioritization based on absolute scores, and the use cut-off thresholds to distinguish between high, medium and low risk. Risk classifications are used to compile lists containing potential invasive species. Considering the findings listed above, it is not surprising that the comparability of these lists between countries is limited (McGeoch et al. 2012). Chapter 3 of this thesis aimed to identify factors that may explain the variability in risk classifications by evaluating classifications of 25 species in seven European countries. The comparison showed that the classifications were dissimilar for 72 per cent of the tested species (Table 3.1). Moreover, for a number of species the differences were remarkably high, as they were classified as low risk in one country and identified as high risk species in others. As outlined above, these differences may be the result of differences in scoring, classification, and, possibly, weighting between the protocols. However, application of the same protocol in different countries also resulted in differences in risk classifications (Figure 3.1). This indicates that variations in assessment outcomes also stem from other reasons. Other factors influencing differences in classifications may be related to regional aspects, such as current distributions, habitat availability, and environmental matching, as well as variability in the number of experts, use of literature and expert judgement (e.g. visions and perceptions of experts). The lack of transparency on many of these aspects conceals a large part of the risk assessment process. This also obscures the values underlying certain choices, for example in the use of expert judgement (Hulme 2012). Invasiveness elsewhere (in surrounding or neighbouring areas) is a frequently used predictor of non-native species performance. The results from the comparison in Chapter 3, however, indicate that risk classifications from other (neighbouring) countries should be applied with caution and stress the importance of conducting risk assessments for the area at hand. This explicates a need for applied research on effects of non-native species in a regional context (as in Chapter 2). Furthermore, the cut-off thresholds of widely used protocols such as the Weed Risk Assessment (WRA) require validation before use in a specific region (Gordon et al. 2012; Koop et al. 2012). 126 The findings from Chapter 3 also suggest that data availability and the use of expert judgement may play an important role in performing risk assessments for non-native species consistently. In order to limit the variability in risk classifications due to external factors as much as possible, and in that way increase the consistency within and between countries, a number of recommendations were made. First, the risk assessment process should be formalized, by setting requirements for the number of assessors and the literature that is used in the assessment, and by using clear language to describe assessment criteria and their categories for differentiating between severities of impacts of invasive species. Furthermore, experts should be transparent in their choice of available literature and, in case of lack of data, in the use of anecdotal or expert knowledge. It is important that values and uncertainties in science are made explicit, as well as the implications for Synthesis the results, notably for policy makers to make informed decisions on prevention and management of invasive species (Ragas 2000). The interaction between science and policy in risk analysis of biological invasions is further discussed in Chapter 4. I conclude here by stating that cost-efficiency, robustness and transparency of risk assessments regarding non-native species are important to ensure the feasibility, quality and objectivity of risk management (see also Caffrey et al. 2014).

In summary, • Inconsistencies in classifications of risk when compared between countries result from differences in (1) risk assessment protocols, (2) biogeographical factors (e.g. species-environment match) and (3) data availability and expert judgement. These inconsistencies emphasize cautious use of existing risk classifications from other countries and calls in favour of performing risk assessments in a regional context. • The qualitative nature of risk protocols allows for processes of framing in (ecological) impact assessments or uncertainty assessments. Formalization of the risk assessment procedure in which the use of literature and expert judgement is made explicit will increase the transparency in the risk assessment process.

Implications of the use of value-laden metaphors for effective risk management Risk assessment outcomes form the basis for management decisions on biological invasions. Chapter 4 showed that ambiguous and value-laden terms in the vocabulary of invasion science have found their way into the policy domain. Furthermore, this chapter discussed the implications of the use of (strong) metaphors for effective risk management of invasive species. It concludes that current terminology and use of metaphors reflect different narratives about biological invasions and that these narratives, in turn, represent different perceptions on invasive species and their management. The challenge for scientists and policy makers lies in recognizing and valuing these different perceptions of non-native species, including their own. I refer to this process of acknowledgment in Chapter 4 as ‘responsible metaphor management’. Invasive species policies have two important pillars, namely the distinction between native and non-native species, and the distinction between invasive and non-invasive species (i.e. the assessment of harm). The fact that these terms are increasingly criticized calls for an evaluation of the meaning and importance of these terms in the policy domain, and, more importantly, how and by which narratives the use of these terms is legitimized. In Chapter 4, three main reasons for using these conceptual terms are identified. From a management perspective, the divide between native and non-native species is useful 127 as the latter are more likely to cause harm. Naturally, to distinguish between harmful and harmless species is helpful in allocating resources in a sensible way. However, it may also stem from a feeling of responsibility, as we (humans) are also the cause for the introduction of non-native species. Finally, the focus of decision makers lies on the most visible, harmful species. This is understandable given their demonstrated impacts, but also debatable, as preventive measures are more cost-effective (Finnoff et al. 2007; Leung et al. 2002). The strong focus on this particular ‘policy narrative’ has drawbacks as well. It lacks the acknowledgment of other narratives that may exist and represent other perceptions of non-native and invasive species. Even within policy many frames coexist alongside the dominant biodiversity and conservation frame, such as that of human security, global Chapter 7

governance and trade (Stoett 2010). The lack of awareness of other perceptions of biological invasions is problematic in two ways. First, cultural differences exacerbate difficulties in creating uniform policies or legislation. For example, European standardisation of risk assessment protocols will contribute to better comparable and transparent risk assessments of non-native species (Caffrey et al. 2014; Hulme et al. 2009). However, this first requires the acknowledgment of the existence of different values, perceptions and narratives that influence perceptions of biological invasions. This is the first step that has to be made in forming a consensus or common ground on which new foundations can be built. Second, narratives differ for groups or individuals, depending on their professional background, experience and knowledge on biological invasions. Two other dominant narratives are those of scientists and the public. The assessment and acknowledgment of public values is necessary to let the public fully participate (i.e. to make policies democratic). This was further explored in Chapter 5 on lay public perceptions. The narratives present in the scientific domain play an important role in ecological impact assessment of non-native species. Chapter 4 argues that scientists should be aware of the distinction between methodological and motivational subjectivity in assessments of harm. The underlying reasons for performing research are often motivational (i.e. to differentiate between native and non-native species and to derive management options for invasive species or to protect native species). The research questions or aims, however, should be formulated in a methodological way (i.e. to analyse the effects of changes in environmental conditions on the species pool in the river Rhine). Please note that I use the example of my own study that is presented in Chapter 2. The distinction between motivational and methodological approaches is that the former are primarily based on values. In practice it may be difficult to distinguish between ecological facts and statements that originate from value judgements (Sarewitz 2004). Even though words are used to describe facts, they may also obscure, and meanings may get lost in translation. As we saw in Chapter 3, most risk assessments are based on qualitative data that are then transformed into numerical scores. This issue of translating verbal into numerical expressions remains problematic, especially in scoring uncertainty (Theil 2002). There is no immediate solution to these kinds of problems. The recommendations in Chapter 3 and 4 that advocate for more transparency, self-reflection and awareness may aid the transfer of more objective knowledge from science to policy and vice versa.

128 In summary, • Metaphors used to describe biological invasions have been adopted in the policy domain. The concepts of nativeness and invasiveness play an important role in risk analysis. Acknowledgment of the values and assumptions underlying the interpretations of conceptual terms such as ‘non- native’ and ‘invasive’ is important. • The use of metaphors may have positive as well as negative consequences. They may serve as useful boundary objects that facilitate the interchange of knowledge. However, divergent interpretations of basic terms may also result in limited comparability, misunderstandings or conflicts. The challenge for scientists and policy makers lies in recognizing and valuing these different perceptions of non-native species, including their own. Synthesis

Lay public perceptions of biological invasions Risk analysis of non-native species not only calls for ecological expertise but for insight into risk perceptions as well. Chapter 5 explored the relations between the lay public’s visions of nature, their knowledge about non-native species and their perceptions of non-native species and invasive species management in the Netherlands (Figure 5.1). This chapter concludes that lay public perceptions of non-native species connect with more deep-lying and profound visions of nature. These visions of nature are often firmly anchored and difficult to change and, thus, create challenges for policy makers and managers. Early stakeholder involvement and timely risk communication are effective strategies to incorporate public values into policy and to reduce conflicts. The findings in this study highlight the importance of perceptions of ‘naturalness’ and ‘balance in nature’ in perceptions of risk of biological invasions. In congruence with other studies we found that, compared to respondents who perceive balance in nature as a threshold system, the view of nature as unstable resulted in higher perceived risks, more support for control and more engagement (Fischer and Van der Wal 2007; McDaniels et al. 1997). Moreover, written comments and oral answers of respondents reported in both Chapter 5 and 6 supported the view that the concept of balance in nature matters to the public and influences their perceptions of risks posed by non-native species. Potential differences between perceptions of the lay public and scientists provide an interesting topic for further study. Scientists may hold a more dynamic view of nature, or even support the conceptual image of ‘novel ecosystems’ (Hobbs et al. 2009). Moreover, Chapter 5 explores the relationship between the level of knowledge about non-native species and perceptions of non-native species. General knowledge on the definition and species examples, as well as knowledge of actual control programmes were positively correlated with level of engagement of respondents. Membership of nature protection organisations may play a role in knowledge dissemination as this variable was linked to both level of knowledge and level of engagement. The reported level of knowledge of the respondents who participated in the survey was quite high. However, Chapter 5 and 6 highlighted some distinct knowledge gaps related to the role of people in the introduction and spread of non-native species and the severity of socioeconomic impacts (compared to the general awareness of ecological impacts). Finally, Chapter 5 also addressed the predictive value of non-native species perceptions in support for invasive species management. Perceived risks of non-native species, views on control and engagement were identified as predictors of public support for the examples 129 of invasive species management included in the survey. However, pluriformity of public response relating to species appeal has to be taken into account in invasive species management in order to do justice to divergent perceptions present in society (Figures 5.2 and 5.3). In other words, ‘the public’ does not exist. The crow case presented in Chapter 1 (Box 1) provides an excellent example of this. This result supports the view that non- market values relevant for policy decisions should not only refer to general benefits for society, such as provision of recreation opportunities and habitat conservation values. They must also include other public values that inform perceptions of non-native species and their impacts, such visions of nature and aesthetic values, as well as the appreciation of landscapes and animal welfare (Dandy et al. 2012; Webb and Raffaelli 2008). Especially Chapter 7

the latter is becoming increasingly relevant in the western world where animal rights are increasingly recognized and individual cases may incite strong responses from society.

In summary, • Lay public perceptions connect with more deeply anchored visions of nature. Relevant nature values in perceiving risks of non-native species include views on naturalness and balance in nature. • Eradication measures for birds and mammals are less supported by the lay public when compared to other species groups, such as plants, insects and aquatic species. This implies that aesthetics and other public values may play a significant role in public support for invasive species management.

Public outreach, public awareness and risk prevention At present, no uniform policies for preventing introductions of invasive plants and animals are in place. Policy instruments include legal bans, voluntary codes of conduct and risk communication (Gren 2008). Public outreach campaigns may be aimed at informing the public (or other stakeholder groups) about risks of non-native species, changing their behaviour to prevent new introductions or to educate and encourage them to report new sightings. However, the majority of these campaigns are far from evidence-based and say little to inform policymakers about their effectiveness, for example in the case of the most prominent invasive mollusc species, the zebra mussel Dreissena polymorpha (Strayer 2008). Chapter 6 presents the results from an evaluation study on the effectiveness of measures issued in the code of conduct for aquatic plants in the Netherlands. The chapter concludes that voluntary measures can be effective policy instruments for risk prevention if certain conditions are met. First, all relevant stakeholders have to be involved. Collaboration between scientists, policy makers and public organizations is needed to formulate mutual goals, encourage mutual learning and construct knowledge on public engagement and risk communication. Second, communication was identified as an essential element of voluntary instruments. Communication between the partners in the code of conduct is needed to provide a platform for dialogue and keep each partner informed and committed to the cause. Public outreach campaigns are necessary to raise awareness among the public, nursery professionals and commercial sector. Chapter 6 also addressed the role of the public in introducing non-native species to the natural surroundings. Aquarists and, especially, water gardeners have been identified as 130 key players in facilitating new introductions (Figure 6.1), emphasising the need for risk prevention in this particular context. Moreover, qualitative data provided information on personal motivations regarding their behaviour and perceptions of risk. These results revealed two conflicting views of the lay public. Their motivations for intentional release of plants often revealed a lack of knowledge and awareness about the possible consequences of their actions. Some respondents considered releasing plants into the environment as positive for nature. Thus, even though they had considerable knowledge about invasive species and their potential impacts, they undervalued their own role in new species introductions. Other results from this study support this view. In their definition of non-native species respondents often failed to mention the role of humans in the introduction and spread. Moreover, they explained their lack of personal commitment or engagement in problems caused by invasive species as something that was beyond their reach of influence (unpublished results). Thus, in order to prevent new introductions Synthesis of animals and plants by citizens, they first have to be made aware of the possible consequences resulting from their own actions (Prinbeck et al. 2011). When asking visitors of pet stores and garden centres about the risks posed by potentially invasive plants, the results showed that they mainly perceive ecological risks and, in congruence with Chapter 5, relate these strongly to the disturbance of balance in nature or to a sense of place or belonging. Focusing information campaigns on our role in spread and introduction of non-native species and on socioeconomic effects may improve their effectiveness in increasing awareness and in gaining support for preventive and eradication measures. Communication strategies should include other relevant target groups, such as pet owners in general (Perry and Farmer 2011), anglers and the bait industry (Kilian et al. 2012), gardeners and gardening professionals (Heywood 2011; Qvenild et al. 2014) and the general public (Crall et al. 2010). The media is an important information source for the public (Boykoff 2009). Content analyses of (written) media sources, such as newspapers and the internet, should provide more insights in how the media frame the issue of non-native species. Specific elements such as metaphors, arguments, problem setting and emphasis need to be identified to find out how frames in popular media may differ from science, policy and other public domains. In summary, • Requirements for effective voluntary policy instruments for prevention of biological invasions, such as codes of conduct, include the involvement of all relevant stakeholders, the setting of mutual goals and sufficient means for (internal and external) communication. • Aquarists and, especially, water gardeners were identified as key players in facilitating new introductions of non-native plants. Their motives for intentional release of plants often revealed a lack of knowledge and awareness about the role of humans in the introduction of non-native species. This disconnect has to be resolved in order to fully engage public in preventive measures for introduction and spread of non-native species.

Methodological reflections on interdisciplinary research approaches During the course of this PhD study, the focus shifted from risk assessment of non- native species to studying the perceptions of and discourses on biological invasions. This also represents a shift from a natural science perspective to a social science perspective. 131 Having reached this point, the present section focusses on the integration of both perspectives. This is done, first of all, by evaluating the use and function of metaphors in one of the ‘science chapters’ (Chapter 2). In addition, I will use the findings presented in this thesis to reflect on the Crow case that was introduced in the Chapter 1.

Use and function of metaphors in risk analysis of non-native species Chapter 2 plays a double role in this thesis as it can be read as a straightforward science paper that aims to assess the influence of changing abiotic stressors on native and non- native mollusc assemblages in the river Rhine. However, the results from the other chapters of this thesis, especially Chapters 3 and 4, provide more angles to reflect on this paper, namely in terms of the use of metaphors, problem framing and subjectivity, the role of humans in biological invasions and the acknowledgment of uncertainties. The first Chapter 7

point of interest is the use of metaphors. In Chapter 2, the dominant terms are native and non-native and this distinction forms the basis for the analyses presented in the paper. However, there is also awareness of the uncertainties in the taxonomic status of particular species, and that, in some cases, a species can be considered native in some regions and non-native in other regions (Table 2.1). Species for which the biogeographical status is unknown are called cryptogenic species (Carlton 1996) and, in fact, many examples of such cases exist, for example in marine environments (Haydar 2011). The use of value-laden terms such as invasive species in Chapter 2 is sparse but occasionally a reference is made to bioinvaders. These terms are commonly used in scientific publications suggesting that they do not incite strong reactions from scientists and are interpreted in a more or less neutral, biological way (Richardson et al. 2010). However, cautious use is recommended as framing of the issue may also incite a different set of responses, thus giving rise to public controversy (Clergeau and Nuñez 2006; Gobster 2005). In Chapter 2, biological invasions are framed in the context of climate change (e.g. changing environmental conditions) and species richness. The behaviour and spread of invasive molluscs in their introduced range are presented as the cause for species replacements and a decrease in native species richness. This fits in the dominant discourse of biodiversity and conservation (Stoett 2010). However, in the explanation of differences in tolerance levels between native and non-native species, this view is broadened and the role of humans becomes apparent in two ways. Firstly, in the modes of introduction of non-native species through ballast water and increased connectivity of waterways; and secondly in the changing of environmental conditions that result from climate change and (thermal) pollution. The latter then provides a starting point for mitigation of impacts on native biodiversity. The final point of reflection is related to uncertainties and how these may limit the reliability and applicability of the results. The limitations of the study are discussed in the final section of Chapter 2 and include for example a lack of data on upper thermal tolerance levels of some native mollusc species. Other uncertainties relate to novel approaches in using field data to assess the effects of combined abiotic stressors in an ecosystem. As a result of these gaps in knowledge, it is stated that the results can only be interpreted and evaluated qualitatively and thus implying cautious use of the results for actual management interventions. 132 Concluding remarks Interventions in the natural environment often incite strong public responses. Public involvement in environmental sciences, and also in biological invasions, often stems from practical advantages, such as support for management interventions or reducing stakeholder conflicts. However, the results from this thesis show that social science contributions are needed to provide more than just end-of-pipe solutions for management of biological invasions. In risk assessment, integrated solutions are needed to remedy inconsistencies in the impact assessment of invasive species and challenge the continued reliance on expert judgment which allows for processes of framing. Concerning risk management, the incorporation of public values in decision making will improve the strategic awareness of public concerns and increase sensitivity towards the coexistence of Synthesis

Box 2 The crow case revisited Bird species represent an interesting case study for public perception of non-native species and their impacts. First, the biogeographical status of bird species is more complex since some are migratory species that live on more than one continent. The main policy argument for the classification of the house crow Corvus splendens as non-native species relates to the shipping vector that facilitated the introduction of this species (Box 1). In this respect, the crow case can be compared to recent examples of accidental introductions of other bird species into the Netherlands via shipping (i.e. the snowy owl Bubo scandiacus and Iago sparrow Passer iagoensis). These birds have had considerable media coverage in Dutch newspapers and received quite a lot of attention from the bird watching community, who perceived them as rare and ‘exotic’ and, even though they are not established, as an addition to Dutch biodiversity. The risk assessment performed for the house crow has labelled this species as invasive in the policy domain. The application of other risk assessment methodologies, however, may result in risk classifications ranging from not invasive to high risk (Chapter 3; Verbrugge et al. 2010). Moreover, in the public domain other values play a role, such as rarity, animal welfare and appreciation of the intelligence or appearance of a species (Janssen 2013). Chapter 4 showed that recognition of both the limitations of risk assessment procedures and the existence of different risk perceptions within society is needed for effective risk management. In this respect, the crow case has been a learning experience for invasive species management in the Netherlands. The second point of interest is the relation between species appeal and public support for management of invasive species. The results from Chapter 5 suggest that measures to control or eradicate mammals and birds do not receive much public support. The introduction of the house crow in the Netherlands has resemblances with the introduction of the American grey squirrel Sciurus carolinensis in Italy. In both cases, it was the first established population in continental Europe and both species are appealing to the public. Moreover, the eradication programmes that were set up failed due to legal issues and public opposition by animal welfare groups and, in the crow case, also by bird watchers. In each case the species were framed both as non-native species with harmful impacts and as object of protection and concern. The case of the squirrel has taught us that fierce societal opposition that make effective use of popular media, in combination with a lack of awareness of the general public may result in complete failure of eradication projects (Genovesi and Bertolino 2001). However, recent evaluations of the capture of non-native squirrels in the southern provinces of the Netherlands have shown that recognition of public values relating to animal welfare, early involvement of the public and targeted communication about the negative impacts may result in effective invasive species control (Dijkstra 2013). Finally, eradication programmes, even if they are successful, may prove to be insufficient in case of repeated introductions (e.g. escapes or releases). This emphasizes the need for a combined approach in risk prevention, focussing on mitigating impacts as well as on preventing new introductions. Chapter 6 has highlighted the significance of intentional releases or escapes in the introduction of invasive plants and evaluated the effectiveness of risk prevention policies. Similarly, trading bans for mammals and bird species held as pets, in combination with informing pet owners about the potential risks of (un)intentional release will limit the number of introductions via this pathway. 133

House crow (Corvus splendens). Photo: Luuk Punt Chapter 7

different narratives on biological invasions. Risk communication relies on the sufficient availability and reliability of data on potential target groups, public perceptions and the effectiveness of communication mechanisms. Finally, risk analysis in general will greatly benefit from research on human behaviour or activities that ultimately drives the introduction, establishment and spread of invasive species.

Recommendations

Recommendations for further research • Risk assessment of non-native species will benefit from research efforts to identify species traits and other predictors for invasiveness. The development of quantitative assessment criteria may aid in reducing potential bias resulting from expert judgments when performing risk assessments. • Further studies on the introduction, establishment and impacts of non-native species should be performed in a societal context, e.g. related to human behaviour, climate change or global trade, as to provide valuable information for risk management. • More insights are needed in identifying key factors that influence public perception of non-native species and public support for invasive species management. This will aid in developing more strategic communication plans aimed at informing and engaging stakeholders and the general public in risk prevention. • Science based evaluations of public outreach campaigns are necessary for developing and improving the effectiveness of risk communication. • Studies on the use of metaphorical language in media reporting on non-native species (i.e. content analyses) and the effects of the use of metaphors on public perceptions are needed to enhance our understanding of public debates on biological invasions.

Policy recommendations • Risk assessments procedures for non-native species should be harmonized, formalized and should become more transparent in order to increase the consistency and comparability of risk classifications within and between countries. • Early stakeholder participation and risk communication are effective strategies to 134 incorporate public values into policies for invasive species management. In addition to reducing conflicts, benefits of this approach include a broader framework for problem setting and knowledge transfer, for example when developing voluntary policy instruments or setting up citizen science projects. • Public engagement at all levels of society is of major importance for effective risk management of biological invasions. This includes the general public as well as industries and the commercial sector. Ignorance of either problems caused by invasive species or the role these stakeholders play in the introduction and spread of non-native species impedes effective management. • Risk communication strategies should focus on the role of humans in the spread and introduction of non-native species and on the socioeconomic effects of biological Synthesis

invasions. More targeted information campaigns (i.e. providing region specific and appropriate information for specific target groups) will improve the effectiveness of communication strategies in increasing awareness and in gaining support for preventive, eradication and control measures.

References Andersen MC, Adams H, Hope B et al. (2004) Risk analysis for invasive species: general framework and research needs. Risk Analysis 24:893-900 Bates AE, McKelvie CM, Sorte CJB et al. (2013) Geographical range, heat tolerance and invasion success in aquatic species. Proceedings of the Royal Society B: Biological Sciences 280:20131958 Boonman-Berson S, Turnhout E, van Tatenhove J (2014) Invasive species: the categorization of wildlife in science, policy, and wildlife management. Land Use Policy 38:204-212 Boykoff MT (2009) We speak for the trees: media reporting on the environment. Annual Review of Environment and Resources 34:431-457 Caffrey JM, Baars J.-R., Barbour JH et al. (2014) Tackling invasive alien species in Europe: the top 20 issues. Management of Biological Invasions 5:1-20 Clergeau P, Nuñez MA (2006) The language of fighting invasive species. Science 311:951 Collas FPL, Koopman KR, Hendriks AJ et al. (2014) Effects of desiccation on native and non- native molluscs in rivers. Freshwater Biology 59:41-55 Crall A, Newman G, Jarnevich C et al. (2010) Improving and integrating data on invasive species collected by citizen scientists. Biological Invasions 12:3419-3428 Dandy N, Ballantyne S, Moseley D et al. (2012) Exploring beliefs behind support for and opposition to wildlife management methods: a qualitative study. European Journal of Wildlife Research 58:695-706 Dijkstra V (2013) Wegvangen Pallas’ eekhoorn verloopt voorspoedig. Kijk Op Exoten 4:10-11 (in Dutch) Elshout PMF, Pires LMD, Leuven RSEW et al. (2013) Low oxygen tolerance of different life stages of temperate freshwater fish species Journal of Fish Biology 83:190-206 Fedorenkova A, Vonk JA, Breure AM et al. (2013) Tolerance of native and non-native fish species to chemical stress: a case study for the river Rhine Aquatic Invasions 8:231-241 Finnoff D, Shogren JF, Leung B et al. (2007) Take a risk: preferring prevention over control of biological invaders. Ecological Economics 62:216-222 Fischer A, Van der Wal R (2007) Invasive plant suppresses charismatic seabird: the construction of attitudes towards biodiversity management options. Biological Conservation 135:256-267 135 Genovesi P, Bertolino S (2001) Human dimension aspects in invasive alien species issues: the case of the failure of the grey squirrel eradication project in Italy. In: McNeely JA (ed) The great reshuffling: human dimensions of invasive alien species. IUCN, Gland, Switzerland and Cambridge, UK, pp. 113-120 Gobster PH (2005) Invasive species as ecological threat: is restoration an alternative to fear- based resource management? Ecological Restoration 23:261-270 Gordon DR, Gantz CA, Jerde CL et al. (2012) Weed Risk Assessment for aquatic plants: modification of a New Zealand system for the United States. Plos One 7:e40031 Gren IM (2008) Economics of alien invasive species management: choices of targets and policies. Boreal Environment Research 13:17-32 Groves RH, Panetta FD, Virtue JG (2001) Weed risk assessment. CSIRO Publishing, Collingwood, Australia Chapter 7

Hanafiah MM, Leuven RSEW, Sommerwerk N et al. (2013) Including the introduction of exotic species in life cycle impact assessment: the case of inland shipping. Environmental Science & Technology 47:13934-13940 Haydar D (2012) What is natural? The scale of cryptogenesis in the North Atlantic Ocean. Diversity and Distributions 18:101-110 Heywood V (2011) The role of botanic gardens as resource and introduction centres in the face of global change. Biodiversity and Conservation 20:221-239 Hobbs RJ, Higgs E, Harris JA (2009) Novel ecosystems: implications for conservation and restoration. Trends in Ecology & Evolution 24:599-605 Hulme PE, Pysek P, Nentwig W et al. (2009) Will threat of biological invasions unite the European Union? Science 324:40-41 Hulme PE, Weser C (2011) Mixed messages from multiple information sources on invasive species: a case of too much of a good thing? Diversity and Distributions 17:1152-1160 Humair F, Edwards PJ, Siegrist M et al. (2014) Understanding misunderstandings in invasion science: why experts don’t agree on common concepts and risk assessments. NeoBiota 20:1- 30 Janssen C (2012) De huiskraai is een exoot, maar is dat erg? De Volkskrant dd. 10-01-2013 (in Dutch) Kilian J, Klauda R, Widman S et al. (2012) An assessment of a bait industry and angler behavior as a vector of invasive species. Biological Invasions 14:1469-1481 Koop A, Fowler L, Newton L et al. (2012) Development and validation of a weed screening tool for the United States. Biological Invasions 14:273-294 Kueffer C, Hirsch Hadorn G (2008) How to achieve effectiveness in problem-oriented landscape research: the example of research on biotic invasions. Living Reviews in Landscape Research 2, Online source: http://www.livingreviews.org/lrlr-2008-2 (Accessed February 25, 2014) Leung B, Lodge DM, Finnoff D et al. (2002) An ounce of prevention or a pound of cure: bioeconomic risk analysis of invasive species. Proceedings of the Royal Society of London Series B-Biological Sciences 269:2407-2413 Leung B, Roura-Pascual N, Bacher S et al. (2012) TEASIng apart alien species risk assessments: a framework for best practices. Ecology Letters 15:1475-1493 Leuven RSEW, Velde G, Baijens I et al. (2009) The river Rhine: a global highway for dispersal of aquatic invasive species. Biological Invasions 11:1989-2008 Leuven RSEW, Hendriks AJ, Huijbregts MAJ et al. (2011) Differences in sensitivity of native and exotic fish species to changes in river temperature. Current Zoology 57:852-862 McDaniels TL, Axelrod LJ, Cavanagh NS et al. (1997) Perception of ecological risk to water environments. Risk Analysis 17:341-352 136 McGeoch MA, Spear D, Kleynhans EJ et al. (2012) Uncertainty in invasive alien species listing. Ecological Applications 22:959-971 Perry G, Farmer M (2011) Reducing the risk of biological invasion by creating incentives for pet sellers and owners to do the right thing. Journal of Herpetology 45:134-141 Prinbeck G, Lach D, Chan S (2011) Exploring stakeholders' attitudes and beliefs regarding behaviors that prevent the spread of invasive species. Environmental Education Research 17:341-352 Qvenild M, Setten G, Skår M (2014) Politicising plants: dwelling and invasive alien species in domestic gardens in Norway. Norwegian Journal of Geography 68: 22-33 Ragas, AMJ (2000) Uncertainty in environmental quality standards. PhD thesis, Radboud University Nijmegen, The Netherlands Rahel FJ, Olden JD (2008) Assessing the effects of climate change on aquatic invasive species. Conservation Biology 22:521-533 Synthesis

Richardson DM, Pyšek P, Carlton JT (2010) A compendium of essential concepts and terminology in invasion ecology. In: Richardson DM (ed) Fifty years of invasion ecology. Wiley-Blackwell, Oxford, UK, pp. 409-420 Sarewitz D (2004) How science makes environmental controversies worse. Environmental Science & Policy 7:385-403 Simberloff D (2011) Non-natives: 141 scientists object. Nature 475:36-36 Sorte CJB, Ibáñez I, Blumenthal DM et al. (2013) Poised to prosper? A cross-system comparison of climate change effects on native and non-native species performance. Ecology Letters 16:261-270 Stoett P (2010) Framing bioinvasion: biodiversity, climate change, security, trade, and global governance. Global Governance 16:103-120 Strayer DL (2008) Twenty years of zebra mussels: lessons from the mollusk that made headlines. Frontiers in Ecology and the Environment 7:135-141 Theil M (2002) The role of translations of verbal into numerical probability expressions in risk management: a meta-analysis. Journal of Risk Research 5:177-186 Thomas CD (2013) The Anthropocene could raise biological diversity. Nature 502:7 Verbrugge LNH, Leuven RSEW, Van der Velde G (2010) Evaluation of international risk assessment protocols for exotic species. Reports Environmental Science no. 352. Department of Environmental Science, Radboud University Nijmegen, The Netherlands, 54 p Webb TJ, Raffaelli D (2008) Conversations in conservation: revealing and dealing with language differences in environmental conflicts. Journal of Applied Ecology 45:1198-1204

137

Appendices Appendices

Appendix 1 Translation of the postal questionnaire (Chapter 5).

strongly disagree / disagree Q1 Human and Nature relationships / neutral / agree / strongly agree Human beings have the right to alter nature radically When I am surrounded by nature I experience something greater than mankind People and nature are of equal value Humans are part of nature I would like to spend a week alone in forest Humans and nature deserve to be treated in the same way Because I can think I am more important than nature I would like a relationship with nature just like I have with my friends I can have a relationship with nature just like I have with my friends It would be wonderful to join wild geese on their journey Human beings have responsibility to conserve the natural environment Nature wants to grow, prosper and develop, just like humans I sometimes feel one with the universe Humans have more value than nature We have to ensure that we leave enough nature for future generations I often feel an intense connection with nature I have the obligation to protect nature Nature should not hamper economic development Natural sites are important even if not useful to us

strongly disagree / disagree / neutral / Q2 Images of nature agree / strongly agree Real nature only exists without human influence Real nature only exists if it is left to function independently Real nature only exists if it is completely wild

Q3 Did you know what a non-native species was before reading this definition? (yes, exactly / yes, for the most part / no, for the most part not / no, not at all) 140 (definition given was as follows: “a non-native species is a plant or animal which doesnot originate from a particular area (for example the Netherlands) but has been introduced by humans, intentionally or unintentionally)”. Q4 Can you name examples of non-native species present in the Netherlands? (y / n) If yes, which species? Appendices

Q5 Do you know about current management of invasive species in the Netherlands? (y / n) If yes, for which species? Q6 What description of the influence of non-native species on nature does most fityour own opinion? (1) Indifferent: nature is essentially indifferent to external influences and therefore the introduction of a non-native species will not influence nature either. (2) Thresholds: non-native species do affect nature but irreversible effects will only occur when certain thresholds are crossed. (3) Unstable: the effect of non-native species on the balance in nature is by definition severe and will prohibit it from returning to its initial state. (4) Stable: nature will return to its original state, independent of the influences of non-native species.

strongly disagree / disagree Q7 Non-native species / neutral / agree / strongly agree Non-native species pose a threat to biodiversity in the Netherlands Presence of non-native species makes a nature area less valuable Non-native species complement biodiversity in the Netherlands All established non-native species are harmful for nature Animals and plants that came to the Netherlands only because humans facilitated it, do not really belong here Non-native species that cause economic damage, have to be controlled A non-native species that causes harm to threatened animal or plant species has to be controlled Non-native species are hazardous because they can spread diseases that are harmful for humans Non-native species that spread quickly and compete with other species must always be controlled Foreign animal and plant species that came to the Netherlands without our help are a part of Dutch nature I worry about the increasing number of non-native species in the Netherlands Economic advantage is a good reason for introducing a non-native species I feel engaged in problems caused by non-native species Non-native species that pose a risk to human health have to be kept 141 out It does not matter if non-native species cause harm, they should always be allowed to stay Appendices

Q8 Examples of invasive species management accept / control / eradicate Ringnecked parakeet (reproduction control / catching / shooting / none) Common ragweed (removal / natural enemy / pesticides / none) Water pennywort (removal / natural enemy / pesticides / none) Pumpkinseed sunfish(catching / natural enemy, pesticides / none) Tiger mosquito (natural enemy / herbicides / pesticides / none) Citrus longhorned beetle (removal / natural enemy / pesticides / none) Grey squirrel (reproduction control / catching / shooting / none) Red swamp crayfish(catching / natural enemy, pesticides / none)

Q9 Demographics Gender (m / f), postal code, level of education (categorized as low or high) Membership nature protection organization (y / n) How often do you visit a nature area? (at least once a week / about twice a month / about once a month / a few times a year / less than once a year)

142 Appendices

Appendix 2 Tables 1-2 Results from the factor analyses performed in chapter 5, including factor loadings and level of adherences with standard deviation

Table 1 Factor analysis of the Human and Nature (HaN) statements, including factor loadings and level of adherences with standard deviation Factor Level of Standard HaN scale itemsa loading adherence deviation Participant Pc_1 I would like to spend a week alone in forest 0.769 -0.13 1.20 Pc_2 It would be wonderful to join wild geese on their journey 0.605 0.25 1.31 Pc_3 I often feel an intense connection with nature 0.543 0.95 0.86 Pc_4 I sometimes feel one with the universe 0.530 0.18 1.08 Pc_5 When I am surrounded by nature I experience something greater than 0.313 1.11 0.83 mankind Master M_1 Humans have more value than nature 0.752 -0.62 1.15 M_2 Because I can think I am more important than nature 0.719 -0.88 1.07 M_3 Nature should not hamper economic development 0.492 -0.65 1.13 M_4 We must especially protect animals that are useful for human beings 0.470 -0.46 1.18 M_5 Human beings have the right to alter nature radically 0.326 -0.83 1.02 St_1 Humans are part of nature -0.267 1.28 0.83 Partner Pa_1 I would like a relationship with nature just like I have with my friends 0.702 0.27 1.09 Pa_2 I can have a relationship with nature just like I have with my friends 0.667 0.36 1.01 Pa_3 Humans and nature deserve to be treated in the same way* 0.636 0.51 1.11 Pa_4 People and nature are of equal value 0.587 0.73 1.05 Pa_5 Nature wants to grow, prosper and develop, just like humans 0.360 0.92 0.99 Steward St_2 Human beings have responsibility to conserve the natural environment 0.694 1.51 0.77 St_3 I have the obligation to protect nature* 0.687 1.19 0.77 St_4 We have to ensure that we leave enough nature for future generations 0.529 1.67 0.64 St_5 Natural sites are important even if not useful to us 0.309 1.33 0.82 aItem scale ranged from -2 = ‘strongly disagree’ to 2 = ‘strongly agree’. *New statements as compared to the 2008 HaN scale from De Groot et al. (2011). The HaN scale did not provide enough statements for all categories; hence, we added two new ones in consultation with the developers of the scale. Note: Requirements for factor analysis were assured with the KMO statistic (0.789) and Bartlett’s test (χ2 = 1892, P < 0.001). Items with low factor loadings (≤ .350) were excluded from a factor. Abbreviations match classifications of the human-nature relationship. Pc: Participant, M: Master; Pa: Partner, St: Steward

143 Appendices

Table 2 Factor analysis of the statements on non-native species (NNS) perception, including factor loadings and level of adherences with standard deviation Factor Level of Standard NNS Scale itemsa loading adherence deviation Perceived risk RB_1 All established non-native species are harmful for nature 0.771 -0.74 0.91 NV_1 Presence of non-native species makes a nature area less valuable 0.651 -0.47 0.93 NV_2 Non-native species complement biodiversity in the Netherlands -0.534 0.05* 1.01 RB_2 Non-native species pose a threat to biodiversity in the Netherlands 0.468 0.28 1.04 RB_3 Non-native species are hazardous because they can spread diseases 0.417 0.29 1.03 that are harmful for humans NV_3 Animals and plants that came to the Netherlands only because 0.355 0.43 1.17 humans facilitated it, do not really belong here NV_4 Foreign animal and plant species that came to the Netherlands -0.330 0.49 1.00 without our help are a part of Dutch nature Control C_1 Non-native species that pose a risk to human health have to be kept 0.676 1.32 0.82 out C_2 Non-native species that cause economic damage, have to be 0.621 0.72 0.99 controlled C_3 A non-native species that causes harm to threatened animal or plant 0.565 1.24 0.76 species has to be controlled C_4 It does not matter if non-native species cause harm, they should -0.449 -1.22* 0.86 always be allowed to stay C_5 Non-native species that spread quickly and compete with other species 0.388 0.77 0.90 must always be controlled Engagement EC_1 I feel engaged in problems caused by non-native species 0.763 0.03 0.99 EC_2 I worry about the increasing number of non-native species in the 0.619 -0.14 0.98 Netherlands RB_4 Economic advantage is a good reason for introducing a non-native -0.233 -0.64 1.03 species aItem scale ranged from -2 = ‘strongly disagree’ to 2 = ‘strongly agree’. * scores for reversed phrased statement; recoded in calculating the total level of adherence. Note: Requirements for factor analysis were assured with the KMO statistic (0.823) and Bartlett’s test (χ2 = 1158, P < 0.001). Items with low factor loadings (≤ .350) were excluded from a factor. Note: One statement was excluded from the NNS scale before factor analysis (i.e. a non-native species that is harmful for all animal and plant species should be controlled) because of multiple interpretations by respondents (as was pointed out in written comments). Abbreviations indicate major themes. NV: Nature Values, RB: Risk and Benefits; C: Control, EC: Engagement and Concern.

144 Appendices

Appendix 3 Translation of survey for aquarists and water gardeners (Chapter 6). All questions were open- ended, except the statements (Q10-12). Questions 14 and 15 only in 2012 survey.

Q1. Do you own an aquarium or water garden? (aquarium / water garden / both) Q2. How often do you purchase a new plant? (less than once a year / once a year / a few times a year / each month) Q3. Where do you usually purchase aquatic plants? (garden centre / pet store / specialist store / other) Q4 .What are important plant characteristics when purchasing a new plant? (…) Q5. How do you dispose of plant waste? (…) If the answer is ‘release into the environment’ then also ask for their motivations. (why?) Q6. Some plant and animal species are called ‘non-native’. Do you know what non-native species are? (y / n) If yes, what description can you give? Q7. Could you name some examples of non-native species (either plants or animals)? (y / n) If yes, which examples? Give definition – reach consensus Q8. Did you realise that some plants that are sold in garden centres and pet stores are non-native species the last time you made a purchase? (y / n) Q9. Do you have any ideas about possible impacts of non-native aquatic plants? (y / n) If yes, which impacts?

very much / much / neutral / not / not at all Q10. What if a native species would disappear as the result of the introduction of a non-native species. To what degree would you care about that? Q11. What if a non-native species would grow so fast that it would reduce the variation of species in an area. To what degree would you care about that? Q12. To what extent do you consider yourself to be personally engaged in the problems caused by invasive species?

Q13. When purchasing a plant, did you ever receive information about the origin of the plant and potential risks associated with it? (y / n) Q14. Have you ever heard about the campaign ‘Geen exoot in de sloot’? (y / n) 145 Q15. Have you ever seen these warning logo’s on plant labels? (examples are shown) (y / n) Demographics Date of birth, gender (m / f), postal code, level of education Appendices

Appendix 4 Translation of survey for retail professionals (Chapter 6).

Q1. Type of store where you work (garden centre / pet store / other) Q2. Job description (manager / permanent staff member / other) Q3. Is your store a member of a trade association (y / n) If yes, which trade association? Q4. Compared to our whole stock, our stock of aquatic plants for use in ponds is… (large / average / small / non-existent) Q5. Compared to our whole stock, our stock of aquatic plants for use in aquaria is… (large / average / small / non-existent) Q6. Does your store provide online sales of aquatic plants? (y / n) Q7. Did you know what a non-native species was before reading this definition? (yes, exactly / yes, for the most part / no, for the most part not / no, not at all) (definition given was as follows: “a non-native species is a plant or animal which doesnot originate from a particular area (for example the Netherlands) but has been introduced by humans, intentionally or unintentionally”).

Q8. Non-native species strongly disagree / disagree / neutral / agree / strongly agree Non-native species pose a threat to biodiversity in the Netherlands Presence of non-native species makes a nature area less valuable Non-native species complement biodiversity in the Netherlands Animals and plants that came to the Netherlands only because humans facilitated it, do not really belong here Non-native species that spread quickly and compete with other species must always be controlled

Q9. Do you have an idea about the effects that invasive aquatic plants may have? (y / n) If yes, which effects?

Q10. Engagement How would you describe your personal level of interest in the high interest / moderate interest topic of invasive aquatic plants? / neutral / little interest / no interest How important is the topic of invasive aquatic plants in very important / important / 146 operational store management? neutral / little important / not important Appendices

Q11. Corporate responsibility strongly disagree / disagree / neutral / agree / strongly agree In our store we do not feel engaged in problems caused by invasive aquatic plants The topic invasive aquatic plants fits well with corporate social responsibility issues As a selling point, our store has an important role in informing the costumer about invasive aquatic plants Informing the costumer about aquatic invasive plants is not our duty

Q12. Do you consider the possible invasiveness of a plant when purchasing new stock? (yes / no/ don’t know) Q13. How would you judge your own knowledge of the code of conduct? (sufficient, largely sufficient, largely insufficient, insufficient) If (largely) sufficient, please answer the following statements:

Q14. Compliance strongly disagree / disagree / neutral / agree / strongly agree Our store fully complies with the agreements in the code of conduct Our store fully supports the agreements in the code of conduct In the beginning we had difficulty with (some) of the agreements In our store, we still have difficulty with (some) of the agreements

Q15. Are your employees familiar with the 13 species that are on the lists in the code of conduct? (completely / largely familiar / largely unfamiliar / unfamiliar) Q16. Are your employees familiar with the warning messages on labels? (yes / no / don’t know) Q17. Do you inform your costumers about the possible effects of invasive aquatic plants? (y / n) If yes, how? (brochures and posters on display in stores / website / newsletter / magazine /oral advice) Q18. In your opinion, what improvements could be made in communicating about the code of conduct?

147

Summary Summary

Non-native species, also referred to as neobiota, alien, foreign, exotic, introduced or non-indigenous species, are generally described as species introduced in areas outside their natural geographical range and whose presence is intentionally or unintentionally facilitated by humans. Biological invasions have been identified as a significant ecological and societal threat. Management of potentially invasive non-native species is costly and has triggered policy makers to develop risk analysis based policies to prioritize and mitigate the impacts of invasive species. Risk analyses are comprised of three components, i.e. risk assessment, risk management and risk communication. All three components have a technical, objective dimension but also include perceptions, values, best practices and other normative aspects which complicate risk analyses considerably. The central aim of this thesis is to analyse the scientific, societal and policy considerations in the risk analysis of biological invasions. Moreover, it aims to evaluate how environmental science and social science may be combined to enhance the understanding of policy design and implementation concerning invasive species management (Chapter 1). Risk assessment of biological invasions requires input on the likelihood of introduction and establishment of a species, together with information on the ability of the species to spread and interact with their surroundings, potentially resulting in ecological or socioeconomic impacts. Chapter 2 comprises a case study on the effects of changing abiotic conditions (resulting from climate change and water pollution) on the occurrence of freshwater mussels and snails in the river Rhine. In this chapter, a novel approach is used to assess the combined effects of changing temperature and salinity on native and non-native mollusc communities. Species sensitivity distributions based on field data revealed that non-native species were able to tolerate higher temperatures compared to native species. In addition, retrospective analyses showed that the effects of increasing temperatures were more pronounced than those of changes in the salinity of the river Rhine. These findings suggest that the reduction of thermal pressure on river ecosystems is an effective strategy for the creation of more optimal conditions for native species. In spite of its high value for invasive species management, no uniform policy exists for the risk assessment of non-native species. As a result, many different methodologies or protocols are used by countries that aim to prioritise and reduce the risks of biological invasions. A comparison of risk classifications for 25 aquatic species in six European countries showed that these were inconsistent for 72 per cent of the species (Chapter 3). Several factors may explain these findings, i.e. differences in the thoroughness and scope of protocols, different species-environment matches in various biogeographical regions, data availability and use of expert judgement. The qualitative nature of risk protocols encourages processes of framing in (ecological) impact assessments or uncertainty assessments (Chapters 3 and 4). Therefore, it is recommended that risk assessments procedures for non-native species should be harmonized and formalized, and should become more transparent in order to increase the consistency and facilitate the comparison of risk classifications within and between countries. Risk classifications form the basis for management decisions on biological invasions. As such, ambiguous, value-laden and contested terms in the vocabulary of invasion biology, such as ‘non-native’ and ‘invasive’ have spilled over to the policy domain (Chapter 4). Metaphors may serve as useful boundary objects to facilitate the interchange of knowledge

150 Summary between different stakeholder groups. However, divergent interpretations of terms may also result in limited comparability, misunderstandings or conflict. The challenge for scientists and policy makers lies in recognizing and valuing these different perceptions of non-native species, including their own. Moreover, the diversity in public response is often related to the public ‘appeal’ of particular species and has to be taken into account in invasive species management (Chapter 5). Survey and interview techniques were used to explore the role and perceptions of public stakeholders (Chapters 5 and 6). A survey was held in the Netherlands in order to uncover perceptions of non-native species and associated risks present in the public domain. In addition, the survey addressed possible relationships between the perceptions of lay people and their values, and meanings attributed to nature (i.e. their visions of nature). The findings presented in Chapter 5 show that lay people’s perceptions of non-native species connect with more deeply anchored visions of nature. Relevant nature values in lay people’s perception of non-native species’ impacts include views on naturalness and balance in nature. However, considerations of respect for nature in combination with a lack of awareness about the role of humans in the introduction of non-native species may result in their deliberate introduction to the environment by the public (Chapter 6). This disconnect has to be resolved in order to fully engage the public in the design of measures aimed at preventing the introduction and spread of non-native species. Policy instruments aimed at preventing new introductions of non-native species include legal bans, voluntary codes of conduct and risk communication. Chapter 6 features an evaluation of the effectiveness of a voluntary code of conduct in limiting the sale of potentially harmful aquarium and pond plants and increasing public awareness. Of the four measures evaluated in this study, the compliance with restricted sale of species was found to be most effective. For the other measures (including public outreach campaigns and labelling of species) the results are less univocal and stress the need for long term evaluation studies. Moreover, for voluntary policy instruments such as codes of conduct to be effective, it is important to include all relevant stakeholders during development, to agree on a shared vision and goal, and to establish sufficient means for internal and external communication (Chapter 6). Chapter 7 discusses the major conclusions of each chapter and reflects on ways to integrate social and environmental science perspectives to enhance our understanding of the management of biological invasions. During the course of this PhD study, the focus shifted from risk assessment of non-native species to studying the perceptions of and discourses on biological invasions. This represents a shift from a natural science perspective to a social science perspective. Chapter 2 plays a double role in this thesis as it can be read as a straightforward science paper but also in terms of the use of metaphors in describing and framing the research results. In general, public involvement in environmental sciences often stems from practical advantages, such as support for management interventions or reducing stakeholder conflicts. The results from this thesis, however, show that social science contributions are needed to provide more than just end-of-pipe solutions for the management biological invasions. In risk assessment, integrated solutions are needed to remedy inconsistencies in the impact assessment of invasive species and challenge the continued reliance on expert judgment which allows

151 Summary

for processes of framing. Concerning risk management, the incorporation of public values in decision making will increase the awareness of public concerns and can be strategically employed to improve (preventive) measures in invasive species management. Risk communication relies on the sufficient availability and reliability of data on potential target groups and the effectiveness of communication mechanisms. Finally, risk analysis in general will greatly benefit from research on human behaviour or activities that ultimately drive the introduction, establishment and spread of invasive species. This chapter concludes with recommendations for further research and policy making.

152

Samenvatting Samenvatting

Uitheemse planten- en diersoorten, ook wel exoten genoemd, zijn planten of dieren die oorspronkelijk niet in een gebied voorkomen maar daar door toedoen van menselijk handelen terecht zijn gekomen. De introductie van exoten kan zowel bewust als onbewust plaatsvinden. We spreken van een invasieve exoot als de geïntroduceerde soort zich snel in het nieuwe gebied verspreid en een bedreiging vormt voor de natuur, economie of volksgezondheid. Voorbeelden van invasieve exoten zijn woekerende uitheemse waterplanten die watergangen verstoppen en inheemse soorten verdringen, of insecten die infectieziektes kunnen overdragen die gevaarlijk zijn voor de mens. Uit de praktijk blijkt dat de bestrijding van invasieve exoten grote (financiële) inspanningen vergt. De ontwikkeling van risicobeoordelingsmethodieken stelt beleidsmakers in staat om de schadelijke gevolgen van uitheemse planten- en diersoorten in kaart te brengen. Aan de hand van een prioritering kunnen vervolgens de schaarse middelen voor exotenbeheer zo efficiënt mogelijk worden ingezet. Het beheer van invasieve exoten is een complex vraagstuk. De effectiviteit van beheermaatregelen, zoals bijvoorbeeld vroegtijdige signalering, preventie- en bestrijdingsmaatregelen, wordt mede bepaald door maatschappelijk draagvlak en publieke participatie. Adequaat beheer is dus niet alleen een kwestie van biologische kennis, maar vereist ook sociaalwetenschappelijke inzichten op het gebied van publieke percepties, risicocommunicatie en taalgebruik. Dit proefschrift heeft daarom een sterk interdisciplinair karakter en tracht de sterke punten van verschillende disciplines (zoals biologie, milieukunde, sociale wetenschappen, filosofie en wetenschapscommunicatie) te verbinden. Hoofdstuk 1 beschrijft het proces van risicoanalyse dat bestaat uit drie componenten: risicobeoordeling, risicomanagement en risicocommunicatie. Risicobeoordelingen zijn onderbouwd met wetenschappelijk kennis maar binnen risicoanalyse spelen ook normatieve aspecten een rol, zoals percepties, waarden en kennis van ‘best practices’. Dit maakt het uitvoeren van risicoanalyses een belangrijke, maar uiterst complexe taak. De hoofddoelstelling van dit proefschrift is om te onderzoeken welke wetenschappelijke, maatschappelijke en beleidsafwegingen gemaakt worden in risicoanalyses van exoten. Daarnaast is het doel om te verkennen hoe het combineren van natuurwetenschappelijke en sociaalwetenschappelijk kennis kan bijdragen aan het exotenbeleid en -beheer. Om de risico’s van exoten goed te kunnen beoordelen is informatie nodig over de verschillende stadia van een bioinvasie: de kans op introductie en vestiging van een soort, de verspreiding, en de interactie met de (natuurlijke) omgeving wat mogelijke ecologische en sociaaleconomische effecten tot gevolg heeft. Hoofdstuk 2 beschrijft een onderzoek naar de effecten van veranderende milieu-omstandigheden, als gevolg van klimaatverandering en (thermische) vervuiling, op de het voorkomen van mosselen en slakken in de Rijn. Aan de hand van literatuuronderzoek naar de maximale temperatuur- en zouttolerantie van inheemse en uitheemse mollusken zijn twee soortgevoeligheidsverdelingen opgesteld. Op basis hiervan is het mogelijk om het gezamenlijke effect van veranderingen in de temperatuur en het zoutgehalte van het water op deze twee groepen te berekenen voor een bepaalde periode. De uitkomsten van deze innovatieve methode laten zien dat uitheemse soorten beter bestand zijn tegen hogere temperaturen dan inheemse soorten, en dat de effecten van een stijging in temperatuur aanmerkelijk groter zijn dan die van de verandering in het zoutgehalte. De belangrijkste aanbeveling die volgt uit deze studie is dat het verminderen van warmte- en afvalwaterlozingen in riviersystemen een effectieve 156 Samenvatting strategie kan zijn voor het creëren van meer optimale milieuomstandigheden voor inheemse soorten. Het belang van betrouwbare risicobeoordelingen voor het exotenbeleid heeft ervoor gezorgd dat deze milieukundige methode in de afgelopen jaren internationaal een grote ontwikkeling heeft doorgemaakt. Echter, het ontbreken van een eenduidig beleid heeft geleid tot een wildgroei aan methoden om de risico’s van bioinvasies in kaart te brengen. Een vergelijking van de risicoclassificaties van 25 aquatische soorten in zes Europese landen laat zien dat deze in 72 procent van de gevallen niet met elkaar overeenkomen (Hoofdstuk 3). Er zijn verschillende factoren die hier een rol in spelen, zoals de verschillen tussen de gebruikte protocollen voor risicobeoordeling en de verschillen in klimaat tussen de landen waar de risicoanalyse is uitgevoerd. Daarnaast spelen databeschikbaarheid en -interpretatie door wetenschappers een rol. Risicobeoordelingsmethodieken hebben vaak een kwalitatieve onderbouwing, gebaseerd op de beschikbare wetenschappelijke literatuur, grijze literatuur en anekdotische (veld)kennis van de beoordelaars. Hierdoor kunnen onzekerheden en kennisgebrek een belangrijk rol gaan spelen in het proces, bijvoorbeeld bij het beoordelen van nadelige (ecologische) effecten. Op basis van de uitkomsten van Hoofstukken 3 en 4 kan worden gesteld dat het formaliseren, harmoniseren en het vergroten van de mate van transparantie van de procedures voor risicoanalyse van exoten positief zal bijdragen aan de consistentie van risicoclassificaties en de mogelijkheden voor vergelijkingen, bijvoorbeeld tussen verschillende landen. Risicoclassificaties vormen de basis voor beslissingen die gemaakt worden binnen het exotenbeleid en het beheer van invasieve exoten. Definities en begrippen die in de terminologie van de invasiebiologie (zoals dit wetenschappelijke vakgebied ook wel wordt genoemd) worden gebruikt, zoals ‘uitheems’ en ‘invasief ’, zijn momenteel onderwerp van discussie. Een belangrijk kritiekpunt is dat deze begrippen niet goed gedefinieerd kunnen worden (bijvoorbeeld ‘wanneer is een soort invasief?’ en ‘kan een uitheemse soort ook inburgeren?’). Een tweede kritiekpunt is dat de terminologie erg sturend is in hoe met exoten wordt omgegaan (Hoofdstuk 4). Hoewel het gebruik van metaforen een belangrijke functie heeft bij de uitwisseling van kennis tussen wetenschap en maatschappij, kunnen uiteenlopende interpretaties ook leiden tot onbegrip of conflicten. Bovendien maakt de veelvoud van definities voor bepalende begrippen binnen de invasiebiologie het moeilijk om informatie uit verschillende gebieden, bijvoorbeeld soortenlijsten, met elkaar te kunnen vergelijken. Een belangrijke uitdaging voor beleidsmakers en wetenschappers ligt ook op het gebied van het herkennen en waarderen van verschillende percepties van uitheemse soorten en hoe deze verschillen van hun eigen beeld. De diversiteit in percepties van exoten in het publieke domein is vaak gerelateerd aan de ‘aaibaarheid’ van soorten en dit is vervolgens weer van belang voor het draagvlak en de acceptatie van beheersmaatregelen gericht op specifieke invasieve soorten (Hoofdstuk 5). In de Hoofdstukken 5 en 6 staan de rol en perceptie van maatschappelijke actoren, zoals burgers en handelaren, centraal. Deze zijn in kaart gebracht met behulp van een ‘mixed methods approach’, een aanpak waarin zowel kwantitatieve als kwalitatieve methoden voor dataverzameling worden gebruikt. De publieke perceptie in Nederland is onderzocht door middel van het uitzetten van vragenlijsten onder een groep burgers (Hoofdstuk 5). In deze vragenlijst is gekeken naar de perceptie van exoten in het algemeen, de risico’s van invasieve exoten, en de mogelijke relaties tussen deze percepties en de visie van de 157 Samenvatting

respondenten op natuur. Uit deze studie blijkt dat de manier waarop burgers kijken naar exoten samenhangt met de wijze waarop ze natuur zien. Hierin spelen ideeën die men heeft over ‘natuurlijkheid’ en ‘evenwicht in de natuur’ een belangrijke rol. In aanvulling hierop laat het onderzoek uit Hoofdstuk 6 zien dat gevoelens van respect voor de natuur, in combinatie met een beperkt inzicht in de rol van mensen bij de introductie van exoten, juist kunnen leiden tot het opzettelijk uitzetten van uitheemse soorten in het wild. Hieruit wordt geconcludeerd dat de koppeling van bewustwording van de eigen rol bij de introductie van exoten aan de mogelijk schadelijke gevolgen hiervan voor de natuur belangrijk is voor het vergroten van de betrokkenheid van burgers. Dit speelt met name een rol bij maatregelen die gericht zijn op preventie van nieuwe introducties van exoten. Voorbeelden van preventieve beleidsinstrumenten zijn een verbod op het houden van bepaalde soorten, een vrijwillige overeenkomst hieromtrent (ook wel een convenant of gedragscode genoemd) en publieksvoorlichting. In Hoofdstuk 6 is de effectiviteit van het convenant waterplanten en de bijbehorende communicatiecampagnes onderzocht. Deze gedragscode is gericht op het vergroten van de bewustwording omtrent uitheemse invasieve waterplanten in de maatschappij en, uiteindelijk, het voorkomen van nieuwe introducties. Van de vier maatregelen die zijn geëvalueerd is de naleving van afspraken over het uit de handel halen van soorten het meest effectief bevonden. De maatregelen voor het vergroten van de bewustwording van consumenten bestonden uit voorlichtingscampagnes en het weergeven van een waarschuwing op het etiket van potentieel invasieve soorten. Het uitblijven van resultaten op dit vlak wordt met name toegeschreven aan de korte looptijd van het evaluatieproject. Succesfactoren voor het opstellen en uitvoeren van gedragscodes in de handelssector zijn het betrekken van alle relevante actoren, het opstellen van een gezamenlijke visie en doel, en het opzetten van een goede communicatiestructuur, zowel tussen de convenantpartners als met de doelgroepen. In Hoofdstuk 7 worden de belangrijkste conclusies van ieder hoofdstuk gepresenteerd. Gedurende dit promotieonderzoek is de focus verschoven van het beoordelen en classificeren van de risico’s van exoten naar de studie van perceptie van exoten en de begrippen die gebruikt worden bij het beschrijven van bioinvasies. Het tweede hoofdstuk van dit proefschrift speelt in dit opzicht een dubbelrol. Dit hoofdstuk kan namelijk gelezen worden als een gerichte natuurwetenschappelijke oefening, maar ook in het licht van het gebruik van metaforen voor het beschrijven en duiden van de onderzoeksresultaten. De verschuiving van een natuurwetenschappelijk naar een sociaalwetenschappelijk perspectief biedt tevens de mogelijkheid voor reflectie op de kansen voor integratie van deze twee perspectieven binnen het exotenbeleid en -beheer. Het nut van sociaalwetenschappelijke studies naast de natuurwetenschappen wordt vaak uitgelegd als een manier om draagvlak te creëren voor maatregelen en om conflicten te voorkomen. Dit proefschrift laat zien dat bijdragen van de sociale wetenschappen meer bieden dan alleen ‘end-of-pipe’ oplossingen voor exotenbeheer. Voor risicobeoordeling ligt de uitdaging op het gebied van het (h)erkennen van normatieve aspecten in het beoordelingsproces en de toepassing van (anekdotische) kennis van experts. Voor risicomanagement ligt de meerwaarde in de kennisneming van publieke waarden en normen die een rol spelen bij de omgang met exoten, en die strategisch kunnen worden ingezet bij het implementeren van (preventieve) maatregelen. Een vereiste voor effectieve 158 risicocommunicatie is voldoende en betrouwbare kennis van potentiële doelgroepen en het uitvoeren van evaluaties van de effectiviteit van publieksvoorlichting. Tot slot zal verder onderzoek naar menselijke activiteiten en (individuele) motivaties die de introductie, vestiging, verspreiding en beheersmaatregelen van exoten faciliteren bijdragen aan verbetering van de kwaliteit van risicoanalyses. Dit hoofdstuk sluit af met een overzicht van de aanbevelingen voor beleid en nader onderzoek.

Dankwoord Dankwoord

Aan ieder proefschrift is een verhaal verbonden. Een verhaal dat vertelt wat de weg van begin tot eind zo bijzonder heeft gemaakt en dat alle omwegen, short-cuts, dalen, hoogtepunten en vergezichten beschrijft. Een aantal bijzondere hoofdstukken uit mijn verhaal wil ik hier met jullie delen. Mijn verhaal begon in 2010 toen ik als deeltijd onderzoeker begon bij de afdeling Milieukunde. In die beginperiode was het nog helemaal niet vanzelfsprekend dat ik de tijd en ruimte zou hebben om mijn werkzaamheden uit te breiden tot een volwaardig promotieonderzoek. Door het bundelen van de krachten van twee instituten binnen deze universiteit, ISIS (Institute for Science, Innovation and Society) en IWWR (Institute for Water and Wetland Research), heb ik de mogelijkheid gekregen om een interdisciplinair onderzoek op te zetten, met dit proefschrift als resultaat. Jan en Hub, dank voor al jullie hulp, geduld en vooral voor de fijne samenwerking tussen ISIS en de afdeling Milieukunde. Dit gaf mij de kans om mijn ambities in zowel de natuurwetenschappen als de sociale wetenschappen te realiseren. Het was soms best moeilijk om daar een tussenweg in te vinden, maar wel een mooie zoektocht die mij hopelijk nog veel meer gaat brengen. Toen ik in 2010 begon waren we overburen in het Huygensgebouw en het is goed dat we dat, na een uitstapje van ISIS naar Mercator, nu weer zijn. Dit proefschrift had ook niet kunnen bestaan zonder de rol van de Nederlandse Voedsel en Waren Autoriteit (NVWA) als opdrachtgever en financierder van een belangrijk deel van mijn onderzoek. Mijn dank hiervoor gaat uit naar alle betrokkenen bij de NVWA in de afgelopen jaren, en in het bijzonder naar Wiebe, José, Tom en Johan. Ik heb bijzonder genoten van het doen van praktijkgericht onderzoek en hoop dat het voor jullie nieuwe inzichten en handvatten biedt voor het exotenbeheer in Nederland. Mijn dank gaat ook uit naar mijn collega-onderzoekers binnen het Nederlands Expertise Centrum Exoten (NEC-E) voor de waardevolle kennisuitwisseling en vruchtbare samenwerking. Daarnaast heeft de toekenning van het Frye Stipendium door het College van Bestuur mij in staat gesteld om mijn onderzoek overzees onder de aandacht te brengen. Deze (internationale) bagage neem ik mee in mijn verdere academische loopbaan. Nu dit boekje hier ligt, weet ik uit eigen ervaring dat promoveren veel meer is dan alleen het doen van onderzoek en het schrijven van artikelen. Gedurende vier jaar wordt je niet alleen als wetenschapper op de proef gesteld maar groei je ook als mens. Op deze reis heb ik veel gehad aan mijn collega’s, vrienden en familie, die ik hier niet allemaal kan noemen maar bij deze wel wil bedanken. Een aantal hoofdpersonen wil ik hier in het bijzonder noemen. Rob, ik wil je bedanken voor veel dingen, maar vooral omdat je aan de wieg stond van dit proefschrift en met al je inspanningen en creatieve constructies deze promotie mede mogelijk hebt gemaakt. Ik weet nog goed dat ik, wegens andere verplichtingen, dacht dat ik niet kon gaan werken aan ons eerste project samen. Gelukkig ben ik daar snel op teruggekomen, en dit boekje is daarvan uiteindelijk het resultaat! Heel veel dank voor alles wat ik van je heb kunnen leren in de afgelopen jaren, en niet te vergeten, je rotsvaste geloof in mij. Ik weet zeker dat dit mij het vertrouwen heeft gegeven om te komen waar ik nu ben.

162 Dankwoord

Riyan, heel veel dank voor al je enthousiasme en inspirerende ideeën die dit proefschrift hebben verrijkt. Met de overstap naar ISIS heb ik een unieke plek gevonden waar ik mijn nieuwsgierigheid de vrije loop kan laten. Het is een mooie uitdaging om daar nu een route uit te gaan stippelen. We delen veel interesses op onderzoeksgebied en ik kijk vooral ook uit naar alles wat we in de toekomst samen nog gaan doen! Lisette en Didi, mijn paranimfen, en steun en toeverlaat op deze mooie dag, jullie verdienen hier natuurlijk ook een plek! Ik ben ontzettend blij dat jullie deze eervolle taak op jullie hebben willen nemen. Martijn, bedankt voor het opmaken van mijn proefschrift, je hebt me veel werk uit handen genomen. Ik wil ook al mijn kamergenoten uit HG02.741 bedanken voor de leuke tijd die ik er heb gehad, in het bijzonder Erik, Lisette, Pieter en Yen. Matteusz, Jochem en Andrea, bedankt voor de gezelligheid tijdens de laatste paar maanden in het Mercatorgebouw. Thanks for all the nice coffee, burgers and beers! Jon Matthews, bedankt dat je als ‘native speaker’ altijd bereid was om mijn teksten door te lezen op correct gebruik van de Engelse taal. Mijn dank gaat ook uit naar Jon Westlake voor alle pogingen die je daartoe ondernomen hebt ;) tussen al je drukke werkzaamheden door. Dat dit uiteindelijk niet zoveel resultaat had, maakt niet uit. It’s the thought that counts! Verder heb ik bij het verzamelen van alle data die ten grondslag liggen aan Hoofdstuk 6 hulp gehad van een aantal collega’s en student-assistenten. Jan, Pieter, Jon, Frank, Remon, Vera, Gitte, Lieke, Christien, Hinke, Lilly, Martina, Loes, Lopke, Dieuwertje en Didi, bedankt! Als promovendus zijn er af en toe ook momenten dat je even niet met je onderzoek bezig wil zijn, om daarna weer met frisse ideeën en energie aan de slag te gaan. Tante Carla, bedankt voor de onafgebroken stroom aan boeken die de afgelopen jaren vanuit Reeuwijk mijn kant zijn opgekomen, en die zorgden voor de nodige afleiding maar ook voor nieuwe inspiratie. Alie en Bernhard, bedankt voor de relativering, humor en gezelligheid bij jullie aan de keukentafel. En last but zeker not least, bedankt pap, mam en Dieuw, gewoon… omdat jullie er altijd voor me zijn!

163

Curriculum vitae CV

Laura Nicoline Halley Verbrugge was born in Rhenen (The Netherlands) on August 9, 1986. She attended high school (Rembrandt College) in Veenendaal. In 2007 she completed her bachelor in Environmental Sciences at Utrecht University with a thesis on the adaptation of Dutch water management to increasing river dynamics of the Rhine. In 2008 she started her Master in Environmental Sciences at the Radboud University Nijmegen. She enrolled in the Science communication track to study the interactions between science, society and the environment. During her first internship at the Department of Environmental Science (Institute for Water and Wetland Research) she studied the effects of climate change on native and non-native species in the river Rhine. Her graduation project at the Department of Philosophy and Science Studies (Institute of Science, Innovation and Society) was part of the science communication track and was titled: ‘Public perception of non-native species in the Netherlands in relation to visions of nature’. She received her Master degree in 2011. During her student time at Radboud University Nijmegen she assisted working group assignments in the course ‘Human and Environment’ for several years. She also worked as a project assistant at the Department of Environmental Science in an OBN research project in which she was responsible for environmental data acquisition on side channels in the Netherlands to facilitate research on habitat requirements of native and non-native riverine fish species. Furthermore, she participated in a number of projects on risk assessment and risk prevention of biological invasions and (co)authored several reports commissioned by the Netherlands Food and Consumer Product Safety Authority (NVWA). During the years 2010-2013, she was employed as junior researcher on a joined PhD project at the Department of Philosophy and Science studies and the Department of Environmental Sciences. This thesis is the result of her research activities conducted during this period. She was awarded the Frye Stipendium in December 2012, a scholarship named after one of the first female faculty members at Radboud University Nijmegen, which aims to encourage female PhD students to continue their academic careers upon completion of their theses. In spring 2014 she started as a Postdoc in the STW-funded RiverCare programme at the Institute of Science, Innovation and Society. She currently lives in Nijmegen.

166

List of publications List of publications

Publications in peer-reviewed journals Verbrugge LNH, Schipper AM, Huijbregts MAJ et al. (2012) Sensitivity of native and non-native mollusc species to changing river water temperature and salinity. Biological Invasions 14: 1187-1199 Verbrugge LNH, Van der Velde G, Hendriks AJ et al. (2012) Risk classifications of aquatic non-native species: application of contemporary European assessment protocols in different biogeographical settings. Aquatic Invasions 7: 51-60 Verbrugge LNH, Van den Born RJG, Lenders HJR (2013) Exploring public perception of non-native species from a visions of nature perspective. Environmental Management 52: 1562-1573 Collas FPL, Koopman KR, Hendriks AJ et al. (2014) Effects of desiccation on native and non- native molluscs in rivers. Freshwater Biology 59: 41-55 Verbrugge, LNH, Leuven RSEW, Zwart HAE (2014) Metaphors in invasion science: implications for risk assessment and management of biological invasions. Submitted Verbrugge LNH, Leuven RSEW, Van Valkenburg JLCH et al. (2014) Evaluating stakeholder awareness and involvement in risk prevention of aquatic invasive plant species by a national code of conduct. Aquatic Invasions 9(3): 369-381, 2014

Reports Verbrugge LNH, Leuven RSEW, Van der Velde G (2010) Evaluation of international risk assessment protocols for exotic species. Reports Environmental Science 352, Radboud University, Nijmegen, 54 p. Verbrugge LNH, Leuven RSEW, Van der Velde G (2010) Towards a risk assessment protocol for exotic species: review of conclusions and recommendations by experts and end users. Reports Environmental Science 366, Radboud University, Nijmegen, 17 p. Verbrugge LNH, Van den Born RJG, Leuven RSEW (2011) Evaluatie convenant waterplanten: startmeting. Reports Environmental Science 383, Radboud University, Nijmegen, 84 p. (in Dutch) Collas FPL, Beringen R, Koopman KR et al. (2012) Knowledge document for risk analysis of the non-native Tapegrass (Vallisneria spiralis) in the Netherlands. Reports Environmental Science 416, Radboud University, Nijmegen, 38 p. Koopman KR, Beringen R, Collas FPL et al. (2012) Knowledge document for risk analysis of the non-native Monkeyflower (Mimulus guttatus) in the Netherlands. Reports Environmental Science 415, Radboud University, Nijmegen, 43 p. Matthews J, Beringen R, Collas FPL et al. (2012) Knowledge document for risk analysis of the non-native Curly Waterweed (Lagarosiphon major) in the Netherlands. Reports Environmental Science 414, Radboud University, Nijmegen, 43 p. Matthews J, Beringen R, Collas FPL et al. (2012) Risk analysis of non-native Curly Waterweed (Lagarosiphon major) in the Netherlands. Reports Environmental Science 418, Radboud University, Nijmegen, 32 p. Matthews J, Beringen R, Collas FPL et al. (2012) Risk analysis of the non-native Monkeyflower (Mimulus guttatus) in the Netherlands. Reports Environmental Science 419, Radboud University, Nijmegen, 29 p. Matthews J, Beringen R, Collas FPL et al. (2012) Risk analysis of non-native Tapegrass (Vallisneria spiralis) in the Netherlands. Reports Environmental Science 420, Radboud University, Nijmegen, 32 p. Rijks JM, Spitzen-Van der Sluijs A, Leuven RSEW et al. (2012) Risk analysis of the common midwife toad-like virus (CMTV-like virus) in the Netherlands. NVWA, Min EZ report 60000784-2012, 81p. 170 List of publications

Matthews J, Beringen R, Lamers LPM et al. (2013) Risk analysis of the non-native Fanwort (Cabomba caroliniana) in the Netherlands. Reports Environmental Science nr. 442. Radboud University, FLORON & Roelf Pot Research and Consultancy, Nijmegen, 46 p. Matthews J, Beringen R, Lamers LPM et al. (2013) Knowledge document for risk analysis of the non-native Fanwort (Cabomba caroliniana) in the Netherlands. Reports Environmental Science 443, Radboud University, FLORON & Roelf Pot Research and Consultancy, Nijmegen, 60 p. Verbrugge LNH, Van den Born RJG, Leuven RSEW (2013) Evaluatie convenant waterplanten 2010-2013. Reports Environmental Science 440. Radboud University, Nijmegen. 98 p. (in Dutch) Matthews J, Creemers R, Hollander, H et al. (2014) Horizon scanning for new invasive non- native species in the Netherlands. Reports Environmental Science 461. Radboud University, Nijmegen. 114 p.

International conferences Verbrugge LNH, Schipper AM, Huijbregts MAJ et al. (2010) Potential effects of water temperature and salinity on native and exotic mollusc species in the river Rhine. In: Stouthamer E (ed) NCR-Days 2010, Netherlands Centre for River Studies, Delft. p. 31-33 Verbrugge LNH, Leuven RSEW, Lammers JW et al. (2010) Evaluation of international risk assessment protocols for exotic species. Abstract for the 17th International Conference on Aquatic Invasive Species (ICAIS), August 29 to September 2, San Diego, US Verbrugge LNH, Van den Born RJG, Lenders HJR (2012) Public perception of non-native species and visions of nature in The Netherlands (poster presentation). Abstract for the 7th European Conference on Biological Invasions (NEOBIOTA), September 12 to 14, Pontevedra, Spain Rijks JM, Spitzen-Van der Sluijs A, Leuven RSEW et al. (2013) Risk analysis of common midwife toad-like virus in The Netherlands. Abstract for the Second International Symposium on Ranaviruses, July 27 to 29, Knoxville, US Verbrugge LNH, Leuven RSEW, Van den Born RJG (2013) Do codes-of-conduct increase public awareness and engagement in problems with aquatic invasive plants? Abstract for the 18th International Conference on Aquatic Invasive Species (ICAIS), April 21 to 25, Niagara Falls, Canada. Verbrugge LNH, Leuven RSEW, Van den Born RJG (2013) Do codes-of-conduct increase public awareness and engagement in problems with aquatic invasive plants? Abstract for the EPPO/CoE/ IUCN ISSG International Workshop “How to communicate on pests and invasive alien plants?” October 8 to 10, Oeiras, Portugal.

Other publications Van den Born RJG, Verbrugge LNH (2013) De maatschappelijke beleving van exoten, NATURA 110: 12-13 Geen exoot in de sloot. De Telegraaf, 1 juni 2013. Achtergronden p. 4

171

Series ‘Mechanisms and constraints in biodiversity conservation and restoration’. 1. Verberk WCEP (2008) Matching species to a changing landscape – aquatic invertebrates in a heterogeneous landscape 2. Remke E (2009) Impact of atmospheric deposition on lichen-rich, coastal dune grasslands 3. Van Kleef HH (2010) Identifying and crossing thresholds in managing moorland pool macroinvertebrates 4. Vermonden K (2010) Key factors for biodiversity of urban water systems 5. Van Turnhout CAM (2011) Birding for science and conservation. Explaining temporal changes in breeding bird diversity in the Netherlands 6. Schipper AM (2011) Multiple stressors in floodplain ecosystems. Influences of flooding, land use and metal contamination on biota 7. Van Duinen GA (2013) Rehabilitation of aquatic invertebrate communities in raised bog landscapes 8. Van Noordwijk CGE (2014) Through arthropod eyes. Gaining mechanistic understanding of calcareous grassland diversity The series ‘Mechanisms and constraints in biodiversity conservation and restoration’ is created to aggregate and disseminate knowledge relevant for the conservation and rehabilitation of biodiversity and ecosystems. The series is a co-production of ‘Natuurplaza’ and the ‘Institute for Water and Wetland Research’ (IWWR) of Radboud University Nijmegen. ‘Natuurplaza’ aims to generate knowledge to be applied in nature management, based on collection and analysis of species distribution data in the Netherlands. It is constituted by the following organisations: - Bargerveen Foundation - SOVON Dutch Centre for Field Ornithology - Reptile, Amphibian & Fish Conservation Netherlands (RAVON) - FLORON Foundation - Dutch Mammal Society The Institute for Water and Wetland Research (IWWR) of the Radboud University Nijmegen aims to increase the understanding of responses and adaptations to stress at various levels of biological organisation, ranging from molecule to ecosystem. It comprises research groups on plant and animal ecology and physiology, aquatic ecology and environmental sciences. The Institute of Science, Innovation and Society (ISIS) of the Radboud University Nijmegen aims to analyse, assess and improve the societal embedding of science and technology, through research, education and communication, and in close collaboration with the other institutes of the Faculty of Science. ISIS and IWWR participate together with ‘Natuurplaza’ in the Netherlands Expertise Centre for Exotic Species (NEC-E). The aim of the NEC-E is to develop and implement science-based innovative management strategies for invasive species, through research on species-specific and ecosystem-based measures as well as their social implications.