4 The production of systems knowledge – Understanding the processes underlying biotic invasions

Seven different research approaches can be distinguished that have been or are used in invasion research to clarify systems knowledge. These research approaches differ in their research questions and methods, and have different implications for problem solving (Table 1). They are introduced shortly in the following in their historical order.

4.1 The classical model

The classical model of biotic invasions structured research on the causal relationships of biotic invasions along two main questions (Drake et al., 1989*; Williamson, 1996*): what factors determine whether a species is an invader or not (species invasiveness)?, and 2) what characteristics explain why some habitats are more vulnerable to invasions than others (habitat invasibility)? The two questions restricted the field of invasion research to population and community ecologists. In particular, explicit spatial processes were treated only marginally by using highly generalised mathematical models for describing the spread of invasive species in space (Shigesada and Kawasaki, 1997*; Williamson, 1996*), and these spread models were not linked to research on species invasiveness or habitat invasibility. This neglect was problematic because it was shown that the number of individuals (e.g. larvae, seeds or other forms of propagules such as vegetative parts of plants) that arrive at a site (propagule pressure) is an important factor for explaining the degree of invasion (Lonsdale, 1999*; Williamson, 1996*). For the prediction of propagule pressure at a given site, processes at larger spatial scales such as population spread, seed dispersal or human transportation need to be considered (Lockwood et al., 2005; With, 2002*). In the classical model these processes were not explicitly studied, yet propagule pressure was included in analyses as a third but unstudied explanatory factor external to the studied system.

Research on plant invasiveness (Daehler, 1998, 2003*; Grotkopp et al., 2002; Kolar and Lodge, 2001*; Rejmanek, 1996; Richardson and Pyšek, 2006*; Sakai et al., 2001) and habitat invasibility (Alpert et al., 2000*; Davis et al., 2000*; Drake et al., 1989*; Lonsdale, 1999; Stohlgren et al., 1999) was mostly based on global biogeographic comparisons of descriptive natural history information or experimental studies of single species, and relied on the assumption that the alien provenance of a species is an important explanatory factor. However, to date it is not clear if invasive alien species generally differ from native species with a high potential to colonise new areas (Thompson et al., 1995). The most consistent predictors for the invasiveness of a species are the history of being invasive in other regions and a matching between the climates of the native and introduce areas (Kolar and Lodge, 2001*). The few more specific traits that proved to be more generally associated with invasive species (Kolar and Lodge, 2001*; Richardson and Pyšek, 2006*) are mostly those already identified for weeds, whether native or alien (Baker, 1974). For instance, invasive species tend to exhibit high growth rates and seed outputs and have efficient dispersal mechanisms such as by wind or birds (Kolar and Lodge, 2001*), but these differences depend on the environmental conditions, and invasive species do not generally outperform native species (Daehler, 2003).

Research on habitat invasibility led to generalisations such as that (anthropogenically) disturbed, and resource-rich, early-successional habitats are more vulnerable to invasions than undisturbed, resource-poor and late-successional habitats (Alpert et al., 2000; Davis et al., 2000; Drake et al., 1989*). It also became evident that the presence of invasive species can have a strong influence on the functioning of the invaded ecosystem (Levine et al., 2003*; Vitousek, 1990*), and in particular that in some cases invasive species change habitat conditions in a way that facilitate further invasions (Simberloff, 2006*).

Research on species invasiveness and habitat invasibility have so far not been successful in providing robust prediction beyond the heuristics mentioned above (Mack and Barrett, 2002*). However, a large, global dataset on biotic invasions has accumulated, which is rather unique for ecology and provides opportunities for studying invasion patterns as well as general ecological patterns through data mining (Cadotte et al., 2006b; Crall et al., 2006).

4.2 Phase transition models

Phase transition models are based on the assumption that invasion processes can be divided into different phases that are characterised by different ecological and evolutionary processes. Originally, three different phases were recognised: i. transport to a new area, ii. establishment and possibly lag-phase during which the population size remains small, and iii. spread (Kolar and Lodge, 2001; Richardson et al., 2000; Williamson, 1996*). Recently, the particularities of the establishment phase in contrast to the spread phase have been studied in more detail (Kolar and Lodge, 2002; Marchetti et al., 2004; Mack and Barrett, 2002*; Puth and Post, 2005). Dietz and Edwards (2006) proposed to further divide the spread phase into a primary and secondary invasion phase. They argue that initial spread happens in highly disturbed habitats by species that had no time to adapt to local environmental conditions, and that invasive alien species invade less disturbed habitats only after adaptation to local conditions during primary invasion. Facon et al. (2006*) more generally emphasised the need to consider evolutionary and habitat changes with the progression of an invasion.

4.3 Natural experiments

Research according to the classical model produced results that touched upon key questions in general ecology, and this triggered an interest among ecologists to use biotic invasions for the study of basic ecological principles (Cadotte et al., 2006a*; Callaway and Maron, 2006*; Sax et al., 2007*). In this way biotic invasions can be understood as large-scale, so called “natural experiments” (Diamond, 1983) that are unique research opportunities for basic ecology (Cadotte et al., 2006a*). The research on habitat invasibility resonated with major research interests in community and ecosystem ecology that address the relationship between biodiversity and ecosystem functioning, or the relative importance of random and deterministic processes in community assembly (Cadotte et al., 2006a; Callaway and Maron, 2006*; Sax et al., 2007*). For example, one of the discussed aspects, already addressed by Elton (1958*), was the hypothesis that species-richer habitats are more resistant to biotic invasions than species-poor habitats (Fridley et al., 2007; Levine et al., 2004). The relevance of propagule pressure for community assembly was further studied with a more theoretical focus (Callaway and Maron, 2006*). Contrary to expectation, it emerged that natural ecosystems are often not saturated with species (Sax et al., 2007). In some cases, the alien provenance of the invasive species was the critical factor explaining invasion success. Alien species can profit in the introduced area from the release from their natural enemies such as pathogens or herbivores that are only present in the area of origin (Keane and Crawley, 2002). Additionally, some plant species compete with neighbouring plants by releasing chemicals (allelopathy). While in the native range the neighbouring plants are adapted through long-term coevolution to cope with these chemicals, this is not the case for plants in the area of introduction that consequently suffer heavily from allelopathic substances of invasive alien species (Callaway and Maron, 2006*). These observations have provided general insights into the regulation of plant populations and the structuring of ecological communities. Another recent observation that owes much to invasion research has been that some species have the ability to evolve rapidly in ecologically relevant time spans (Callaway and Maron, 2006*; Facon et al., 2006; Richardson and Pyšek, 2006). Species niches, i.e., the specialisation of a species in environmental space, may therefore be less stable than previously thought (Broennimann et al., 2007; Holt et al., 2005).

4.4 Multifactorial analyses of case studies

It has been recurrently concluded that invasion processes are often idiosyncratic and that a multifactorial understanding of particular cases (Kueffer, 2006*; Orians et al., 1986; Shrader-Frechette, 2001*) is therefore needed (Callaway and Maron, 2006; Eppstein and Molofsky, 2007; Williamson, 1996*). For instance, the impact of herbivores on invasive species depends on soil fertility (Blumenthal, 2005), and this relation is further linked to propagule pressure (Sanders et al., 2007). Invasions interact in complex ways with anthropogenic habitat modification (Didham et al., 2007), climate change (Thuiller et al., 2007) and other global change factors (Mooney and Hobbs, 2000).

4.5 Landscape ecology

Throughout most of the history of invasion biology, the spatial spread of invasive species was described by fitting highly generalised mathematical models (Shigesada and Kawasaki, 1997; Williamson, 1996; With, 2002*). With (2002) initiated a broader research interest in landscape ecological research that explicitly addresses the influence of landscape structure on invasions, and it became evident that the spatial and temporal variation of environmental factors influences the spread of invasive species (Hastings et al., 2005; Melbourne et al., 2007). Landscape research on biotic invasions awaits a synthesis, but it appears that the integration of different spatial scales will be a major challenge in invasion research in the coming years (Kühn and Klotz, 2007; Pauchard and McKinney, 2006; Pyšek and Hulme, 2005). While the application of spatial ecology to biotic invasions has attracted interest, other fields of landscape research have so far mostly ignored the issue, even though geographers have recurrently emphasised the value of their expertise for studies of biotic invasions (e.g. Vale and Parker, 1980). Contributions from physical geography may for instance come from remote sensing (Asner and Vitousek, 2005; Bradley and Mustard, 2006) and GIS modelling (Peterson, 2003).

4.6 Vector science

The study of transportation vectors or pathways has become an active research area over the past few years (Kowarik and von der Lippe, 2007; Lodge et al., 2006*; Meyerson and Mooney, 2007*; Mooney et al., 2005*; Mack and Barrett, 2002*; Ruiz and Carlton, 2003*). Because of the relevance of human agency for transportation, such research necessarily has to integrate natural and social sciences. Important past and present transportation factors that contribute to explaining distributions of alien species include colonial expansion, wars, ballast water of ships, plant and animal trade, railway, road and water canal networks, agricultural and forestry activities, botanical gardens and urbanisation (McNeely, 2001*; Ruiz and Carlton, 2003). A well-studied example is the role of ornamental trade in biotic invasions (Dehnen-Schmutz et al., 2007a,b; Reichard and White, 2001*). A relevant aspect of deliberate human-assisted introductions is that these are non-random; i.e., deliberately introduced organisms are often selected or bred specifically for the local conditions (e.g. in forestry Richardson, 1998). In order to reconstruct paths and predict future transport pathways, a thorough understanding of peoples’ motivations for moving particular plants is needed (Brook, 2003; Daehler, 2007; Mack, 2001; McNeely, 2001).

4.7 Land use science

A multitude of studies have shown the relevance of anthropogenic habitat modification and land use for explaining biotic invasions (e.g. Deutschewitz et al., 2003; Hobbs, 2000; Maskell et al., 2006; Pauchard and Alaback, 2004). For the understanding of land use practices that influence plant invasions, social sciences research on human activities is essential. Not only current, but also the legacy of past land use can be relevant for current invasion processes (Domènech et al., 2005; Von Holle and Motzkin, 2007).

The urban ecosystem is a pronounced case of an ecosystem shaped by human activity that is of relevance to invasion research. Urban areas function as hubs for biotic exchange (La Sorte et al., 2007, and citations therein) and create novel habitats favourable for alien species. The influence of human factors on the occurrence of invasive species in urban areas is, for instance, evident in the cases of the vegetation composition of green spaces (e.g. Thompson et al., 2003), or the presence of invasive fire ants (Plowes et al., 2007).

Another human-dominated system with high relevance to invasions is agricultural land (Smith et al., 2006*). In Europe, alien species that were introduced with early agriculture are more often associated with crops from this time period (cereals), while recently introduced weeds are more often associated with recently introduced crops (maize, rape) (Pyšek et al., 2005). Agricultural practices may influence the evolution of invasive species (Franks et al., 2004; Kowarik, 2003*). In turn, invasions can feed back on land use decisions of farmers (Schneider and Geoghegan, 2006*). Through the expansion of agri-environmental schemes and extensification of agriculture in Europe and North America, socio-political changes may influence invasion spread (Donald and Evans, 2006).

Research on the relation between land use and biotic invasions has so far mainly compiled case examples, and waits for a conceptual synthesis (cf. Kueffer and Daehler, 2008*). It is directly related to the management of invasive species in human-dominated habitats. Such an integration of invasive species management in different economic sectors has been termed “mainstreaming of invasive species management” (Petersen and Huntley, 2005).