Supporting Information Table S1
Supporting Information Table S1
Integrative invasion science: model systems, multi-site studies, focused meta-analysis, and invasion syndromes
Christoph Kueffer1, Petr Pyšek2,3, David M. Richardson4
Table S1 Overview of interesting model systems for invasion science
The table lists interesting model systems for invasion science in three sections: (1) individual species or small groups of congeners, (2) genera and families, and (3) model ecosystems. The table is not meant to be comprehensive but rather illustrates the range of interesting model systems by including examples of those that (i) are already intensively studied, (ii) have produced important insights, (iii) provide good illustrations of particular aspects of model system research, or (iv) are underutilised to date as model systems.
1. INDIVIDUAL SPECIES OR SMALL GROUPS OF CONGENERS
Model organism / ExplanationAcer spp. (esp.A. negundo, A. platanoides) / Among the most intensively studied invasive plant species(Pyšek et al., 2008b)Shade-tolerant invaders of undisturbed forest (Martin & Marks, 2006). Reciprocal pair of invaders in North America and Europe - allows for reciprocal comparative studies of behaviour in native and alien range (Reinhart & Callaway, 2004)
Ailanthus altissima / Asian species invasive in riparian and disturbed forest habitat in both North America and Europe (compare entries on Fallopia, Impatiens, Lonicera, and riparian habitat invaders). Recent comprehensive synthesis (Kowarik & Saumel, 2007).
Alliaria petiolata / Among the most intensively studied invasive plant species(Pyšek et al., 2008b); Recent syntheses (Barney & Whitlow, 2008; Rodgers et al., 2008a). Comprehensive coverage of biogeography, enemy release, evolution of increased competitive ability, allelopathy, the role of plant-soil interactions, belowground effects on competing plants (both direct, and indirect via interference with mutualisms), phenotypic plasticity, and the empty niche concept (e.g. Bossdorf et al., 2004; Durka et al., 2005; Callaway et al., 2008; Rodgers et al., 2008b; Lankau et al., 2009; Cipollini & Lieurance, 2012). In-depth studies on allelopathy and belowground plant-plant interactions (e.g. Stinson et al., 2006; Callaway et al., 2008; Wolfe et al., 2008; Barto et al., 2011; Lankau, 2011a; Lankau, 2011b).An exciting research opportunity is provided by well-documented chronosequences of Alliaria invasions in North America (e.g. Lankau et al., 2009; Lankau, 2011b). Comparisons of invasion patterns between the native and invaded distribution range in preparation ( Comprehensive data on Alliaria has been used to develop detailed population models for management (Pardini et al., 2009; Evans et al., 2012). See also main text.
Bromus tectorum / One of the most intensively studied invasive species {Pyšek, 2008 #9;Pyšek, 2008 #5304}(Pyšek et al., 2008b) including impacts(Hulme et al., 2012); and one of the most problematic plant invaders in North America. Comprehensive reviews on the species have recently been published (Young & Clements, 2009; Mack, 2010b; Mack, 2010a), and older species monographs are also available (Klemmedson & Smith 1964; Upadhaya et al., 1986). A large genus with both invasive and non-invasive species facilitating comparisons across species. Particularly interesting as a model system of grass invasions into dry grasslands, documenting the effect of interaction among life form and adaptation to herbivory in invasions, and the role of invasive grasses in affecting fire regimes (compare entry on herbaceous grassland invasions). The introduction history, population genetics, population biology, and ecosystem impacts of the species in North America have been very well documented (Mack, 2010b; Mack, 2010a).
Centaurea spp. (esp. C. stoebe [maculosa], C. solstitialis) / Among the most intensively studied invasive plant species(Pyšek et al., 2008b). Classical studies on plant-plant interactions, the novel weapons hypothesis and allelopathy (Callaway & Aschehoug, 2000; Bais et al., 2003; Callaway et al., 2004; Callaway et al., 2005; Callaway et al., 2011), and climatic niche shift (Broennimann et al., 2007; Petitpierre et al., 2012). Also enemy release, evolution of increased competitive ability (EICA), or rapid evolution have been studied(e.g. Seastedt et al., 2005; Hahn et al., 2012). Some of the best empirical evidence of polyploids as invasives comes from this species (Treier et al., 2009). Versatile model invader of grassland (fc. Alliaria petiolata invading forests). Large genus with both invasive and non-invasive species.
Cirsium (esp.C. arvense, C. vulgare) / Long-term and intensive agricultural weed research in both native and alien range. Also invasive in naturalareas.
Clidemia hirta / One of the most widespread invasive plants in the tropics (Lowe et al., 2000; Kueffer et al., 2010a). Classical studies on the role of enemy release in facilitating invasion of shaded forest understorey (DeWalt et al., 2004) and low genetic diversity in invasive populations (DeWalt & Hamrick, 2004). See also entries on Melastomataceae.
Cynoglossum officinale / An exemplary study that integrates and evaluates multiple facets of a plant invasion, including enemy release and differences in life-history strategies, through population models and the comparison of multiple native and invasive populations has recently been published (Williams et al., 2008; Williams, 2009; Maron et al., 2010; Williams et al., 2010).
Cytisus spp. (C. multiflorus, C. scoparius) / Among the most intensively studied invasive plant species(Pyšek et al., 2008b), including early examples ofcomparative studies in the native range (Paynter et al., 1998) Nitrogen-fixing invader of heathland and pasture both in the native range (Europe) and contrasting alien ranges (North America, Australia, New Zealand). Invader of mountain ecosystems. See also entries on woody plant invasions of grasslands and mountain ecosystems.
Falcataria moluccana / syn. Paraserianthes falcataria. One of the most widespread invasive plants on tropical islands (Kueffer et al., 2010a). Besides Morella faya, the best studied tropical woody nitrogen-fixing species impacting nutrient dynamics. Contrasting results from nitrogen-poor sites in Hawaii (Hughes & Denslow, 2005; Hughes & Uowolo, 2006; Mascaro et al., 2012) and phosphorus-poor soils in the Seychelles (Kueffer et al., 2008; Kueffer, 2010)emphasize the importance of cross-site studies.
Fallopia [Reynoutria] spp. (esp. F. japonica) / Among the most intensively studied genera of invasive plants (Pyšek et al., 2008b)including impacts (Hulme et al., 2012) and multi-site comparative studies (Maurel et al., 2013), that are among the most problematic plant invaders in Europe. Clonally reproducing species with rare events of interspecific hybridization provide an interesting model for studying the role of hybridization, genome identity(Pyšek et al., 2003; Mandak et al., 2004), epigenetic differentiation (Richards et al., 2012), and vegetative growth (Hollingsworth & Bailey, 2000; Bimova et al., 2003) in invasiveness.Attractive for comparative analyses: Two Asian species of the Polygonaceae family (see entry), and invasive in riparian and disturbed forest habitat in both North America and Europe (compare entries on Ailanthus, Impatiens, Lonicera, and riparian habitat invaders), but also other habitat such as beaches or saltmarshes (Richards et al., 2008).
Hedychium spp. (esp. H. gardnerianum) / One of the most widespread invasive plant genera in the tropics (Lowe et al., 2000; Kueffer et al., 2010a) where species invade shaded forest understorey and montane cloud forest. The invasive behaviours of the species are not well understood. See entry on forest understorey invaders.
Heracleum mantegazzianum / Among the most intensively studied invasive plant species(Pyšek et al., 2008b)including impacts (Hulme et al., 2012); and among the most problematic plant invaders in Europe. The species has been comprehensively addressed through an EU research program ( that produced detailed knowledge of long-term invasion dynamics at different spatial scales (Müllerová et al., 2005; Pyšek et al., 2008a), the role of long-distance dispersal (Pergl et al., 2011)and addressed complex factors determining its invasiveness including genetic relationships with other species in the genus (Jahodová et al., 2007). Recent comprehensive synthesis (Pyšek et al., 2007).
Hypericum spp. (esp. H. perforatum) / Classic studies on rapid evolution (Maron, 2004; Dlugosch & Parker, 2008), evidence for enemy release (Vila et al., 2005), and comprehensive demographic studies(Buckley et al., 2003b; Buckley et al., 2003a).
Impatiens glandulifera (and congeners) / Among the most intensively studied invasive plant species(Pyšek et al., 2008b). Asian species are invasive in riparian and disturbed forest habitat in both North America and Europe (compare entries on Ailanthus, Fallopia, Lonicera, and riparian habitat invaders). Classical studies on latitudinal clines (Kollmann & Banuelos, 2004) and competition for pollinators (Chittka & Schurkens, 2001; Lopezaraiza-Mikel et al., 2007). Recent review on the species (Clements et al., 2008). The genus has both invasive species with different dynamics and history of invasion, and a native species co-occurring in the same habitats provides a suitable model for congeneric comparisons(Skálová et al., 2011; Skálová et al., 2012).
Lantana camara / Among the most intensively studied invasive plant species(Pyšek et al., 2008b); although mostly applied research, with limited work on invasion dynamics. Recent synthesis from South Africa (Vardien et al., 2012) and multi-site study from Australia (Osunkoya et al., 2012). Globally a major invader (Lowe et al., 2000; Kueffer et al., 2010a; Johnson, 2011). A comparable species of disturbed (sub)tropical sites with very wide global distribution is Leucaena leucocephala(Lowe et al., 2000; Kueffer et al., 2010a).
Ligustrum spp. / Eight invasive Ligustrum species from both temperate and tropical climates are known (Richardson & Rejmánek, 2011), which allows for comparison of multiple woody shade-tolerant forest invaders across climate zones. See entry on forest understorey invaders.
Lonicera spp. (esp. L. japonica, L. maackii) / Asian species are invasive in riparian and disturbed forest habitat in both North America and Europe (compare entries on Ailanthus, Fallopia, Impatiens, and riparian habitat invaders). Shade-tolerant forest invader (Martin et al., 2009). See entry on forest understorey invaders.
Lythrum salicaria / Among the most intensively studied invasive plant species(Pyšek et al., 2008b)including impacts (Hulme et al., 2012); and one of the most problematic invaders in North America. Studies on competition for pollinators (Brown & Mitchell, 2001; Brown et al., 2002) and clines in flowering phenology (Montague et al., 2008) invite comparisons with Impatiens. Recent research on genetic constraints on the evolution of flowering phenology (Colautti & Barrett, 2010; Colautti et al., 2010; Colautti & Barrett, 2011) opens new avenues for Lythrum research on specific mechanisms that requires bundling of research efforts. A species used for formulating the EICA hypothesis (Blossey & Nötzold, 1995).
Morella [Myrica] faya / Classical studies on the effect of a nitrogen-fixing woody species in Hawaii on soil properties and ecosystem functioning in succession(Vitousek et al., 1987; Vitousek & Walker, 1989; Asner & Vitousek, 2005). The species isa dominant native species on oceanic islands in Macaronesia, and there is a potential for comparative studies between native and alien populations.
Phalaris spp. (esp. P. arundinacea) / Among the most intensively studied invasive plant species(Pyšek et al., 2008b); and one of the most problematic invaders in North America. Recent comprehensive synthesis (Lavergne & Molofsky, 2004). The species shows increased phenotypic and genetic diversity in invasive populations thanks to novel genetic admixture (Lavergne & Molofsky, 2004; Lavergne & Molofsky, 2007). Recent research on genetic architecture of different native and invasive populations (Calsbeek et al., 2011) holds much promise for in-depth genetic studies and comparisons with similar research on Lythrum.
Phragmites australis / Among the most intensively studied invasive plant species(Pyšek et al., 2008b); and also widely studied in the native range, which allows for comparison of the effects of anthropogenic environmental change on native and alien populations. Its global distribution (Meyerson et al., 2010), introduction history (Hauber et al., 2011), sexual and clonal reproduction strategies (Brisson et al., 2010; Saltonstall et al., 2010), phenotypic plasticity (Mozdzer & Megonigal, 2012), and high genetic diversity within the species (McCormick et al., 2010b; McCormick et al., 2010a; Saltonstall, 2011)make it a suitable model species for investigating the role of genetic determinants of invasiveness (Saltonstall, 2002).Recent synthesis (Mal & Narine, 2004) and in-depth local case study integrating local and scientific knowledge (Bart, 2006).
Prosopis spp. / Considered one of the worst invaders (Lowe et al., 2000), in arid areas (van Klinken & Campbell, 2001)and on oceanic islands (Gallaher & Merlin, 2010; Kueffer et al., 2010a). Research has focused on the role of environmental change (climate, elevated CO2, grazing) in driving Prosopis expansion into savanna habitat both in native and alien ranges(Polley et al., 1994; Archer, 1995). See also entry on woody plant invasions of grasslands. Most invasive populations, at least in Australia and South Africa, are hybrids, and there is much potential for further comparative work on the role of hybridization in invasions in different regions.
Pueraria montana ('Kudzu') / This vine species is considered one of the worst invaders (Lowe et al., 2000), especially in the USA. Recent comprehensive syntheses (Forseth & Innis, 2004; Simberloff, 2011), but given its prominence it is little studied. Like Tamarix (see below) Kudzu has become embedded in local culture in invaded regions and is also an interesting model species for studying cultural aspects of plant invasions (Simberloff, 2011). Its invasion history is well documented (Forseth & Innis, 2004).
Silene latifolia and S. vulgaris / Evidence for evolution of increased competitive ability (EICA) (Blair & Wolfe, 2004; Wolfe et al., 2004; Elzinga & Bernasconi, 2009). Recent phylogenetic comparative study of the genus (Jenkins & Keller, 2012). Of particular interest as a model organism because the genusSilene is emerging as a model system in ecology and evolution beyond plant invasions (Bernasconi et al., 2009).
Solidago spp. (S. canadensis, S. gigantea) / Among the most widespread plant invaders in Europe. Research has addressed a broad range of aspects including molecular biogeography (Schlaepfer et al., 2008a; Schlaepfer et al., 2008b; Schlaepfer et al., 2010), latitudinal clines (Weber & Schmid, 1998), spatiotemporal spread (Weber, 1998; Weber, 2001), demography (Meyer & Schmid, 1999b; Meyer & Schmid, 1999a; Meyer & Schmid, 1999c), evolution of increased competitive ability (EICA) (Jakobs et al., 2004; Meyer et al., 2005), allelopathy (Abhilasha et al., 2008), and impacts (Hulme et al., 2012); e.g. soil impacts (Chapuis-Lardy et al., 2006; Guesewell et al., 2006; Vanderhoeven et al., 2006; Scharfy et al., 2009; Zhang et al., 2009; Scharfy et al., 2010).
Spartina spp. (S. alterniflora, S. anglica, S. maritima) / Among the most intensively studied invasive plant species(Pyšek et al., 2008b). Spartina is in particular an interesting model organism for the study of hybridization and polyploidy in plant invasions involving sophisticated molecular and genetic techniques (e.g. Daehler & Strong, 1997; Ayres et al., 1999; Baumel et al., 2001; Baumel et al., 2002; Salmon et al., 2005; Castillo et al., 2010; Chelaifa et al., 2010a; Chelaifa et al., 2010b), which has recently been reviewed (Ainouche et al., 2009).
Tamarix spp. (esp. T. ramosissima) / Considered one of the most problematic invaders of the USA (Zavaleta, 2000). Long-term data is available to analyse the invasion of the species in the context of changing environmental management and stakeholder perception (Di Tomaso, 1998; Zavaleta, 2000; Shafroth et al., 2005; Harms & Hiebert, 2006; Stromberg et al., 2007; Stromberg et al., 2009; Hultine et al., 2010).
Triadica sebifera / Syn. Sapium sebiferum. Among the most intensively studied invasive plant species(Pyšek et al., 2008b). In-depth studies on induced herbivory defence(Carrillo et al., 2012a; Carrillo et al., 2012b; Wang et al., 2012), and evidence for evolution of increased competitive ability (EICA) (Siemann & Rogers, 2003; Rogers & Siemann, 2004; Zou et al., 2008).
Ulex europaeus / A major invader in many parts of the world (Lowe et al., 2000; Clements et al., 2001; Kueffer et al., 2010a). Recent research has documented phenotypic and genetic variability across populations from the whole native range and multiple areas of introduction (Tarayre et al., 2007; Atlan et al., 2010; Hornoy et al., 2011; Hornoy, 2012). See also entry on woody plant invasions of grasslands.
Verbascum thapsus / One of the globally most widespread plant invaders of mountain ecosystems (McDougall et al., 2011; Seipel et al., 2012) that occurs across broad temperature gradients likely due to high phenotypic plasticity (Parker et al., 2003). It reaches exceptional population densities and plant size in Hawaii (Ansari & Daehler, 2010). Data from multiple sites and along broad climate gradients in both the native and multiple areas of introduction have recently become available (Alba et al., 2011; Alba et al., 2012; Seipel, 2012; Kumschick et al., 2013).
2. GENERA AND FAMILIES
Model group / ExplanationAcacia (sensu lato) / At least 30 species of Acacia (sensu lato) are invasive; some are among the most damaging of all invasive plant species. Research on Australian acacias in particular has shed new light on many aspects of plant invasion ecology, including determinants of invasiveness, factors driving impacts, and on many facets of the human dimensions of plant introductions (Richardson et al., 2011). For a synthesis see Richardson (2011)
Eucalyptus / Given the widespread planting of eucalypts around the world for a century or more, the limited number of invasive species and extent of invasions in this group is enigmatic. For a synthesis see Rejmánek and Richardson(2011)
Oenothera / A genus with specific mechanism of fixation of hybrid genotypes (PTH, permanent translocation heterozygosity) resulting in the existence of a diversity of hybridogenous species in the invaded range in Europe. Hybrids differ in their invasion history and invasiveness, which makes them a suitable model for addressing the role of biological traits in invasion success(Mihulka & Pyšek, 2001; Mihulka et al., 2006).
Pinus / For a synthesis see Richardson (2006)
Populus / Five Populus species are known invaders (Richardson & Rejmánek, 2011). The genus is an emerging model organism in plant research and ecological genetics (Bradshaw et al., 2000; Taylor, 2002; Cronk, 2005; Jansson & Douglas, 2007; Whitham et al., 2008), and especially research on community and ecosystem consequences of within-species genetic variation (‘community and ecosystem genetics’)(Whitham et al., 2008). Such research may form an interesting basis for associated research in invasion science. Of management relevance in particular because of the potential future risks of (genetically-modified) Populus used in forestry and for biofuel production.
Rubus / A genus with an overrepresentation of invasive species (Daehler, 1998; Richardson & Rejmánek, 2011), including both temperate and tropical species allowing for comparative studies across biomes. Rubus species often show also weedy behaviour in the native range, and it is not well established if and when ecological behaviour in the alien range is novel. Clonal growth is an important characteristic of this genus.
Salix / A genus with an overrepresentation of invasive species (Daehler, 1998; Richardson & Rejmánek, 2011). Salix species are also fast-growing, early-successional species in the native range, and it is not well established if and when ecological behaviour in the alien range is novel. Potential future invasion risks as biofuel plant.
Senecio / Large genus of some 1000 species with over 150 introduced species (Randall, 2002), including major invasive species such as S. inaequidens or S. madagascariensis. The Senecio genus may in particular be an interesting model system for processes during the introduction, establishment and spread of unintentionally introduced herbaceous species spreading from small founder populations. A high diversity of breeding systems has been reported for invasive Senecio species including high inbreeding (Roux et al., 2010), self-incompatability (Hiscock, 2000), and hybridization (Lafuma et al., 2003). See entry on small founder populations. More generally Asteraceae as one of the largest plant families with many invasive species is an interesting group for phylogenetically constrained analyses.
Cactaceae / A family that represents species with special functional traits (succulents, CAM photosynthesis). Long history of biological weed control, especially of Opuntia species (Zimmermann et al., 2009). It would be particularly interesting to know whether the overrepresentation of invasive Opuntia species compared to other cactus genera can be explained by human use and introduction history only or whether traits also contribute to differences in invasion success.
Fabaceae / A family with an overrepresentation of invasive species (Daehler, 1998; Richardson & Rejmánek, 2011). In particular systematic comparative studies across species and habitats of impacts on soil nutrient dynamics by nitrogen-fixing invasive plants may be useful.
Iridaceae / A family with many introduced species for horticulture but relatively few invasive species (Van Kleunen et al., 2007). This family has been used for a taxonomically-constrained test of hypotheses explaining invasiveness, including Baker's rule (Van Kleunen et al., 2008), seedling characteristics (Van Kleunen & Johnson, 2007), and human use, taxonomy, and geographic distribution (Van Kleunen et al., 2007).
Lauraceae / The family includes some of the major (sub)tropical woody invasive species, especially in the genera of Cinnamomum and Litsea(Weber, 2003; Richardson & Rejmánek, 2011). Case studies on Cinnamomum verum indicate that nutritious frugivore-dispersed fruits and ability to grow on nutrient-poor soil are important characteristics (Kueffer et al., 2007; Kueffer et al., 2009; Kueffer et al., 2010b), but few studies have been done on invasive species in the family.
Melastomataceae / A species-rich tropical family with an underrepresentation of invasive species (Daehler, 1998; Meyer & Medeiros, 2011; Richardson & Rejmánek, 2011); however harbouring two of the most problematic tropical plant invaders: Clidemia hirta and Miconia calvescens (Kueffer et al., 2010a; Meyer & Medeiros, 2011).
Myrtaceae / Family with an overrepresentation of invasive species (Daehler, 1998), especially in the genera Melaleuca, Psidium, and Syzygium, but also including the genus Eucalyptus with a low proportion of invasive species (see entry). Fleshy frugivore-dispersed fruits, vegetation growth, and for some species shade tolerance seem to be important characteristics of invasive Myrtaceae (Huenneke & Vitousek, 1990; Daehler, 1998; Kueffer et al., 2009; Martin et al., 2009; Schumacher et al., 2009).
Pinaceae / With 30 known invasive species (Richardson & Rejmánek, 2011) (and many more naturalized species) this family has the highest proportion of invasive taxa (13%) of any other large family of trees. Invasiveness has been thoroughly reviewed for the family (Richardson & Rejmánek, 2004) and invasion dynamics are well studied for many species, especially pines (e.g. Richardson, 2006), but there is much scope for further comparative studies to elucidate determinants of invasiveness and management solutions.
Polygonaceae / A family with invasive vines, herbs and shrubs colonizing a broad range of habitats including ruderal sites, stream banks, forests, and mountain ecosystems; many species profit from vegetative growth. See entry on Fallopia.
Proteaceae / A family with many species adapted to very nutrient-poor soil, especially through special traits such as cluster roots (Neumann & Martinoia, 2002). Although intensively traded in horticulture and despite unique functional traits, few species have become invasive (Daehler, 1998; Richardson & Rejmánek, 2011).
3. MODEL ECOSYSTEMS