To establish, a NIPS must colonize a site and develop self-sustaining, expanding populations. Establishment may last longer than colonization and occurs on a slightly larger spatial scale (Fig. 2). At this stage, small subpopulations of individuals may be tightly linked through dispersal (Melbourne et al., 2007). During establishment, biotic filters that constrain the population size of NIPS may be most important, although they will interact with environmental conditions, species traits, and continued propagule pressure from source regions (Table 2). Biotic filters are barriers to invasion created by the actions or presence of living organisms. While biotic filters will not necessarily prevent the germination of seeds or the spread of NIPS, these filters can affect survival, growth, and reproduction.
Traits that enhance competitive performance, reduce niche overlap between NIPS and natives or increase enemy resistance may be most important during establishment (Lloret et al., 2005; Dietz & Edwards, 2006). Species that share similar resource acquisition traits are likely to compete strongly. Conversely, NIPS representing functional groups not present or in low abundance within a new community may encounter less competition with native species, especially in regions with a number of different resources or heterogeneous resource conditions (Lloret et al., 2005; Turnbull et al., 2005; Melbourne et al., 2007). Other advantageous traits include secondary chemical compounds that deter herbivores, ‘novel weapons’, such as root exudates that negatively impact other plants, fast growth, and high fecundity (Rejmanek, 1996; Callaway & Ridenour, 2004; Richardson & Rejmanek, 2004; Dietz & Edwards, 2006). Although specific traits conferring these abilities may vary among habitats, examples of traits that correlate with competitive ability include vegetative reproduction, leaf size, stem height and flowering phenology (Goodwin et al., 1999; Lloret et al., 2005).
i. Plant–plant interactions: competition (–), novel weapons (–), and facilitation (+) Competition is likely the best studied of the biotic filters of invasion, although this filter alone appears unlikely to fully exclude invasive plant species (Levine et al., 2004). Competition or, more specifically, exploitation competition occurs at local scales when plants reduce the growth of their neighbors by consuming resources. Because invasive NIPS are generally most successful in areas with high resource availability (Dukes & Mooney, 1999; Davis et al., 2000; but see Funk & Vitousek, 2007), competition undoubtedly reduces the size, density, and impact of many NIPS. In some instances a single, strongly competitive species may slow the growth of an NIPS by reducing availability of a limiting resource. In other cases a suite of species may collectively reduce the availability of critical resources to levels that suppress growth of the NIPS. This latter scenario, along with growing recognition of the pace of global biodiversity loss, has given rise to dozens of studies examining the role of plant community diversity in determining invasibility (e.g. Knops et al., 1999; Levine, 2000; Naeem et al., 2000; Dukes, 2001; Hector et al., 2001; Kennedy et al., 2002; Fargione et al., 2003; van Ruijven et al., 2003; Fargione & Tilman, 2005).
Taken together, results of these neighborhood-scale diversity–invasibility studies suggest that diverse plant communities often (but not always) provide greater competitive resistance to NIPS (Hooper et al., 2005). So, does resistance result from niche complementarity or reduced resource overlap (i.e. many species with different resource requirements collectively reducing the perceived availability of resources for the invader)? Or are diverse communities resistant to invasion simply because they are more likely to include the species that most strongly compete with a suite of NIPS (i.e. the much-discussed ‘sampling effect’ of the biodiversity literature) (Hooper et al., 2005)? While many early studies were unable to address this question (Wardle, 2001), it now seems that the answer may be: both.
Recent studies suggest three nonexclusive patterns of competition. (1) In some systems, growth of invasive species can be suppressed by species that are morphologically, phenologically, and physiologically similar, that is, species of the same functional type (e.g. Dukes, 2001; Fargione et al., 2003; van Ruijven et al., 2003). (2) In other cases (and even in some of the same systems), a single dominant species or functional group can most strongly suppress all or most invaders (Symstad, 2000; Fargione et al., 2003). (3) Finally, in some systems, an assemblage of species with different traits can compete more strongly with an invader than any one species alone (Fargione & Tilman, 2005; Milbau et al., 2005; Losure et al., 2007). Thus, niche complementarity among residents can contribute to a community's biotic resistance to invasion in cases where a single resident species is unlikely to out-compete the invader. The degree to which complementarity (and thus species diversity) plays a role in determining invasibility may be influenced by resource availability of a site, with more fertile sites being more prone to the influence of dominant species. In some cases, losses of even the least abundant native species can markedly increase the invasibility of resident communities (Lyons & Schwartz, 2001; Zavaleta & Hulvey, 2004). The critical variable in the diversity–invasibility relationship is likely to be whether the species that are lost contribute to lowering the availability of a limiting resource below some threshold level at a sensitive time for the invasive species (Davis & Pelsor, 2001). For example, in systems with a strong temporal component to resource availability (e.g. water in Mediterranean-climate systems), there may be greater opportunity for rare species to affect resource availability at these sensitive times (e.g. Dukes, 2001; Zavaleta & Hulvey, 2004).
Negative interactions between NIPS and native plants may also result from NIPS with novel weapons. Some NIPS have biochemical root exudates that act as allelopathic agents or alter plant–soil microbial interactions in the introduced range (Callaway & Ridenour, 2004). One mechanism through which NIPS root exudates can negatively impact native plants is through the disruption of beneficial relationships between native plants and soil biota. In forests of the northeastern USA, Allaria petiolata, an herbaceous mustard species, contains a type of phytotoxic glucosinolate that appears to disrupt the mutualism between arbuscular mycorrhizal fungi and hardwood canopy trees. Because the success of these juvenile hardwoods depends on the association with arbuscular mycorrhizal fungi, the invasion of A. petiolata results in tree mortality that favors further success of this invader because of reduced competition with tree species (Stinson et al., 2006).
Resident species do not always suppress growth of NIPS, and sometimes contribute to their success. Facilitation is less studied in invasion biology and perhaps generally in ecology, although recent studies suggest that it may be an important local regulator of community assembly (but see Prieur-Richard et al., 2000; Bruno et al., 2003). Facilitative relationships are most commonly observed in harsher abiotic environments where neighboring plants ameliorate microclimatic stressors (Bruno et al., 2005; Brooker, 2006), but facilitation is not limited to these environments. Smith et al. (2004) found that native dominants increased seedling establishment of the invasive Melilotus officinalis in a relatively productive North American grassland. Additionally, certain invasive species may facilitate the success of other invaders, leading to invasional meltdown (Simberloff & Von Holle, 1999). For example, invasions of nitrogen fixers into communities without native nitrogen fixers can increase the pool of soil nitrogen (Vitousek & Walker, 1989; Hughes & Denslow, 2005), facilitating the invasion of other NIPS previously limited by nitrogen availability (Yelenik et al., 2004).
ii. Interactions with other trophic levels Herbivores, parasites, pathogens, mutualistic soil biota, pollinators, and dispersal agents also influence NIPS establishment. Escape from herbivory or disease may increase growth rates, and the chance of establishment in a new region. The enemy release hypothesis (ERH) suggests that NIPS benefit from transport outside the range of their natural enemies (Elton, 1958; Maron & Vila, 2001; Keane & Crawley, 2002; Carpenter & Cappuccino, 2005). Building on the ERH, the evolution of increased competitive ability (EICA) hypothesis (Blossey & Notzold, 1995) may also explain disproportionate success of invasive plants in new ranges. The EICA hypothesis suggests that, under reduced enemy pressure, selection may shift the resource allocation of NIPS from enemy defense to faster growth (Blossey & Notzold, 1995). Greater enemy pressure on native species should shift the competitive balance to favor NIPS (Keane & Crawley, 2002; Blumenthal, 2006).
There are mixed results for both the ERH and the EICA hypothesis (Keane & Crawley, 2002; Daehler, 2003). Studies show that some NIPS have longer life-spans, grow larger, and achieve higher reproduction in invaded ranges than in native ranges (Daehler, 2003; Leger & Rice, 2003). However, these studies have not always found mechanistic explanations linking increased NIPS growth to herbivory (Keane & Crawley, 2002). Covarying factors such as competition (Leger & Rice, 2003) and resource availability (Blumenthal, 2006) may also complicate predictions of the relative importance of herbivory. The Resource–ERH (Blumenthal, 2006) suggests that enemy release in combination with areas of high resource availability increases the success of fast-growing, ‘high resource use’ NIPS in novel environments (Fig. 4).
Figure 4. The resource–enemy release hypothesis (Blumenthal, 2006) suggests that nonindigenous plant species (NIPS) that require the most resources for growth will benefit most from enemy release in their introduced range. (a) Enemy regulation may be highest for high-resource-use species in their native range. (b) In an introduced range, high-resource-use species may have greater potential to increase growth in response to enemy release (solid line) relative to native competition (dashed line). Low-resource-use NIPS will be less influenced overall. Figure redrawn from Blumenthal (2006).
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Herbivores also influence interactions between NIPS and the native plant community. For instance, intense grazing by introduced ungulates can increase the invasibility of native plant communities (D’Antonio et al., 2000). In a meta-analysis of 63 studies, Parker et al. (2006) found that native generalist herbivores suppressed introduced plants more than they suppressed natives, while native specialist herbivores did not suppress NIPS. Introduced generalist herbivores facilitated NIPS through their negative impact on natives. These results suggest that novel pressure from generalist herbivores may be an important line of defense against NIPS, but, in ecosystems heavily invaded by nonnative herbivores, native plants may also suffer from novel herbivore damage. Specialist enemies that switch from native hosts to NIPS, or that accompany NIPS from other regions, can limit the degree of enemy release. Although rare, host-switching has been observed among native and NIPS congeners (Creed & Sheldon, 1995).
Plant–soil feedbacks can strongly regulate the diversity and productivity of plant communities and affect NIPS success. Plant–soil interactions may be positive or negative, although negative feedbacks are most common (Reinhart & Callaway, 2006). Negative feedback is driven by soil pathogens, herbivores and parasites. These organisms reduce plant growth, provide density regulation and maintain higher degrees of diversity within plant communities. Positive feedback results from the presence of mycorrhizal fungi, nitrogen-fixing bacteria and other beneficial soil biota. Positive feedback may disproportionately facilitate the success of some species over others (Reinhart & Callaway, 2006). In general, interactions between native plants and soil communities tend to be negative, while positive feedbacks often occur between NIPS and soil biota in their introduced range (Klironomos, 2002).
Altered relationships and feedback with soil biota in the introduced vs native range may partially explain why some NIPS are so successful. Several studies have demonstrated that soil communities favor NIPS over native species (Reinhart et al., 2003, 2005; Callaway et al., 2004; Wolfe & Klironomos, 2005). In a California grassland, Klironomos (2002) found that four out of five nonnative species experienced positive soil feedbacks, while all five rare native plants experienced negative feedback. Reinhart et al. (2003) found that invasion of Prunus serotina (black cherry) was facilitated by soil communities of north-western Europe, while soil communities in the native range of the species inhibited its survival and growth. Reinhart & Callaway (2006) recently reviewed available biogeographical comparison studies investigating the effect of soil biota on NIPS in native and nonnative ranges. In all six studies the direction of soil–plant feedback was strongly negative in the native ranges of the NIPS. In the introduced ranges, feedback was strongly negative in only one case.
NIPS can directly affect the structure and function of soil biota (Wolfe & Klironomos, 2005), with a variety of consequences. In some cases, NIPS form novel mutualisms, increasing establishment success and changing the availability of soil nutrients (Richardson et al., 2000a; Callaway et al., 2004). For example, many NIPS increase soil nitrogen by forming associations with native nitrogen-fixing bacteria (Richardson et al., 2000a; Callaway et al., 2004). Increases in soil nitrogen resulting from these mutualisms may change native community structure and increase the success of future NIPS invasions (Vitousek et al., 1987; Vitousek & Walker, 1989; Yelenik et al., 2004). In other cases, NIPS may alter the prevalence of disease in a community. In a model with field-estimated parameters, Borer et al. (2007) showed that invasive annual grasses in California may increase the presence of generalist viral pathogens in native perennial communities. Annual grasses are inferior competitors in this system, but they may be able to successfully invade in part because of the negative effect of increased viral pathogens on native perennial grasses. Finally, as already discussed, NIPS may have biochemical exudates that act as ‘novel weapons’ and may disrupt beneficial mutualisms between native plants and soil fungi (Stinson et al., 2006).
Mutualisms with pollinators and seed dispersal agents in the introduced region are also necessary to ensure establishment of some NIPS (Richardson et al., 2000a), although seed dispersal agents are most important during spread. It is unlikely that plants with very tightly coevolved pollinator or disperser mutualisms will find replacements in their introduced range. Plants that are pollinated by generalists, display vegetative reproduction or are self-compatible may have significant advantages (Richardson et al., 2000a). Competition for pollination, similar to competition for resources, may occur between natives and NIPS (Brown & Mitchell, 2001). Showy NIPS may draw pollinators away from native species, reducing pollen quantity and seed set. Alternatively, these NIPS may attract more pollinators to natives, facilitating increased pollination (Brown et al., 2002).
iii. Lag phase A lag phase often takes place between establishment and spread, when small populations of established NIPS adapt to their new community. This phase may correspond to a lack of genetic variation, which prevents rapid adaptation to novel conditions, or the time necessary for the population to reach a threshold size that allows it to spread (Sakai et al., 2001; Barney, 2006). Lag time may also reflect a lack of suitable local habitat, inclement environmental conditions, or a statistical artifact (Pysek & Hulme, 2005). During this period, multiple introductions, range expansion and migration of NIPS, and gene flow between populations of establishing NIPS may decrease the time spent in the lag phase (Sakai et al., 2001; Lavergne & Molofsky, 2007). Rapid evolution can sometimes produce new genotypes capable of surviving in different climates, competing more successfully with native species, or deterring enemies (Lee, 2002). For example, Abultilon theophrasti (velvetleaf) was originally introduced before 1700 in the USA. This species has only recently become an aggressive invader as a result of the evolution of different life-history strategies based on the nature of competition in its new environment (Weinig, 2000; cited in Lee, 2002).