Assessing Vulnerability to Invasion

The two instances in which the native community experienced a significant decline, while invasive plants benefited significantly, were studies in which propagule availability and lack of biotic resistance (or higher competitive ability of the invasive plants) were identified as the drivers of vulnerability to invasion (Figure 1). In all other cases, the native community response to the invasion was neutral or positive (i.e., under herbivory; Figure 1). There were also several instances of native and invasive performances differing, with an overall pattern of higher effects sizes among invasive plants (Figure 1).

Figure 1. Results for the analysis of invasive and native plant performance or community assessment (effect size [ES] mean + 95% credible interval [CI]), as a function of drivers of vulnerability (darker bars) and their subcategories (white and light gray bars). CIs that do not overlap with zero are considered statistically significant. An asterisk indicates invasive and native species ES 95% CIs do not overlap but are of the same sign (i.e., same direction of change). Two asterisks indicate invasive and native species ES 95% CIs do not overlap and are of different sign (i.e., opposite direction of change). Numbers denote number of observations included.

In the field of biological invasions, propagule availability refers to both the number of propagules and the rate of arrival (Simberloff Reference Simberloff2009). High propagule pressure from introduced species has been strongly associated with their spread and abundance (e.g., Catford et al. Reference Catford, Vesk, White and Wintle2011; Ibáñez et al. Reference Ibáñez, Silander, Allen, Treanor and Wilson2009). Our results link higher levels of invasive propagules to a reduction in native plant performance and thus to higher native plant community vulnerability to invasion (Figure 1). Furthermore, these results could simultaneously reflect low native seed abundance (Schuster et al. Reference Schuster, Wragg and Reich2018; Vilà and Ibáñez Reference Vilà and Ibáñez2011; von Holle and Simberloff Reference von Holle and Simberloff2005). This finding underscores the importance of legacy (what is left) and priority (what arrives first) effects during plant establishment, particularly after disturbance (Corbin and D’Antonio Reference Corbin and D’Antonio2012; Uricchio et al. Reference Uricchio, Daws, Spear and Mordecai2019). If invasive propagules are the most abundant, any removal of vegetation will likely result in reinvasion (Pearson et al. Reference Pearson, Ortega, Runyon and Butler2016; Prior et al. Reference Prior, Adams, Klepzig and Hulcr2018). Thus, management practices that decrease invasive propagules (e.g., removal before seeding), while at the same time increasing native propagules (e.g., via seeding or planting), may have particularly successful results (Reinhardt Adams and Galatowitsch Reference Reinhardt Adams and Galatowitsch2008).

Lack of biotic resistance or high competitive ability of invasive plants is frequently associated with successful invasions (Carboni et al. Reference Carboni, Calderon-Sanou, Pollock, Violle, DivGrass and Thuiller2018; Vilà and Weiner Reference Vilà and Weiner2004). Numerous studies have documented a variety of plant traits conferring invasive plants an advantage over the invaded native communities. For example, high total and specific leaf area (Allred et al. Reference Allred, Fuhlendorf, Monaco and Will2010), high germination rates (Deschenes et al. Reference Deschenes, Caubel and Sirois2019), specific mechanism of nitrogen acquisition (Laungani and Knops Reference Laungani and Knops2009), and chemical inhibition of native plant photosynthesis (Musil et al. Reference Musil, Arnolds, van Heerden and Kgope2009) have all, among others, been identified as features of invasive plants contributing to their invasion success. Also, competition for space and resources during recruitment or the production of allelochemicals by invasive plants may prevent native species from growing populations that could resist the invasion (e.g., Edwards et al. Reference Edwards, Schlesinger, Ooi, French and Gooden2019; Esch et al. Reference Esch, Ashbacher, Kopp and Cleland2018; Grove et al. Reference Grove, Haubensak, Gehring and Parker2017).

Still, high invasive competitive ability is not only a function of the invasive itself, but is usually associated with particular features of the ecosystem (Daehler Reference Daehler2003; Metlen et al. Reference Metlen, Aschehoug and Callaway2012); which, if managed, could confer the native community a higher level of resistance to the invasion (Byun et al. Reference Byun, de Blois and Brisson2018). High resource ability and/or low enemy pressure are conditions under which invasive plants become highly competitive (Blumenthal Reference Blumenthal2006; Burns et al. Reference Burns, Halpern and Winn2007; Garcia-Serrano et al. Reference Garcia-Serrano, Sans and Escarre2007). Our review showed that under these conditions, native plants tended to underperform compared with invasive species: native plants marginally benefited from enemy release and from changes in resources, while invasive plants strongly benefited from both increases and decreases of resources and lack of enemies (Figure 1).

After the enemy release hypothesis was formulated as a main mechanism of invasion success (Keane and Crawley Reference Keane and Crawley2002), several studies questioned its relevance (Agrawal and Kotanen Reference Agrawal and Kotanen2003; Beckstead and Parker Reference Beckstead and Parker2003; Colautti et al. Reference Colautti, Ricciardi, Grigorovich and MacIsaac2004; Maron and Vilà Reference Maron and Vilà2001). Our results show that with respect to herbivory, the category for which we have more observations, invasive species strongly benefited from absence of herbivory, while native plant response was neutral (although invasive and native performances were not significantly different). This might be an indication of overall higher palatability among invasive plants, as acquisitive and fast-growing traits are associated with lower plant defenses (Blossey and Nötzold Reference Blossey and Notzold1995; Blumenthal et al. Reference Blumenthal, Mitchell, Pyšek and Jarošík2009). Thus, successful invasive species control might involve managing herbivores, for example, by providing access or shelter.

Fluctuation of resources has also been postulated as a major mechanism underlying biological invasions (Davis et al. Reference Davis, Grime and Thompson2000). Our analysis shows that changes in resources were strongly associated with higher invasive performance, while native plants varied in their response (Figure 1). Although the sample sizes for native species are low in some of these comparisons, native plants were significantly outperformed by invasive plants in instances of decreasing water and of increasing light and nutrients (Figure 1; note there were no observations of native responses to water increase). Increases in light have often been identified as a major driver of invasive plant establishment (e.g., Huebner et al. Reference Huebner, Regula and McGill2018), even if the abundance of other resources also promotes native plants (Knight et al. Reference Knight, Oleksyn, Jagodzinski, Reich and Kasprowicz2008). Traits that lead to rapid growth (e.g., high specific leaf area and leaf nutrient content) are most advantageous under high light conditions, and these traits are common among invasive plants (Allred et al. Reference Allred, Fuhlendorf, Monaco and Will2010; van Kleunen et al. Reference van Kleunen, Weber and Fischer2010; Vilà and Weiner Reference Vilà and Weiner2004). In contrast, there were also a few instances in which a decrease in resources (i.e., water) favored invasive plants over natives (Figure 1), but we lack enough data to generalize as to when this is the case. Together, these results underscore the importance of managing available resources to avoid situations that favor invasive species, for example, maintain resource levels within their natural range of variability.

Vulnerability to Invasion across Metrics, Vegetation Types, and Biomes

Performance and impact of invasive plants were assessed with different metrics across our review. Abundance and biomass were the two most common measurements of invasive performance (68%), while richness and abundance were the prevalent metrics across native communities (45%; Figure 2). When assessing the impact of plant invasions through the lens of the native community, the two metrics that strongly differentiated invasive and native plants were abundance (e.g., cover, density) and richness (i.e., number of species) (Figure 2). Other metrics (i.e., growth, recruitment, survival) were quite variable among native plants (also note the low number of observations). Differences in native biomass between sites with low and high invasions were of the same magnitude as those for invasive species (Figure 2).

Figure 2. Results for the analysis of plant performance or community assessment (effect size [ES] mean + 95% credible interval [CI]), invasive and native, as a function of metric used. CIs that do not overlap with zero are considered statistically significant. Asterisks indicate invasive and native species ES 95% CIs do not overlap and are of different sign (i.e., opposite direction of change). Numbers denote number of observations included.

These results might indicate that invasive impact on the native community is exerted at the population level through higher density of individuals (or higher cover). Of course, changes in population density come through changes in recruitment, growth, and survival (Harper Reference Harper1977). In our review, we had very few observations in these categories, showing a wide range of responses, which might explain the lack of significant differences. Biomass, for which we had a higher number of observations, is a common metric used in experimental work. Our results indicate that biomass may not be a good measure of native community vulnerability to invasions; that is, on an individual basis, native plants accumulate as much biomass as invasive, plants but at the population level (abundance or fecundity) their performances differ (Figure 2), indicating that invasion success may be more complex than just straight competition for resources (Daehler Reference Daehler2003; Maron and Vilà Reference Maron and Vilà2001).

Our results also corroborate other studies that document a decrease in native plant species in communities that are being invaded by introduced plants (e.g., Linders et al. Reference Linders, Schaffner, Eschen, Abebe, Choge, Nigatu, Mbaabu, Shiferaw and Allan2019; Powell et al. Reference Powell, Chase and Knight2013). Still, there was no correlation (not shown) between number of native species and the size of the effect, contradicting many studies that have found higher levels of invasion in richer native communities (Aguiar et al. Reference Aguiar, Ferreira and Albuquerque2006). Several studies have associated high native diversity with high levels of invasion (e.g., Long et al. Reference Long, Trussell and Elliman2009; Peng et al. Reference Peng, Kinlock, Gurevitch and Peng2019; Stohlgren et al. Reference Stohlgren, Binkley, Chong, Kalkhan, Schell, Bull, Otsuki, Newman, Bashkin and Son1999, Reference Stohlgren, Barnett and Kartesz2003), but such comparisons between systems with inherently high or low levels of diversity make it very difficult to assess the actual effect of invasions on native diversity. Here, our comparisons were done for the same ecosystem, with the only difference being the degree of invasion, and indicated a strong decline in native richness under invasion.

Our assessment of how native plant communities perform under invasion across vegetation types and biomes is limited by the number of observations (Figure 3); thus, we are cautious not to overinterpret our results. Only Mediterranean and temperate communities were well represented, although not for all mechanisms of vulnerability (Figure 3A). In boreal and temperate areas, native plants seem to fare well under invasions, with natives outperforming invasive plants in temperate areas when disturbance was the mechanism driving the invasion. Still, invasive plants showed higher performance under all other drivers. Tropical and Mediterranean native vegetation tended to experience a considerable drop in performance under high levels of invasive plants (Figure 3A). When looking across vegetation types represented in the data, differences between the native and invasive communities become more significant (Figure 3B). Most of the data came from forests and grasslands, which drove the trends discussed above: native species performance was positive under invasion except when lack of biotic resistance or propagule availability were the drivers of vulnerability (Figure 3B). The only vegetation type diverging from the overall trend was wetlands. Disturbance had a strong detrimental effect on wetland natives, while the effect was positive on natives in all other vegetation types (Figure 3B). Wetland habitats are highly susceptible to invasion (Sobrino et al. Reference Sobrino, Sanz-Elorza, Dana and González-Moreno2002), they act as “landscape sinks” of residuals, that is, areas where loose soil and plant material from other systems accumulate, and under disturbance, alterations in their hydrology and nutrient levels create conditions for invasive plants to succeed (Zedler and Kercher Reference Zedler and Kercher2004). Surprisingly, in this vegetation type, invasions attributed to lack of biotic resistance were not associated with lower native performance, as was the case in all other vegetation types (Figure 3B). Because most of these observations, 9 out of 12, were related to species richness, information on other native performance metrics might result in a different outcome.

Figure 3. Effect sizes (ES) on invasive and native plant performance/community assessment across drivers of vulnerability by biome (A) and vegetation type (B). Credible intervals (CI) that do not overlap with zero are considered statistically significant. An asterisk indicates invasive and native species ES 95% CIs do not overlap but are of the same sign (i.e., same direction of change). Two asterisks indicate invasive and native species ES 95% CIs do not overlap and are of different sign (i.e., opposite direction of change). Numbers denote number of observations included.

Disturbance and Vulnerability to Plant Invasion

Disturbances—natural, anthropogenic, or as result of management—are common among plant communities and in many cases provide optimal conditions for invasive species establishment and spread (Jauni et al. Reference Jauni, Gripenberg and Ramula2015; Lembrechts et al. Reference Lembrechts, Pauchard, Lenoir, Nuñez, Geron, Ven, Bravo-Monasterio, Teneb, Nijs and Milbau2016). Resource fluctuations usually follow disturbances (Jentsch and White Reference Jentsch and White2019); then, species better adapted to rapidly use those resources, like many invasive plants, are likely to outcompete later arrivals (Dickson et al Reference Dickson, Hopwood and Wilsey2012; Radford Reference Radford2013). As a result, native community capacity to respond to a disturbance will largely determine its vulnerability to invasion.

In this analysis, we found mostly neutral to positive responses of native plants to disturbance. Natives were only outperformed by invasive species when disturbance was caused by human activities (e.g., pollution, edge effect, trampling, hiking; Figure 1). However, our meta-analysis included observations wherein the lack of disturbance was associated with higher dominance of invasives (16% of the records). Thus, to better assess the role of disturbance in invasion, we specifically compared plant performance of native and invasive plants in communities that had experience a disturbance event (Figure 4). Overall, plant performance after disturbance was quite variable and tended to be positive for both invasive and native plants (Figure 4). Our assessment of the effect of disturbance on plant species performance was based only on the publications selected specifically to address questions of vulnerability and resistance to invasion. Our search terms were not targeted to select all papers that report disturbances, or their lack, during invasions. Thus, our results and discussion are limited to this search.

Figure 4. Effect of disturbance in invasive and native plant performance/community assessment for each disturbance type (darker bars) and subcategories (lighter bars). Credible intervals (CI) that do not overlap with zero are considered statistically significant. Asterisks indicate invasive and native species ES 95% CIs do not overlap and are of different sign (i.e., opposite direction of change). Numbers denote number of observations included.

In the case of fire, we only had observations for native plants for human-initiated burns (e.g., prescribed burns), none from wildfire. Here, native species tended to have a negative response to burning, although this was not statistically significant. We found a similar trend when the disturbance was removal of vegetation via thinning. Both burning and removal of vegetation (by using herbicides, cutting, hand pulling) are the most common invasive plant removal management practices (Kettenring and Reinhart Adams Reference Kettenring and Reinhardt Adams2011). However, as our results show, these practices could have unintended consequences for the native community. Extensive use of herbicides to reduce invasive plants, for example, can negatively affect native plants as well (Flory and Clay Reference Flory and Clay2009; Rinella et al. Reference Rinella, Maxwell, Fay, Weaver and Sheley2009). Removal without further management may result in profound changes to the ecosystem that the native community is not adapted to handle (Zavaleta et al. 2001). Furthermore, because removal of vegetation is a disturbance on its own, this practice may only be effective in reducing invasions if natives are not affected and the availability of invader propagules is low (Firn et al. Reference Firn, Rout, Possingham and Buckley2008). Only disturbances that promote native plants will be associated with resistance to invasion (Chance et al. Reference Chance, McCollum, Street, Strickland and Lashley2019).

Recommendations

Risk assessments of plant invasions rarely account for native plant performance (Daehler Reference Daehler2003; Maron and Vilà Reference Maron and Vilà2001); but this information could provide additional insights for management aimed at decreasing vulnerability, or increasing resistance, to plant invasions. Informed by results from our analyses, we have developed four key recommendations that could be followed to minimize vulnerability to plant invasions:

1. 1. Assess and implement management that reduces propagule availability of invasives and/or promotes priority effects of natives. If invasive propagule availability is high, avoid any disturbance or management operation that promotes plant establishment (e.g., removal of vegetation if most available seeds and resprouts are invasive). If removal takes place, ensure competitive native propagules are available or carry out native reseeding with a diversity of functional groups (e.g., fast- and slow-growing native plants) (Byun et al. Reference Byun, de Blois and Brisson2013; Leffler et al Reference Leffler, Leonard, James and Monaco2014). A diversity of functional groups will help stabilize the community and provide long-lasting resistance to invasion (Byun et al. Reference Byun, de Blois and Brisson2018; Coutinho et al. Reference Coutinho, Alves, Sampaio, Schmidt and Vieira2019).

2. 2. Because fluctuation of resources, particularly increases in resources, benefit invasive plants more than natives, avoid management practices (or mitigate conditions) that increase plant resources (mainly light and nutrients). For example, avoid opening or clearing the canopy to maintain a relatively low light level, and assess nutrient sources, mostly nitrogen, from any nearby sources (e.g., fertilizers, animal operations, industrial activities).

3. 3. Carry out a careful assessment of potential effects on both the invasive and native plant communities when planning to implement any type of management practice that might disturb the system (Rinella et al. Reference Rinella, Maxwell, Fay, Weaver and Sheley2009). Consider decoupling management from environmental conditions (such as resource availability) that might facilitate reinvasion (Gabler and Siemann Reference Gabler and Siemann2013). Removal and reduction of disturbance, in particular anthropogenic disturbances, including management-caused disturbances, might be the best strategy to reduce/prevent invasion in cases with high invasive propagule pressure or lack of native plants capable of responding to resource availability. For example, a floral inventory of the native community may help to determine the diversity and availability of functional groups that can rapidly establish after the removal of invasive species.

4. 4. In post-management monitoring, consider assessing native community recovery rates and compare them with those of invasive plants. Identifying poor native recovery early on, before invasive plants dominate, will be critical for considering follow-up interventions.