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Invasive species can often transform their new communities, and many theories have been proposed to explain their success in the new range (Catford et al., 2009). Many of these theories posit that invaders gain some ecological advantage because of their evolutionary novelty (Callaway & Ridenour, 2004; Hallett, 2006). For example, a lack of coevolutionary history with the native herbivores or pathogens could lead to enemy release (Keane & Crawley, 2002), or the allelochemicals produced by an invasive plant species may be especially toxic to naive native plants (Callaway & Ridenour, 2004).
For many invasive plants, their evolutionary novelty can lead to altered interactions with diverse soil microbial communities. Soil microbial communities can play an important role in driving plant invasions (Callaway et al., 2004; Wolfe & Klironomos, 2005). In many cases, this occurs because the invasive plant changes soil communities in a way that promotes its own growth while inhibiting the growth of native species (Klironomos, 2002). This can be driven by the lack of soil pathogens in the new range (Reinhart et al., 2003, 2005; Blumenthal et al., 2009), the preferential build up of microbial species pathogenic to native plants (Mangla et al., 2008; Beckstead et al., 2010), or the inhibition of species mutualistic with native plants (Stinson et al., 2006; Vogelsang & Bever, 2009).
Altered soil microbial interactions have been suggested to partly underlie the invasion of Alliaria petiolata (garlic mustard) into forest understories throughout eastern North America (Rodgers et al., 2008a). Like most members of the mustard family, this species does not form connections with mycorrhizal fungi, while most of its native competitors benefit from mycorrhizal associations in which certain soil fungi aid plants in nutrient uptake in exchange for fixed carbon. Alliaria petiolata produces a suite of potential allelochemicals, many of which are unique to the species or novel to its new range. These chemicals have been shown to have toxic effects on mycorrhizal fungi (Roberts & Anderson, 2001; Stinson et al., 2006; Burke, 2008; Wolfe et al., 2008). Invasions of A. petiolata may also affect soil microbial communities through more generalized effects on biogeochemical cycles (Rodgers et al., 2008b) or plant diversity (Stinson et al., 2007). By reducing the diversity or abundance of mycorrhizal fungal species, A. petiolata could gain a competitive advantage against native plant species dependent on the mutualism.
The antimycorrhizal action of A. petiolata may be partly a consequence of the evolutionary naivety of fungi in the introduced range, since secondary chemicals of A. petiolata are more toxic to North American vs European arbuscular mycorrhizal fungal (AMF) species (Callaway et al. 2008). Thus, A. petiolata’s allelochemicals may act as a ‘novel weapon’ because of the mismatch of evolutionary histories between the invader and the native fungi. This also suggests that European AMF have evolved some resistance to these compounds and raises the possibility that, given sufficient time, such resistance could evolve in North American species.
If an invader gains an ecological advantage because of its evolutionary novelty, one would predict that invaders with strong impacts would exert pressure on native communities to shift in composition, and on native populations to adapt, in response to these novel traits (Callaway et al., 2005; Carroll et al., 2005; Lau, 2006; Strauss et al., 2006). Depending on the outcome of these ecological and evolutionary responses, this could lead to a reduction in the invader’s ecological advantage. Such a process could lead to ‘boom-and-bust’ invasion dynamics, as have been observed for some invaders (Simberloff & Gibbons, 2004). For example, while many invasive plants benefit from a release from herbivore pressure, some invaders have been found to gradually accumulate herbivores in their native range over time (Strong et al., 1977; Siemann et al., 2006). While the impact of invasive plants on soil communities has been well documented, it is unclear whether these communities will also develop resistance to invaders as herbivore communities have done. Community-level resistance could arise via ecological changes, as sensitive taxa are replaced by more resistant ones, or via evolutionary ones, as resistance traits within populations rise in frequency.
The novel traits of the invader may themselves evolve during the invasion. This evolution may also reduce the impact of the invader, if invaders evolve reduced investment to the novel traits once they have come to dominate an area. Recent research found that A. petiolata populations may evolve lower allelochemical concentrations over time (Lankau et al., 2009), and genotypes with lower concentrations have weaker impacts on soil communities (Lankau, 2010b) [Correction added after online publication 28 October 2010: in the preceding citation, Lankau, in press was corrected to Lankau, 2010b]. This decline in allelochemical concentration may reduce the impact exerted on the soil community, allowing the re-establishment of sensitive species or strains.
Here I compared the microbial communities in soils from sites across a gradient of invasion history with A. petiolata. I used these communities to answer two questions:
I specifically looked for evidence of species sorting (a continuous loss of richness and community similarity over time) and recovery (a rise in richness or similarity with increasing age). I predicted that soil communities with a longer history with A. petiolata should be more resistant to additional exposure to A. petiolata. However, it is also possible that recovery of sensitive taxa in older, less toxic A. petiolata populations could lead to decreased resistance in the oldest sites.
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- Materials and Methods
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Invasive species often gain ecological advantages because of their novelty in a system, leading to altered interactions with native competitors, herbivores and soil communities (Hallett, 2006). However, relatively little is known about the long-term stability of these novel advantages. The ecological impact of the invader could decrease over time if native communities develop resistance to the novel traits of the invader. In addition, evolution in the invader may act to reduce investment to its novel traits. Previous research found that A. petiolata populations tended to evolve reduced investment into allelochemicals over time (Lankau et al., 2009). The reduction in allelochemical concentrations led to weaker impacts on soil microbial communities (Lankau, 2010b) [Correction added after online publication 28 October 2010: in the preceding citation, Lankau, in press was corrected to Lankau, 2010b]. This evolutionary decline in invader impact could potentially allow native microbial communities to recover over long enough time-scales. In this study bacterial, fungal and arbuscular mycorrhizal fungal communities showed both increasing resistance and recovery over a gradient of history with the invasive A. petiolata.
Soil microbial communities collected along a gradient of invasion history showed a complex pattern in which richness and composition progressively changed with longer associations with the invader up to a point, but then appeared to recover in the oldest sites. This is consistent with an initial phase of species sorting, in which microbial species sensitive to the impacts of A. petiolata are progressively lost from communities over time. However, over long enough time-scales, a sufficient decrease in the soil impacts of the A. petiolata population may allow the return of some of these sensitive taxa. This would explain the high richness of the oldest sites, as well as the high compositional similarity of the oldest and youngest sites. This hypothesis was further supported by the analysis of ‘sensitive’ and ‘resistant’ taxa, which found that ‘sensitive’ taxa tended to be common in the youngest sites, declined in abundance with increasing site age, but then rose again in the oldest sites. These results were surprisingly consistent among bacterial, general fungal, and arbuscular mycorrhizal fungal communities and the different metrics of community structure, despite the wide range of diversities and resolution between the groups.
If an invasive plant exerted a constant selection pressure on native species, one would expect resistance to develop through time, such that native communities with a longer association with the invader should show greater resistance to that invader’s effects. However, if the impact of the invader also varied temporally, then the level of resistance in the native community may track the impact of the invader rather than show a progressive increase. In this study, communities showed increasing resistance over time to a point, but then reduced resistance in the oldest sites for some taxa and resistance metrics. Resistance was measured by the degree of change in either taxa richness or community composition between initial samples and the resulting communities after 3 months of growth with A. petiolata individuals from a common, highly allelopathic population. Youngest and oldest communities tended to have the largest decrease in taxa richness – likely the result of the greater number of sensitive taxa in these communities. Samples with intermediate invasion histories, and lower initial richness, were already depauperate in sensitive taxa, and thus showed less change following additional exposure to a highly allelopathic A. petiolata individual. Again, this pattern was consistent across all three taxonomic groups.
The compositional resistance of a community also varied with the history of association with A. petiolata, but in this case the patterns were not consistent among the taxonomic groups. For bacterial and general fungal communities, compositional resistance was highest in the oldest sites, in contrast to the pattern seen for richness. This contradiction may be result in part from the limitations of the analytic method used. The majority of fungal, and about half of bacterial, communities actually had increased OTU richness in the final samples. As there was little opportunity for new microbial taxa to enter the glasshouse pots (except for general contamination from the glasshouse environment, which should have been relatively equal across pots and thus not a major driver of differences along the invasion history gradient), an increase in observed richness may actually reflect an increase in evenness. Polymerase chain reaction-based community fingerprint methods, especially for highly diverse groups, are likely to miss taxa that are not at relatively high abundance. If exposure to A. petiolata reduced the dominance of some highly abundant taxa, and thus increased the relative abundance of other taxa, this could have lead to an apparent increase in richness. Compositional resistance, as measured by the Bray–Curtis similarity index, is simply a function of the number and abundance of taxa common to both the initial and final community, divided by the total number of taxa in both. Thus, similarity would be decreased both by a large reduction in taxa, but also by a large increase. In fact, a close examination of Fig. 3 shows that the youngest fungal communities tended to show a reduction in OTU richness, intermediately aged communities showed an increase, and the oldest ones had very little change. This led to a generally increasing trend in compositional resistance with age, but for different reasons at different invasion ages.
This pattern is also likely influenced by the responses of ‘sensitive’ and ‘resistant’ taxa. For bacterial and fungal communities, the richness of ‘sensitive’ and ‘resistant’ taxa was highly correlated (r > 0.66 for both), indicating that these groups did not respond differentially to gradients in A. petiolata population age or per capita impact. As most fungal and bacterial communities were dominated by ‘resistant’ taxa, the increase in ‘sensitive’ taxa in older sites may have been overwhelmed by a concomitant increase in ‘resistant’ taxa.
By contrast, AMF communities showed the same pattern for richness and composition, with lowest resistance in the oldest and youngest sites. These differences among taxonomic groups may result partly from the resolution of the methods for each group. The AMF communities in soil have a much lower taxonomic diversity than general bacterial or fungal communities, and thus a larger percentage of available taxa were probably amplified by the PCR. The majority of AMF communities had fewer OTUs detected in the final vs initial samples, implying a general loss of taxa following exposure to A. petiolata, likely because there were fewer taxa ‘missed’ in the initial sample that could appear in the final one. Thus the oldest and youngest communities had the lowest compositional resistance primarily because of the loss of taxa in the final sample, while intermediately aged communities had higher similarity because they had relatively minor changes in OTU richness.
The AMF communities also differed from general bacterial and fungal communities in that the majority of AMF taxa were classified as ‘sensitive’ rather than ‘resistant’, and while there was a significant quadratic relationship between invasion history and number of ‘sensitive’ taxa, there was no significant relationship with ‘resistant’ taxa. Thus, while the oldest sites regained some ‘sensitive’ taxa, this gain was not balanced with an increase in ‘resistant’ types, leading to decreased overall resistance for those communities. However, this pattern may be influenced by the higher resolving power of the AMF primers.
While the patterns in microbial communities across the gradient of invasion history were quite consistent across taxonomic groups and several measures of composition and resistance, ultimately, the number of sampled communities was somewhat limited. This is especially true for the oldest sites, where only two sites at the far end of the sampled spectrum had a strong influence on the observed quadratic trends. When those two sites were removed from the analysis, microbial community structure and resistance generally showed linear patterns with invasion history. The quadratic patterns remained strong when controlling for a host of abiotic variables as well as geography, so the results cannot be explained by unusual conditions at these particular sites that are independent of A. petiolata invasion history. Nevertheless, future studies that include more samples from long-invaded sites and other areas of the invaded range are warranted.
The mechanisms underlying A. petiolata’s effects on soil microbial communities are likely multifaceted, including the well-studied allelopathic effects (Vaughn & Berhow, 1999; Roberts & Anderson, 2001; Wolfe et al., 2008), as well as more general effects on nutrient cycling (Rodgers et al., 2008b) and plant diversity (Stinson et al., 2007; Rodgers et al., 2008a). While the responses of bacterial and general fungal communities were highly correlated, neither of these broader community’s responses correlated with those of AMF communities. The AMF communities were also the only ones to show a compositional difference between samples taken near and far from actively growing A. petiolata plants. It is possible that the responses of the functionally and taxonomically diverse bacterial and general fungal were driven by generic aspects of A. petiolata invasion (changes to nutrient cycling, litter biomass, etc.), while the response of the more functionally and taxonomically restricted AMF guild were also influenced by more specific aspects of the invader, such as its allelochemicals (Stinson et al., 2006; Wolfe et al., 2008).
A secondary goal of this study was to compare microbial communities collected near and far from actively growing A. petiolata plants at each site. The AMF community composition differed significantly between samples taken near and far from A. petiolata individuals, consistent with the results of previous studies (Roberts & Anderson, 2001; Stinson et al., 2006; Burke, 2008). However, similar patterns were not evident for general bacterial or fungal communities, and in general the temporal patterns were similar for near and far samples. As A. petiolata populations can be extremely patchy in space and time, and the samples taken from ‘far’ from A. petiolata were still relatively close to the current population, it is likely that these soils had been exposed to A. petiolata in the past. This suggests that the kinds of community changes seen in this study are the result of many generations of exposure, rather than reflecting the effects of individual A. petiolata plants. The patchiness of A. petiolata populations may also help explain why 20 yr (the estimated age of the youngest site) was not long enough to extirpate all of the sensitive taxa from a community. It likely takes many years, even decades, for an A. petiolata population to completely and consistently fill all of the available understory habitat (Nuzzo, 1999), and during that time the impact of A. petiolata on the soil communities will be limited by temporal and spatial patchiness.
While there was evidence for increasing resistance of soil communities over time, it was complicated by a countervailing pattern of declining per-capita impacts of the invader. These patterns combined to give nonlinear relationships, in which soil communities declined in richness initially, as the invader selected for resistant microbial taxa and extirpated sensitive ones, but then regained some of this richness after invasions reached a certain stage. This may have resulted from a lag between ecological and evolutionary effects. In the initial stages of the invasion at a given site, the per-capita impact of the invader is likely relatively constant and the dominant effect on soil communities results from the cumulative impact of the invader over years (and the increasing density of the invader). However, over longer time-scales evolutionary changes in the invader may become important. In this case, A. petiolata tends to evolve reduced per-capita impact over time, owing to a reduction in allelopathic traits. Once this impact has been reduced far enough, sensitive microbial taxa may be able to re-establish in the invaded site. If these microbes play an important role in the establishment and growth of native plants, than this microbial recovery may also aid in the recovery of native plant communities. Consistent with this prediction, Lankau et al. (2009) found that native woody species tended to increase in abundance over a 5-yr interval in sites with the longest history of A. petiolata invasion, while they declined in abundance over the same interval in more recently invaded sites.
The results have important implications for how invasive species are studied and managed. The primary mechanisms driving invasions may vary through the different stages of invasions, and the impact of particular invasive species may also change over time because of changes both in the invader and the invaded community. However, most studies of species invasions do not explicitly consider the history of the species or population in question; Strayer et al. (2006) found that 40% of the studies they reviewed did not even report the number of years since the focal species was first introduced to a new continent. The current results suggest that researchers could come to very different conclusions about the threat posed by a given invader if their research is limited in spatial and temporal scale. These results also suggest that management of invasive species could benefit from understanding how invasive impacts change over time. For example, the recovery of soil communities in areas with the longest history of A. petiolata invasion suggests that restoration of native plant species may be successful in these areas, even without eradicating the invader. By contrast, in younger sites eradication may be the prime goal, to remove the invader before soil communities are severely degraded.