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- Materials and Methods
- Supporting Information
The ability of plants to increase performance by taking advantage of free resources may depend on plasticity of functional traits, in particular specific leaf area (SLA) and root : shoot ratio (Nicotra et al., 2010), and it has been suggested that such plasticity contributes to the invasion success of alien plants (Richards et al., 2006). Globally widespread alien species may exhibit high plasticity in physiological and morphological traits that contribute to the maintenance of plant performance under varying amounts of resources (Richards et al., 2006). Alternatively, successful species may exhibit plastic responses to increased resource availability that result in a higher plant performance in high-resource environments, whereas less successful alien or native co-occurring species are less plastic, and are thus less able to increase performance in high-resource environments (Richards et al., 2006). This second scenario might be a mechanism underlying the theory of fluctuating resource availability and invasibility (Davis et al., 2000), which suggests that the apparently idiosyncratic nature of invasion events results from a requirement of increased resource availability coinciding with invading propagule input.
In addition to biological invasions, increases in resource availability through habitat disturbance and eutrophication (e.g. atmospheric nitrogen deposition) are major elements of global environmental change (Sala et al., 2000). It is possible that such increases in resource availability have been to the advantage of those alien, as well as native, species that can capitalize on extra resources. Such potential synergisms between elements of global change may have significant future implications for the extent of floral homogenization worldwide (Dukes & Mooney, 1999; Bradley et al., 2010), if widespread alien species are able to further exploit such resource increases.
Several studies have tested experimentally how invasive plant species respond to changes in resource availability relative to native species (Funk, 2008; Funk & Zachary, 2010) or noninvasive alien species (Burns, 2004; Hastwell & Panetta, 2005; Schlaepfer et al., 2010). Such studies are at a local scale and consider several species, and in order to build wider generalizations the results of such studies can be combined in a quantitative meta-analysis (Davidson et al., 2011; Palacio-Lopez & Gianoli, 2011). However, many studies have been conducted that are not necessarily focused on invasions, and assess the responses of various plant species to increased availability of resources such as light (e.g. Reich et al., 1998), nutrients (e.g. James, 2008) and water (e.g. Sack & Grubb, 2002). Such studies offer a valuable opportunity to assess whether more widespread alien plant species tend to be better than less widespread species in general at maintaining plant performance when resources are low, or at increasing performance when resource availability is high, and whether they differ in plastic responses of functional traits, such as SLA and root : shoot ratio. Moreover, use of data from studies that did not focus on invasions per se should minimize the potential for bias toward including only well-known or intensively studied invasive species that have been observed to become dominant after changes in resource availability in the field.
In this study, we employed a meta-analytical approach to test, across many studies and three resource types (nutrients, water and light), whether widespread alien plant species respond more strongly to increased resource availability than do less widespread species. Biomass offers the most direct measure of plant performance as a product of growth, and thus change in biomass should also offer the clearest indicator of a plant’s ability to respond to and take advantage of increased resource availability. In this study, we combined published data on responses of biomass, root : shoot ratio and SLA of plant species to increased resource availability and a global measure of alien species distribution (Randall, 2002). Specifically, we asked whether:
Whilst two other meta-analyses have recently compared trait responses to increased resources of invasive, noninvasive and native species (Davidson et al., 2011; Palacio-Lopez & Gianoli, 2011), our study is novel for three important reasons. First, we do not restrict our included studies and effect sizes to studies which focused on invasive species, allowing a larger number of effect sizes and species to be considered. Secondly, Palacio-Lopez & Gianoli (2011) combined effect sizes of different traits together in the same analysis. However, there is no reason to expect success of species to be related to responses of all traits in the same way. Thirdly, we also incorporate phylogenetic structure in our analyses, as species more closely related to one another may respond more similarly to changes in availability of resources than species that are more distantly related to one another. Failure to consider the potential for phylogenetic nonindependence in such analyses could result in concluding that a significant relationship exists between responses to resource availability and global success when it is actually confounded by phylogenetic history.
- Top of page
- Materials and Methods
- Supporting Information
Recently, increasing theoretical attention has been paid to the potential role of phenotypic plasticity in species traits in facilitating the spread of invasive alien species by maintaining plant performance under varying environmental conditions, or through allowing species to maximize performance when resource availability is increased (Richards et al., 2006). The results of our meta-analysis of large numbers of studies manipulating resources for single or few species suggest that species that are more globally widespread are better at capitalizing on increased resource availability, when light, nutrients and water are considered together. Thus, among alien plants, globally successful species are not those best able to maintain plant performance in varied environments, but tend to be those that are best able to utilize the increases in resource availability that typify human-disturbed habitats worldwide (Richards et al., 2006; Pyšek & Richardson, 2007). The lack of a significant relationship between biomass responses and global distribution when resources are considered separately may reflect lower statistical power, as the trends all tended to be positive. Our results support those of Davidson et al. (2011), who found that when studies compared invasive alien plant species with native species, the alien species tended to be more plastic in their biomass responses to increased resource availability than the native species. Gonzalez et al. (2010) also found that invasive plant species increased performance and growth rate to a greater extent than native species, under increased nutrient availability. For this response to be a true advantage, globally successful alien species should also be more responsive to increased resources than less successful alien species (van Kleunen et al., 2010), and our findings indicate that this is likely to be the case.
Our results may also corroborate the theory of fluctuating resource availability and invasibility, if invasion depends upon alien species responding strongly to increased resource availability. Davis et al. (2000) suggested that species are only able to colonize and establish in a community if resource availability increases, either through resource input or by reduced resource uptake by the community. An extension of this theory is that species better able to use an increase in resource availability may be more successful at establishing than those that are less able to respond. Leishman & Thomson (2005) found that increases in nutrient availability were crucial in allowing invasive alien plants to establish over low-fertility adapted natives in areas of disturbance with big increases in water availability, but with inherently low fertility. It is unclear from our study whether globally successful species tend to establish in open, disturbed habitats with low amounts of competition, or whether they are also able to establish in less disturbed, competitive communities when resource availabilities are increased. Many studies in our analyses did not test the responses of species to resource increase in a community context, which would be a prerequisite for testing both the theory of fluctuating resource availability and the hypothesis that greater alien responses increase the likelihood of the alien invading a community. We cannot rule out the possibility that globally distributed species are merely those best suited to establishing in open, anthropogenically altered habitats, which also tend to have elevated amounts of resources. Thus, the global distributions of successful species may simply reflect the worldwide distribution of similarly disturbed, resource-enriched environments.
In less disturbed habitats, the importance of an increase in resources for establishment of alien plants is likely to vary, depending on how historically limiting the resources in question are at a particular location (Davis & Pelsor, 2001), and on how the recipient community responds to increased resource availability relative to incoming aliens. Increased availability of a limiting resource is only likely to reduce the amount of competition and community resistance if growth responses by the community do not result in other resources becoming limited. For example, without adequate disturbance, nutrient additions may increase the competition intensity for light exerted by the resident community (Hautier et al., 2010) in areas where soils are relatively fertile, thus increasing, rather than decreasing, resistance to invasion. Moreover, it has recently been argued that factors affecting the ability of alien species to establish may act in concert rather than in isolation, such that patterns of invasion success in relation to single factors alone are not apparent (Blumenthal, 2005). Local-scale studies that set species’ responses to increased resource availability in a community context, and interacting with other factors such as enemy release (Blumenthal et al., 2009), will better elucidate how different responses among species play out in terms of shifts in abundance and dominance of alien and native species in those communities. However, notwithstanding interactions with resident communities and other biotic and abiotic factors, our study still indicates that globally successful species tend to be more suited to take advantage of increases in resource availability than less successful species.
Optimal-resource allocation theory (Bloom et al., 1985) predicts that plants should invest biomass into structures that allow for uptake of the most limiting resource. However, we found that plants, on average, did not reduce biomass allocation to roots when below-ground resources increased. This contrasts with the results of Reynolds & D’Antonio (1996) and Poorter et al. (2012), who showed that root mass ratios across multiple species decreased on average in response to increased nutrient availability. Moreover, there was no relationship between root : shoot ratio responses to increased resource availability and global distribution. This corroborates further the findings of Reynolds & D’Antonio (1996), and more recently Poorter et al. (2012), in that species best suited to high-nutrient environments did not alter their root mass ratios in response to increased nutrient availability compared to species from low-nutrient environments. However, Davidson et al. (2011) found that invasive alien species tended to be more plastic in root : shoot ratio responses to increased resource availability than native species. Whilst aliens may be better than neighbouring natives at shifting biomass allocation from roots to shoots under more favourable resource availability (Davidson et al., 2011), our results suggest that at a global scale an ability to change biomass allocation may not offer a consistent advantage to alien species.
In line with expectations of adaptive shade-tolerance plasticity (Valladares & Niinemets, 2008), SLA decreased when light availability increased, and this decrease tended to be stronger when the difference in light availability increased between treatment and control plants. However, in contrast to expectations, widespread species did not decrease SLA to a greater extent than did less widespread species when light availability was higher. A recent multi-species study, including 14 invasive and noninvasive congeneric pairs of species, also found no difference between invasive and noninvasive species in SLA responses to light (van Kleunen et al., 2011). Similarly, plasticity in SLA did not differ between invasive alien and native species in the meta-analysis by Davidson et al. (2011). This implies that plasticity in the ability of plants to capture more light under both low- and high-light conditions by changing SLA does not necessarily contribute to success at a global scale.
The presence of a relationship between global success and biomass responses, but the absence of a relationship with root : shoot ratio and SLA responses is intriguing. The greater biomass increases of more widespread alien species under higher availability of resources may be the result of changes in resource-capture and physiological traits other than SLA and root : shoot ratio. Alternatively, the performance of plants in varied environments may not simply be the product of their ability to change individual traits (Funk, 2008), but may involve varied responses by multiple traits (Richards et al., 2006). Moreover, resource-acquisition traits of successfully invading species are often dependent on the type of habitat being invaded (Leishman et al., 2010; Tecco et al., 2010). Differences (Ordonez et al., 2010; Godoy et al., 2011) or similarities (Leishman et al., 2010; Tecco et al., 2010) between aliens and natives may be more important to alien success than differences in the capacity of traits to vary (Godoy et al., 2011). Alternatively, Palacio-Lopez & Gianoli (2011) suggest that establishment success of newly introduced species in wide-ranging environments may be determined more by rapid local adaptation than by plasticity. In any case, direct and consistent correlations between plasticity of single traits and plant performance or global success seem increasingly unlikely. Focusing on the endpoint of trait plasticity – the performance or fitness of the plant under different environmental conditions – is perhaps a more useful approach to understanding whether or not globally widespread or invasive species are successful owing to their ability to survive and outperform other species in multiple environments.
In summary, our study suggests that the ability of plant species to increase biomass in response to increased resource availability also appears to confer species success at a global scale, but that plasticities of individual resource-capture traits are unlikely to be consistently related to species success. The search for a relationship between plasticity of individual traits and species success may be less fruitful than measuring plant performance under different environments. Whether an ability to increase biomass translates ultimately to increased individual and population-level fitness for widespread, successful species requires more detailed experiments involving multiple native and alien, successful and unsuccessful species, grown under different environmental conditions and involving direct fitness measurements.