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• Leaf carbon capture strategies of native and exotic invasive plants were compared by examining leaf traits and their scaling relationships at community and global scales
• Community-level leaf trait data were obtained for 55 vascular plant species from nutrient-enriched and undisturbed bushland in Sydney, Australia. Global-scale leaf trait data were compiled from the literature for 75 native and 90 exotic invasive coexisting species.
• At the community level, specific leaf area (SLA), foliar nitrogen and phosphorus (Nmass and Pmass) and N:P ratio were significantly higher for exotics at disturbed sites compared with natives at undisturbed sites, with natives at disturbed sites being intermediate. SLA, Nmass and Pmass were positively correlated, with significant shifts in group means along a common standardized major axis (SMA) slope. At the global scale, invasives had significantly higher Nmass, Pmass, assimilation rate (Amass and Aarea) and leaf area ratio (LAR) than natives. All traits showed positive correlations, with significant shifts in group means along a common slope. For a given SLA, invasives had higher Amass (7.7%) and Nmass (28%).
• Thus, exotic invasives do not have fundamentally different carbon capture strategies from natives but are positioned further along the leaf economics spectrum towards faster growth strategies. Species with leaf traits enabling rapid growth will be successful invaders when introduced to novel environments where resources are not limited.
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The invasion of natural communities by introduced plants is recognized as a significant threat to global biodiversity (Lodge, 1993; Cronk & Fuller, 1995; Mooney, 2005) and as a major component of global change (Lovei, 1997; Vitousek et al., 1997; Ewel et al., 1999; Millenium Ecosystem Assessment, 2005). Much of the success of invasive plants is thought to be associated with their superior ability to capture and maintain space. The potential for rapid growth, particularly in environments that are not resource limited, is a key component of this ability and is strongly tied to carbon (C) fixation strategy. Thus, it seems likely that an understanding of the C fixation strategy of invasive compared with native species may further our understanding of what makes invasive species successful in new environments.
Leaf traits describing the C fixation strategy are one of the major spectra of trait variation in the ecological strategies of plants (Westoby et al., 2002; Wright et al., 2004). There is a fundamental trade-off among several ecologically important leaf traits, where species with low specific leaf area (SLA) generally have longer leaf life span (LL) than high-SLA species, suggesting that longer LL requires greater structural strength. Low SLA/long LL species also tend to have greater allocation to defensive chemicals (Coley, 1988), lower photosynthetic capacity per unit leaf mass (Amass), lower leaf nitrogen (N) concentration (Nmass) and lower dark respiration rates (Rd-mass) (Field & Mooney, 1986; Reich et al., 1997, 1998). Consequently, species with high SLA have a shorter return time on their investment in nutrients and dry mass in leaves and hence greater potential for fast growth, while species with a longer LL have a longer return time on their investment, a characteristic often associated with increased nutrient conservation. Recent evidence suggests that these relationships are consistent across habitats and lineages, indicating global convergence in plant functioning (Reich et al., 1997, 1999; Wright et al., 2001, 2004).
In this study, the SLA and leaf N and leaf phosphorus (P) concentrations of native and exotic invasive species were examined from both low-fertility undisturbed sites and nutrient-enriched sites in urban bushland remnants within Sydney, Australia. Data were then compiled from the global literature on leaf traits of exotic invasive and native species to assess whether the patterns found in these communities were consistent with patterns found for a wide range of species from around the world. For both data sets, both differences in mean values of leaf traits for exotic and native species and pairwise ‘scaling’ (log10–log10) relationships among leaf traits of native and exotic invasive species were compared.
Using standardized major axis regression, the following alternative hypotheses were tested.
Hypothesis 1. Leaf traits (SLA, Nmass, Pmass and Amass) will scale positively with one another across all species, with the trait relationships of exotic invasive and native species not differing in either slope or elevation (intercept). Any differences in leaf trait relationships between exotic invasive and native species will take the form of shifts along the common relationship slope, with invasives having generally higher trait values than native species.
Hypothesis 2. Leaf traits will scale positively with one another across all species, but the slope elevations will differ between exotic invasives and natives. For example, release from herbivore pressure in a new environment may enable exotic invasive species to achieve a higher Amass for a given SLA.
Hypothesis 3. Leaf traits will scale positively with one another across all species, but the scaling slopes will differ between exotic invasives and natives, suggesting that natives and invasives have fundamentally different C fixation strategies.
Materials and Methods
Hawkesbury Sandstone vegetation data set
Study sites All study sites were located in urban bushland remnants on Hawkesbury Sandstone-derived soils in the Sydney region. Average annual rainfall is 1220 mm. These soils are quartz-rich with well-drained, acidic sandy surface textures, and are poor in organic matter and nutrients, particularly P and N (Walker, 1960; Williams & Raupach, 1983). Typical vegetation communities supported by these soils are dry sclerophyll open forests and woodlands, dominated by species of Eucalyptus, Acacia and Banksia (Benson & Howell, 1990).
Three site types were surveyed: sites adjacent to urban creeks, sites below stormwater outlets, and undisturbed hill-slopes. Sites adjacent to urban creeks and stormwater outlets are typically subject to nutrient enrichment via stormwater run-off (Leishman, 1990; Leishman et al., 2004). The stormwater system transfers run-off from impervious surfaces in urban catchments and discharges it at outlets that generally drain into previously dry areas of natural bushland at the edge of urban development, or directly into creeks. Earlier work has shown that soils receiving stormwater run-off have average total P concentrations of approximately 600 mg kg−1 compared with background soil P concentrations of 40–100 mg kg−1 and are heavily invaded by exotic plants such as Ligustrum sinense, Cardiospermum grandiflorum, Lantana camara and Protoasparagus aethiopicus (Leishman, 1990; Leishman et al., 2004).
Sampling protocol and analyses Three replicates of each site type were surveyed. At each site, an area of 20 m × 20 m was surveyed. For all species with an estimated percentage cover > 10%, 50–100 leaves from at least three individuals were sampled. Leaf traits were measured on young to medium-aged, fully expanded outer canopy leaves. Ten leaves from each individual were separated for calculation of SLA (leaf area/leaf dry weight). Projected leaf area was determined with a flatbed scanner (HP Desk II scanner) and image analysis software (Delta-T SCAN; Delta-T Devices, Cambridge, UK). All leaves were oven-dried at 60°C for 48 h before weighing (SLA calculation) or grinding (N and P analysis). Homogenized leaf samples were analysed for total N using complete combustion gas chromatography (Howarth, 1977), and for total P using inductively coupled plasma–atomic emission spectrometry (ICP-AES). All foliar nutrient analyses were conducted at the Waite Analytical Laboratory, University of Adelaide, Adelaide, Australia.
Individual measurements were averaged for each species at each site. Species were classified into five plant types: natives from undisturbed sites, natives from urban creeks, natives from stormwater outlets, exotics from urban creeks, and exotics from stormwater outlets. In all cases, the exotic species originated from outside Australia, and are considered environmental weeds (Blood, 2001; Muyt, 2001), while the native species are indigenous to the area and have not been introduced historically.
Ten soil samples (5 cm diameter and 10 cm depth) were collected from random locations at each site, bulked and oven-dried at 110°C for 48 h, and then sieved to 2 mm. Total P was determined by ICP-AES following aqua-regia digestion and total N was analysed using the cadmium reduction flow injection method (Clesceri et al., 1999). Soil analyses were conducted at the Australian Government Analytical Laboratories, Pymble, NSW, Australia.
Global data set
The literature was searched for all studies where values for leaf traits relevant to C strategy were reported for co-occurring native and exotic invasive species. For each study, the native species were defined as indigenous to the site and the exotic species were defined as nonindigenous and invasive. Species covered a wide range of growth forms and habitats, including Hawaiian rainforest, tallgrass prairie, neotropical savanna and the Mediterranean flora. Traits for which data were available were SLA, Nmass, leaf N concentration per unit leaf area (Narea), Pmass, Parea, photosynthetic capacity (Amass and Aarea), dark respiration (Rd-area) and LAR (leaf area per unit plant mass). Species trait values from different habitats or sites within a study were averaged. This resulted in a database of leaf trait values for 75 native and 90 exotic invasive species; however, not all traits were available for all species.
All data were log10-transformed for analysis. One-way analyses of variance (ANOVAs) were used to examine trait differences between plant types. Standardized major axis (SMA) regression was used to describe the relationship between each possible pairwise combination of traits. This method is appropriate when the purpose of the study is to describe how variables are related (i.e. scaling relationships) (Warton et al., 2006). Our aim was to estimate the line best describing the bivariate scatter of two traits, and SMA regression is considered to estimate lines with greater precision than major axis regression (Warton et al., 2006). On log–log axes, SMA regression describes the best-fit scaling relationship between pairs of traits. When comparing the cloud of points that describe the pairwise relationship of traits from the different plant types, several outcomes are possible: (1) the slope of the line of best fit may differ between plant types; (2) if the slopes do not differ (are homogeneous), the clouds of points may completely overlap, or may be shifted along the common slope relative to each other, and/or may be shifted in one dimension only, resulting in a difference in elevation. SMA slopes were fitted for each plant type and tested for homogeneity. When slopes were found to be homogeneous a common slope was estimated. Elevation differences between SMAs were then tested. SMA regression analyses were performed using (s)matr software (Falster et al., 2006), with significance tested at α = 0.05.
For the Hawkesbury Sandstone data set, species were grouped into three plant types (exotics from nutrient-enriched sites, natives from nutrient-enriched sites and natives from undisturbed sites) as one-way ANOVAs showed no significant differences between exotics from urban creeks and stormwater outlets or between natives from urban creeks and stormwater outlets. For the global data set, plants were grouped into two plant types (invasive and native).
Hawkesbury Sandstone vegetation data set
Soil nutrients As expected, soil total P and N concentrations were highest for sites below stormwater outlets (mean P = 280 mg kg−1; mean N = 3322 mg kg−1) and adjacent to urban creeks (mean P = 141 mg kg−1; mean N = 2400 mg kg−1). Soil total P and N concentrations for undisturbed hill-slope sites were consistent with previously published concentrations for these naturally infertile soils (mean P = 58 mg kg−1; mean N = 1546 mg kg−1).
Comparison of traits among plant types A total of 55 species were sampled: 27 natives from undisturbed sites, 16 natives from disturbed sites and 12 exotic invasives. There were significant differences among the three plant types in SLA (F2,52 = 10.0, P < 0.0001), Nmass (F2,52 = 9.4, P < 0.0001), Pmass (F2,52 = 15.4, P < 0.0001) and N:P ratio (F2,52 = 6.6, P = 0.003). Natives from undisturbed sites had the lowest values of SLA, Nmass and Pmass, exotic invasives had the highest, and natives from disturbed sites were intermediate (Fig. 1). Natives from undisturbed sites had significantly higher N:P ratios than natives or exotic invasives from disturbed sites (Fig. 1).
Comparison of leaf trait relationships among plant types – SLA and Nmass SLA and Nmass were positively correlated and individual SMA slopes did not vary significantly among the three species groups (P = 0.674) (Table 1). There was no significant difference in y-intercepts among groups (P = 0.461). However, there were significant differences in group shifts along a common SMA (P < 0.0001), indicating that shifts in SLA result in associated shifts in Nmass. Exotic invasive species had higher SLA and Nmass than native species from undisturbed sites, with natives from nutrient-enriched sites being intermediate (Fig. 2a).
Table 1. Results of standardized major axis regression (SMA) analysis of pairwise combinations of specific leaf area (SLA), and foliar nitrogen and phosphorus (Nmass and Pmass) for 55 species of the Hawkesbury Sandstone vegetation communities in the Sydney region of Australia
Trait pair (X and Y)
Slope homogeneity (P)
Shift in elevation (P)
Shift along slope (P)
Significant results (P < 0.05) are shown in bold.
SLA and Nmass
SLA and Pmass
Nmass and Pmass
SLA and Pmass SLA and Pmass were positively correlated and individual SMA slopes did not vary significantly among the three species groups (P = 0.898) (Table 1). There was no significant difference in elevation among the SMA slopes (P = 0.747), allowing a common SMA to be fitted to examine group shifts. Significant differences in group shifts were evident along the common SMA (P < 0.0001), with exotics having higher SLA and Pmass than natives at undisturbed sites, and natives from nutrient-enriched sites being intermediate between the two other groups (Fig. 2b).
Nmass and Pmass There was a positive correlation between Nmass and Pmass, with the individual SMA slopes not varying among plant types (P = 0.924) (Table 1). SMA elevations did not differ either (P = 0.165), but significant differences in group shifts were evident along the common SMA (P < 0.0001), with exotic invasives having higher Nmass and Pmass than natives at undisturbed sites, and natives from nutrient-enriched sites being intermediate (Fig. 2c).
Global data set
Comparison of traits among plant types Invasive species had significantly higher values than native species for Nmass, Pmass, Amass, Aarea and LAR. No significant differences between invasive and native species were found for SLA, Narea or Rd-area (Table 2).
Table 2. Results of one-way analysis of variance (ANOVA) comparing leaf trait values of native and exotic species from the global data set of 165 species derived from the literature
All trait values were log10-transformed for analysis. Significant results are shown in bold.
Amass and Aarea, photosynthetic capacity per unit leaf mass and per unit leaf area, respectively; d.f., degrees of freedom; LAR, leaf area ratio; Nmass and Pmass, foliar nitrogen and phosphorus concentrations per unit leaf mass; Rd, dark respiration rate; SE, standard error; SLA, specific leaf area.
SLA (cm2 g−1)
Narea (mg N m−2)
Amass (nmol g−1 s−1)
Aarea (µmol m−2 s−1)
Rd (µmol m−2 s−1)
LAR (cm2 g−1)
Comparison of leaf trait relationships among plant types Pairwise comparisons were examined for all traits that had data for at least 20 species and that were calculated on a per unit mass basis. This reduced the traits to SLA, Nmass, Pmass and Amass. There were positive correlations for all pairwise trait relationships, with only the relationship between Pmass and Amass for natives not having a significant slope (Table 3). There were no significant differences in SMA slopes for any of the pairwise comparisons. There were significant shifts along a common SMA for the relationships between SLA and Nmass, SLA and Pmass, Pmass and Amass, and Pmass and Nmass (Fig. 3), with invasives having higher values of all trait pairs than natives.
Table 3. Results of standardized major axis (SMA) regression analysis for all pairwise combinations of specific leaf area (SLA), photosynthetic capacity per unit leaf mass (Amass), and foliar nitrogen and phosphorus concentrations (Nmass and Pmass) from the global data set of 165 species derived from the literature
Trait pair (X and Y)
Slope homogeneity (P)
Shift in elevation (P)
Shift along slope (P)
Significant results (P < 0.05) are shown in bold.
SLA and Amass
SLA and Nmass
SLA and Pmass
Nmass and Amass
Pmass and Amass
Nmass and Pmass
For the relationships between SLA and Amass and between SLA and Nmass, there were also significant shifts in elevation of SMA slopes (P = 0.027 and P = 0.030, respectively), such that, for a given SLA, invasives had higher Amass (7.7% increase) and Nmass (28% increase) (Fig. 3).
Clear differences were found between native and invasive exotic plant species in their leaf traits, and leaf trait scaling relationships were found to be consistent between these groups, both within a community and across a range of species from the global literature.
Within the Hawkesbury Sandstone vegetation community, exotic invasive species from disturbed sites had significantly higher values of SLA, Nmass and Pmass and lower N:P ratios than native species from undisturbed sites. Interestingly, native species from disturbed sites had intermediate values of these three traits. The trait-relationship comparisons of the three plant types were consistent with our first hypothesis, i.e. leaf traits scaled positively with one another across species, the slope describing the relationship between each trait pair did not differ among plant types, and differences among plant types were seen as a shift along a common axis from native species at the low end of the axis to exotic invasives at the higher end of the axis. This suggests that native species of this undisturbed vegetation community have a more conservative, slow growth strategy than exotic invasives. The soil nutrient analyses showed that soil N and P values were significantly lower at the undisturbed sites compared with the disturbed sites, consistent with previous studies (Lake & Leishman, 2004; Leishman et al., 2004). Similarly, the very high N:P ratio of natives at the undisturbed sites suggests strong P limitation (Koerselman & Meuleman, 1996). Thus the slow growth strategy of natives is entirely consistent with the low nutrient availability of these soils. However, when these soils become nutrient-enriched through proximity to urban development (particularly via stormwater run-off), there is a marked shift in vegetation composition to mesic fast-growing species including both exotic invasive species and native species that are typical of other vegetation types on higher nutrient soils (Clements, 1983). Previous studies in this vegetation community have shown that exotic invasives have better growth and survival than natives under nutrient-enriched conditions (Leishman & Thomson, 2005) and that natives have high mortality under high-nutrient conditions (Thomson & Leishman, 2004). Thus it seems likely that nutrient enrichment facilitates the invasion of exotic species into this community that are able to take advantage of the high soil nutrients available because of their fast growth C capture strategy.
How consistent are our results for 55 plant species from the Hawkesbury Sandstone vegetation community with those for 165 species from a range of habitats around the world? There was a clear and consistent pattern of exotics having higher values of leaf traits associated with C capture than natives. Exotics had significantly higher values of Nmass, Pmass, Amass, Aarea and LAR. Exotics also had higher mean values of SLA and Narea, although these differences were not significant. Only Rd (expressed on a leaf area basis) showed no pattern in relation to exotic/native status. The trait-pair relationships also showed consistent shifts along a common SMA slope, with native species having lower values for traits in each pair compared with exotics (Nmass and SLA, Pmass and SLA, Pmass and Amass, and Pmass and Nmass). Although the number of species for which data were available from the global literature was quite small for some pairwise comparisons, the consistency of these results with the community-level results suggests that the outcomes are quite robust. Overall, our results suggest that exotic and native species do not have fundamentally different strategies of C capture (seen as different scaling relationships between traits), but instead fall out at different ends of a common spectrum of variation in leaf C economics.
Two cases were found where the elevation of SMA slopes was significantly different between exotic and native species. Exotic species had 7.7% higher Amass and 28% higher Nmass for a given SLA than native species. This is consistent with previously reported results of Gulias et al. (2003), and would result in exotic species achieving a greater C gain for a given investment in leaves, resulting in an even greater return on investment and hence faster growth. Interestingly, Funk & Vitousek (2007) recently published the results of a comparison of resource-use efficiencies of native and exotic species in resource-limited environments in Hawaii. They concluded that photosynthetic nitrogen use efficiency (PNUE) of exotics was greater than that of natives in light- and N-limited habitats, but not in water-limited habitats. SMA analysis of our data showed that there was no difference in the scaling relationships of Nmass and Amass between exotic and native species and no difference in trait values. PNUE was calculated for our data and it was found that there was a trend for higher PNUE of exotics compared with natives but this was not significant (P = 0.06). It is suggested, then, that the use of ratios such as PNUE should be treated cautiously. This is because differences in ratios such as PNUE are affected by both the slope and the intercept of the line describing the relationship (between Amass and Nmass in the case of PNUE). Thus, differences in PNUE may not reflect fundamentally different strategies of resource acquisition but instead may simply reflect shifts along a common slope.
Previous studies on global patterns in leaf trait relationships have been concerned with species native to a site across a range of biomes and in relation to climate or soil nutrients (Reich et al., 1997; Wright et al., 2001, 2004, 2005). These studies have suggested that there is a universal spectrum of leaf C economics, ranging from slow to fast return on investment in dry matter and nutrients of leaves (Wright et al., 2004). This spectrum of variation has been shown to be independent of plant functional type (Reich et al., 1997; Wright et al., 2004). Our study extends this work to incorporate exotic invasive species and tested whether the success of exotic invasive plants may be attributable to a different C capture strategy, seen as different scaling relationships between leaf C capture traits. Our results suggest that this is not the case. Instead, invasive exotic species are positioned further along the universal spectrum of variation in leaf economics towards a faster growth strategy than native species. This may result from a shift in allocation from defence to growth made possible by release from herbivores, or, alternatively, species that become invasive may be those that initially have a fast growth strategy. In a recent review, Blumenthal (2006) suggested that release from natural enemies and increased resource availability may interact to facilitate invasiveness, with the resulting prediction that exotic species will tend to have high-resource traits relative to coexisting native species. Our results are consistent with this prediction. This has important implications for risk assessment of plant introductions, as it suggests that species with leaf traits that enable rapid growth (high SLA, high foliar N and P, and high Amass) are likely to be successful invaders when introduced to a new environment where resources are not limited.
We warmly thank Ian Wright, Julia Cooke, Belinda Medlyn and Brad Murray for their helpful comments on the manuscript. Thanks also to David Ackerly and two anonymous reviewers whose constructive comments improved the manuscript. We also thank those authors who provided raw data in their publications. This research was supported by the Australian Research Council.