Present address: Department of Rangeland Ecology and Management, Texas A&M University, College Station, TX 77843, USA.
Differences in morphological and physiological traits between native and invasive populations of Sapium sebiferum
Article first published online: 2 JUN 2007
Volume 21, Issue 4, pages 721–730, August 2007
How to Cite
ZOU, J., ROGERS, W. E. and SIEMANN, E. (2007), Differences in morphological and physiological traits between native and invasive populations of Sapium sebiferum. Functional Ecology, 21: 721–730. doi: 10.1111/j.1365-2435.2007.01298.x
- Issue published online: 2 JUN 2007
- Article first published online: 2 JUN 2007
- Received 14 February 2007; revision 29 March 2007; accepted 27 April 2007 Editor: James Cresswell
- biomass allocation;
- common garden;
- evolution of increased competitive ability;
- invasive species;
- plant traits
- 1Functional traits contribute to the success of invasive plants. These traits can reflect inherent properties or they can be new adaptations from evolutionary responses to escape from natural enemies of the introduced range. We tested the hypothesis that genetic shifts in morphological and physiological traits have occurred between native and invasive populations of Sapium sebiferum.
- 2Sapium sebiferum seedlings were grown in a greenhouse using seed collected from four populations of its introduced range (US) and four from native Chinese populations that are thought to be genetic candidates of the introduced populations. We examined plant biomass production, relative growth rate (RGR), relative stem height growth rate (RHR), root : shoot ratio (RSR), total number of leaves (TLN) and leaf area (TLA), specific leaf area (SLA), leaf area ratio (LAR), net CO2 assimilation (A) and shoot specific respiration rate (RD).
- 3US populations of S. sebiferum differed from Chinese populations for most plant variables. Final shoot and total biomass, as well as, RGRs of invasive (US) populations were significantly greater than those of native (Chinese) populations, although RHR and TLN per seedling did not differ between them. Root : shoot ratios (RSR) were significantly lower, while leaf traits including TLA, LAR and SLA were generally greater for invasive populations compared to native populations. Net CO2 A was significantly higher for invasive populations than for native populations, but no significant difference in RD was found between two population types.
- 4Of 13 measured plant variables, RSRs, TLA and CO2 A were identified as traits that contributed the most to differences observed between native Chinese and invasive US populations. The suite of morphological and physiological traits functioning together may result in different growth strategies for native versus invasive populations. By virtue of these traits, invasive populations of S. sebiferum may use soil resources and light more efficiently than native populations, which may have given rise to their competitive superiority in the introduced range.
Invasive plants often grow more vigorously and attain higher abundances in their introduced range compared to conspecifics in their native range (Elton 1958; Crawley 1987; Thebaud & Simberloff 2001; Leger & Rice 2003; Jakobs, Weber & Edwards 2004; Bossdorf et al. 2005). To identify factors contributing to their invasive success, a number of studies have investigated morphological and physiological traits of invasive plants by comparing them with the native species they displace or non-invasive congeners (e.g. Roy 1990; Rejmánek & Richardson 1996; Williamson & Fitter 1996; Reichard & Hamilton 1997). In these studies and others, greater relative growth rates (RGR) of introduced species are generally associated with lower root : shoot ratios (RSR), higher specific leaf areas (SLA; leaf area per unit leaf mass), leaf area ratios (LAR; total leaf area per unit plant mass) and higher net CO2 assimilation (A) as well as lower respiration costs (RD) (Pattison, Goldstein & Ares 1998; Baruch & Goldstein 1999; Durand & Goldstein 2001; Smith & Knapp 2001; Grotkopp, Rejmánek & Rost 2002; McDowell 2002; Ehrenfeld 2003; Wilsey & Polley 2006).
These functional traits, common to invasive plants, may reflect their inherent properties due to previous evolution in the native range before its introduction or new adaptation as a result of an evolutionary response to escape from natural enemies in the introduced range (Blossey & Nötzold 1995; Callaway & Aschehoug 2000; Leger & Rice 2003; Erfmeier & Bruelheide 2005; Güsewell, Jakobs & Weber 2006). Some invasive plants may be innately better competitors because they evolved in a more competitive environment (Crawley 1987; Tilman 1999; Callaway & Aschehoug 2000; Davis, Grime & Thompson 2000). Once established in the introduced range, they may gain a systematic advantage over competitively inferior native plants. On the other hand, since allocation to defence may be as costly as herbivore damage (Bazzaz et al. 1987; Baldwin, Sims & Kean 1990), plants that escape their enemies in an introduced range could gain a selective benefit from decreasing their defensive investment. As a consequence, they may evolve to be fast-growing and low herbivore-defence plants (EICA hypothesis, Blossey & Nötzold 1995; Thompson 1998; Mooney & Cleland 2001). The distinction between environmentally induced phenotypic differences and a genetic change could be revealed by common garden experiments in which both native and invasive individuals are grown together in the same environment (Siemann & Rogers 2001; Leger & Rice 2003; Wolfe, Elzinga & Biere 2004; Erfmeier & Bruelheide 2005; Güsewell et al. 2006).
While the majority of past studies have compared invasive plants with natives or non-invasive congeners, only a few common garden studies have concentrated on variation in morphological and physiological traits between native and invasive populations of exotic plants (Bastlová & Kvêt 2002; DeWalt, Denslow & Hamrick 2004; Erfmeier & Bruelheide 2004, 2005; Buschmann, Edwards & Dietz 2005; Güsewell et al. 2006). A greenhouse study revealed that introduced Hawaiian and native Costa Rican populations of the tropical shrub Clidemia hirta displayed no significant differences in RGR, Amax or SLA (DeWalt et al. 2004). Common garden and greenhouse experiments showed significant but not always consistent differences in growth and reproductive characteristics between native and introduced ranges of invasive Brassicaceae species except Bunias orientails (Buschmann et al. 2005). Güsewell et al. (2006) found that invasive European plants produced more shoots than native American plants of Solidago gigantea, but they did not differ in shoot size, leaf traits and litter decomposition. A 4-month greenhouse experiment indicated that total leaf area (TLA) and SLA were significantly greater for plants from invasive populations than from native populations of Lythrum salicaria, but no significant differences in LAR or A were found between them (Bastlová & Kvêt 2002). Recently, a study on Rhododendron ponticum provided evidence for a genetic shift in invasive populations towards an increased investment in growth relative to native populations (Erfmeier & Bruelheide 2005).
Chinese tallow tree (Sapium sebiferum L. Roxb., Euphorbiaceae, synonyms include Triadica sebifera, ‘Sapium’ henceforth) is native to China (Zhang & Lin 1994), and has recently become a severe invader that aggressively displaces native plants and forms monospecific stands in the south-eastern USA (Bruce et al. 1997). Results of recent studies on S. sebiferum generally support the EICA hypothesis (Siemann & Rogers 2001, 2003a,b; Rogers & Siemann 2004, 2005; Zou et al. 2006), suggesting that Sapium has evolved to be a faster-growing, less herbivore-resistant plant in response to low herbivore loads in its introduced range. In a 14-year common garden study, Siemann & Rogers (2001) found that plants of invasive Texas genotypes were larger, yet less chemically defended against herbivores than native Asia genotypes. Results of a pot experiment indicated that invasive Sapium genotypes tolerated simulated herbivory more effectively than native genotypes (Rogers & Siemann 2004). A common garden study showed that invasive Sapium populations still out-competed native populations despite more damage from herbivores in the native Chinese range (Zou, Rogers & Siemann, unpublished data). These previous studies focused primarily on a trade-off between plant growth and herbivore defence, rather than shifts in morphological and physiological traits between native and invasive populations. If the EICA hypothesis holds for Sapium, however, native and invasive populations may also differ in some functional traits that typically characterize invasive plant species: biomass production, total number of leaves (TLN) and leaf area (TLA), relative stem height growth rate (RHR), relative growth rate (RGR), below- and above-ground biomass allocation (RSR), non-photosynthetic and photosynthetic tissue allocation (SLA and LAR), net CO2 assimilation (A) and dark respiration rate (RD).
The objective of this study was to examine whether native and invasive populations of Sapium genetically differ in morphological and physiological traits. Specifically, we predicted that plant biomass, RGR, RHR, TLN, TLA, SLA, LAR and A would be higher, while RSR and RD would be lower in invasive (US) than in native (Chinese) populations of Sapium. To test this prediction, we compared plant traits between four invasive US populations and four native Chinese populations in a greenhouse common garden experiment.
Materials and methods
In November and December 2004, seeds were hand collected from four populations of naturalized Sapium trees in Texas, USA and four populations in China (Table 1). Seeds were collected from 4 to 10 different trees of each population. Seeds from native populations were located within the northern part of Sapium's range in China (Zhang & Lin 1994). Genetic analyses using microsatellites suggest that north Chinese populations are likely to be genetic candidates of Sapium introductions in Texas (DeWalt, Siemann & Rogers 2006; DeWalt, Siemann & Rogers, unpublished data). One thousand seeds with the similar size (weight and volume) of both native and introduced Sapium trees were separately planted in 65-mL cone-tainersTM (Stuewe & Sons, Corvallis, OR, USA) in a greenhouse at Nanjing Agricultural University, Nanjing, Jiangsu, China (32º2′N, 118º50′E) in December 2004. Cone-tainers were filled with soil taken from the top 20 cm of the profile in fields at Jiangsu Academy of Agricultural Sciences in Nanjing where Sapium trees are naturalized in uncultivated areas. Planted seeds remained dormant throughout the winter season and germinated during March. The small seedlings grew in the cone-tainers for about 4 weeks until they had secondary leaves, at which time they were transplanted into pots. To minimize maternal effects due to difference in seed qualities, seedlings of similar height, basal diameter and leaf numbers (two leaves) were selected for the pot experiments in this study. Height of selected seedlings did not significantly differ between two population types at the time of transplanting (P = 0·17). Difference in seedling height between two population types at the first harvest was independent of the initial height at transplanting (manova, P = 0·24).
A 120-day greenhouse pot experiment was performed in the greenhouse at Nanjing Agricultural University, Jiangsu, China. On May 10, 2005, 48 Sapium seedlings of native populations (Chinese) and 48 Sapium seedlings of invasive populations (US) were individually transplanted into 6·50-L tree-pots filled with topsoil from the uncultivated fields. We measured stem height and recorded leaves on each seedling before transplanting. Pots were randomly placed in the greenhouse and they were reassigned haphazardly to new positions bi-weekly. To investigate seasonal dynamics of plant traits, Sapium seedlings were separately harvested on June 19 (40 days), July 29 (80 days) and September 7, 2005 (120 days), and the effect of population type on plant traits was separately examined within each harvest date. On each of the first two harvest dates, four seedlings per population from US and Chinese population types (2 population types × 4 populations × 4 replicates = 32 pots) were randomly selected and harvested. After each of the first two harvests, remaining pots were again randomly placed in the greenhouse and rotated bi-weekly. The final harvest consisted of the 32 seedlings not selected in either of the first two harvests. The replicate seedlings within each population were from different maternal trees. All seedlings grew healthily until the harvest.
growth analyses and biomass allocation
We measured plant growth and biomass allocation on each harvest date. Before harvesting, we recorded stem height and TLN per seedling. Plants were divided into roots, leaves, and stems and dried at 70 °C for 48 h. Total leaf area per seedling (TLA, cm2) was measured on fresh leaves using a computer program Sscnimage (Scion Image for Windows, Scion Corporation at: http://www.scioncorp.com). This program is based on NIH Image that was used to calculate leaf area in our previous studies (Siemann & Rogers 2003a). Based on plant biomass and leaf area measurements, we calculated plant morphological traits: root : shoot ratio (RSR, ratio of below- to above-ground (AGB) biomass, g g−1), specific leaf area (SLA; leaf area per unit leaf mass, cm2 g−1), leaf area ratio (LAR; total leaf area per whole plant mass, cm2 g−1). Relative stem height growth rates (RHR) were calculated as: RHR =[ln(harvest stem height) – ln(initial stem height at transplanting)]/time in growth days. Relative biomass growth rates (RGR) for each population were calculated as: RGR = [ln(seedling mass at second or third harvest) –ln(seedling mass at first or second harvest)]/interval days (40 days).
gas exchange measurements
A chamber method was used to measure gas exchange rates in this study (Grogan & Chapin 2000; Maljanen et al. 2001; Zou et al. 2004). The soil–plant system CO2 fluxes were measured in each harvest pot using a Plexiglas cylindrical ‘top-hat and open-bottom’-shaped chamber fitted with a circulation fan inside (Zou et al. 2004, 2005, 2006). This cylindrical chamber was 25 cm diameter and 100 cm high. About 80% of ambient photosynthetic effective radiation can penetrate the transparent chambers. While taking gas samples, the chamber was placed over the vegetation with the rim of chamber fitted into the groove of pot. The top edge of each pot had a groove for filling with water to seal the rim of the gas-collecting chamber. On each date, gas samples were simultaneously taken from the headspace inside the chamber for each pot. Air temperature, humidity and photosynthetic photon flux density inside the chamber were recorded with each set of emission measurements. No significant difference in humidity inside the chambers was found before and after gas sampling. In this study, air temperature inside the chambers was 25–28 °C while measuring CO2 fluxes on three dates. Photosynthetic photon flux density inside the chambers was about 428 µmol m−2 s−1 on June 19, 533 µmol m−2 s−1 on July 29 and 345 µmol m−2 s−1 on September 7.
Carbon dioxide mixing ratios in gas samples were detected by a modified gas chromatograph (Agilent 4890D) with a hydrogen flame ionization detector (FID) (Zou et al. 2005, 2006). Carbon dioxide was separated by one stainless steel column (2 m length and 2·2 mm inner diameter) packed with 50–80-mesh porapack Q. Afterwards hydrogen reduced CO2 to CH4 in a nickel catalytic converter at 375 °C, and CH4 was detected by the FID. The oven was operated at 55 °C and the FID at 200 °C. Fluxes were determined from the slope of the mixing ratio changes over four consecutive 1-min intervals starting 0·5-min after chamber closure.
We measured the soil–plant system CO2 fluxes three times on each harvest date. First, CO2 fluxes of the soil–plant system (FLUXA) were measured by transparent Plexiglas cylindrical chambers under ambient light conditions. Here, FLUXA is the measurement of the net ecosystem CO2 exchange (NEE) between soil–plant system and atmosphere, representing the balance between C uptake by above-ground plant net photosynthesis (net CO2 assimilation, A) and total C losses from soil respiration (S), that is, FLUXA = A – S. After the transparent chambers were removed to adequately equilibrate CO2 concentrations and temperatures with ambient conditions, the soil–plant system CO2 fluxes were measured using the opaque chambers wrapped in a layer of sponge and aluminium foil. CO2 fluxes measured by the opaque chambers (FLUXD) stands for ecosystem respiration (ER), the sum of shoot respiration (R) and soil respiration (FLUXD = R + S). Finally, a cutting-plant method was used to quantitatively partition soil respiration and shoot respiration from the whole soil–plant system CO2 emissions. The cutting-plant method is described in detail by Zou et al. (2005, 2006). In this method, soil CO2 efflux (S) measured after the shoots were removed at the soil surface is the sum of soil microbial heterotrophic respiration and root autotrophic respiration. Shoot respiration (CO2 effluxes from shoots) was, therefore, quantified as the difference in FLUXD and S since plant photosynthesis in an opaque chamber was interrupted while gas sampling (Zou et al. 2004, 2005). This difference in CO2 fluxes (mg CO2–C m−2 h−1) was divided by the corresponding shoot mass and then translated into shoot specific respiration rate (RD) that was expressed in terms of a respiratory coefficient (RD, µmol g−1 s−1). Similarly, net CO2 A was quantified by the difference between FLUXD and S, in terms of per unit leaf area (Aa, µmol m−2 s−1) or leaf mass (Aw, µmol g−1 s−1).
Analysis of variance (anova) was used to examine the effect of the population type (native Chinese vs invasive US population types) and population within type on plant growth, morphological and physiological traits for each harvest time with a simple nested model. The population type was considered as fixed factor and population nested within type as random factor (Table 3). No transformations were needed if variables tended to be distributed with normality and homoscedasticity; otherwise, they were log-transformed to achieve the assumptions of anova. We also checked the distribution pattern of residuals for the tests. We examined whether US and Chinese populations separated in multivariate space by conducting a discriminant analysis. Different plots in canonical components space allowed us to determine which variables contributed most to this separation, which was based on pairwise correlation coefficients between the first canonical score of discriminant ordinations and 13 variables measured on S. sebiferum since the variables had different units of measurement. All statistic analyses were carried out using the jmp statistical software, v. 5·1 (SAS Institute, Cary, NC, USA).
|Variable||Source||First harvest||Second harvest||Third harvest|
|LB||Population type||18·9||0·005||7·0||0·04||19·3||< 0·001|
|Population||3·4||0·01||8·5||< 0·001||7·4||< 0·001|
|RSR||Population type||159·5||< 0·0001||26·2||0·002||4·9||0·07|
|SLA||Population type||0·0||0·91||57·8||< 0·001||6·1||0·05|
|Aw||Population type||5·7||0·06||129·7||< 0·001||35·2||0·001|
plant growth and biomass allocation
An analysis of variance (anova) showed no significant difference in RHR between native Chinese and invasive US population types (Tables 2 and 3). Compared to native populations, leaf biomass (LB) of invasive populations was significantly greater over the entire experiment. During the early growth stage, root biomass (RB) of invasive populations was significantly lower than that of native populations, but no significant difference was found on July 29 and September 7, 2005. The first harvested stem (SB) and above-ground biomass (AGB) did not significantly differ between two population types, but they were significantly greater for invasive populations than for native populations at the second and third harvests. By the end of experiment, nevertheless, final harvest shoot and total biomass of invasive populations were significantly higher than those of native populations (Tables 2 and 3). The calculated biomass RGR were significantly greater for invasive US populations than for native Chinese populations (Table 2, F1,6 = 6·17, P < 0·05 on July 29, 2005, F1,6 = 8·31, P < 0·05 on September 7, 2005). In contrast, no significant difference in growth among populations within each type (native Chinese or invasive US population type) was found on RHR, LB, SB, AGB and TB throughout the experiment (Table 3).
|Variable||First harvest (19 June 2005)||Second harvest (29 July 2005)||Third harvest (7 September 2005)|
|RHR (mm cm−1 day−1)||0·35 ± 0·01||0·31 ± 0·02||0·21 ± 0·01||0·20 ± 0·01||0·18 ± 0·00||0·17 ± 0·00|
|LB (g)||1·50 ± 0·07**||1·07 ± 0·07||3·21 ± 0·17*||2·89 ± 0·15||6·47 ± 0·23***||4·68 ± 0·22|
|SB (g)||1·14 ± 0·04||1·14 ± 0·08||3·69 ± 0·22*||2·56 ± 0·18||6·40 ± 0·23**||5·21 ± 0·19|
|RB (g)||0·56 ± 0·03**||0·77 ± 0·05||1·77 ± 0·10||2·10 ± 0·13||3·20 ± 0·15||2·84 ± 0·10|
|AGB (g)||2·64 ± 0·11||2·22 ± 0·14||6·90 ± 0·39*||5·45 ± 0·30||12·87 ± 0·45**||9·88 ± 0·40|
|TB (g)||3·19 ± 0·13||2·99 ± 0·19||8·67 ± 0·49||7·55 ± 0·43||16·07 ± 0·58*||12·73 ± 0·40|
|TLN||31·50 ± 2·10||27·50 ± 1·70||52·50 ± 4·61||36·71 ± 4·12||70·21 ± 4·02||63·81 ± 6·23|
|TLA (cm2)||62·40 ± 2·50*||51·00 ± 3·20||127·50 ± 7·22**||91·22 ± 4·63||155·13 ± 5·81**||107·42 ± 4·93|
|RSR (g g−1)||0·21 ± 0·01***||0·35 ± 0·02||0·26 ± 0·01**||0·39 ± 0·02||0·25 ± 0·01||0·29 ± 0·01|
|SLA (m2 g−1)||41·78 ± 1·50||41·61 ± 1·92||39·66 ± 2·21***||31·87 ± 1·62||24·10 ± 1·00||20·35 ± 0·65|
|LAR (m2 g−1)||19·58 ± 0·67*||16·91 ± 1·07||14·73 ± 0·83**||12·25 ± 0·61||9·71 ± 0·41||8·14 ± 0·30|
|Aa (µmol m−2 s−1)||21·94 ± 0·74**||16·48 ± 1·18||25·58 ± 1·86*||18·33 ± 0·97||19·15 ± 0·64*||14·39 ± 0·67|
|Aw (µmol g−1 s−1)||91·58 ± 3·20||77·72 ± 5·31||95·22 ± 5·46***||60·91 ± 3·21||46·02 ± 1·78**||32·16 ± 1·03|
|RD (µmol g−1 s−1)||21·24 ± 0·96||21·09 ± 1·65||10·82 ± 0·91||10·22 ± 0·76||9·77 ± 0·40||10·21 ± 0·38|
|RGR (mg g−1 day−1)||–||–||25·03 ± 0·60*||23·19 ± 0·45||15·47 ± 0·21*||13·04 ± 0·82|
Total number of leaves (TLN) per seedling did not significantly differ between native and invasive population types, but it significantly differed among populations within each type (Tables 2 and 3). In contrast, TLA per seedling of invasive populations was significantly greater than that of native populations. Also, LAR were significantly higher for invasive populations than for native populations on June 19 and July 29, and tended to be greater on September 7 (Tables 2 and 3). Significant differences in SLA and RSR between native and invasive population types were found on June 19 and July 29, but they did not differ among populations within each type (Tables 2 and 3).
Net CO2 A in terms of leaf area (Aa) or leaf mass (Aw) was significantly greater for invasive populations than for native populations under the photosynthetic photon flux density 330–550 µmol m−2 s−1 in this study (Tables 2 and 3). In contrast, RD did not differ between native and invasive populations throughout the experiment, while a significant variation among populations within each type was found on July 29 and September 7, 2005.
The canonicals of discriminant analyses of 13 morphological and physiological traits provided a clear separation of US and Chinese population types throughout the experiment. For analyses on three different dates, the first two axes explained 69%–77% of the total variation (Fig. 1). Pairwise correlation analyses showed that RSR was the variable most strongly correlated with the first canonical during the early growth stage (Table 4), which supported the univariate analyses showing that invasive population types had significantly lower RSR than native population types on June 19 (Tables 2 and 3). At the end of experiment, however, Aa (Aw) and TLA became the physiological and morphological trait variables that were most strongly correlated with the first canonical. This suggests that Aa and TLA accounted for distinguishing invasive population types from native population types of Sapium (Table 4). Over the entire experiment, pairwise correlation coefficients between the first two canonical scores of discriminant ordinations and 13 variables suggested that RSR, TLA and A were the functional traits that contributed most to the distinction between population types from native and invasive ranges (Table 4).
|Variable||First harvest||Second harvest||Third harvest|
|Canonical 1||Canonical 2||Canonical 1||Canonical 2||Canonical 1||Canonical 2|
shifts in functional traits
One of the most important findings of this study was that shifts in morphological and physiological traits might combine to result in different growth strategies for native vs invasive populations of Sapium. Most individual traits of invasive US populations of Sapium differed from native Chinese populations. Shifts in the individual traits may work in combination to determine alternative adaptive strategies of invasive populations relative to native populations of Sapium. For instance, lower RSR suggests that invasive population types used soil nutrients more efficiently compared to native population types, and thus can uptake higher nutrients with relatively lower below-ground C allocation. By virtue of their higher TLA and A, invasive populations apparently capture and use light more efficiently than native populations. Thus, the suite of morphological and physiological traits functioning together may result in different growth strategies between native and invasive populations of Sapium.
Genetic changes among conspecifics in their native and introduced ranges account for differences in plant functional traits observed between native and invasive population types (Growth-Differentiation Balance (GDB) hypothesis, Herms & Mattson 1992; EICA hypothesis, Blossey & Nötzold 1995). From these genetic-shift hypotheses, we predict that introduced US populations of Sapium would have greater TLA, SLA, LAR and A, but lower RSR and RD than native Chinese populations because such characteristics have been predicted to be associated with fast-growing (growth-dominated) rather than slow-growing (differentiation-dominated) population types (Herms & Mattson 1992). Measurements of most morphological and physiological traits are generally consistent with our prediction, except for no significant difference in RHR, TLN and RD throughout the experiment. Such genetic shifts in morphological and physiological traits were also partially found on L. salicaria (Bastlová & Květ 2002), R. ponticum (Erfmeier & Bruelheide 2004, 2005), Barbarea vulgaris and Rorippa austriace (Buschmann et al. 2005) as well as S. gigantea (Güsewell et al. 2006), when native and invasive populations were compared in a common garden study.
One mechanism by which invasive plants may achieve fast-growth is through changes in below- and above-ground biomass allocation (Schierenbeck, Mack & Sharitz 1994; Gremmen, Chown & Marshall 1998; Sexton, McKay & Sala 2002; Wilsey & Polley 2006). Based on a review of the previous studies that compared the root : shoot ratio of exotic plants and the native plants that they displace, Ehrenfeld (2003) proposed that lower RSR is closely associated with the increased size and growth rate of invasive plants. This hypothesis is supported by the result of Wilsey & Polley (2006) who showed that RSRs of introduced grasses were lower than those of native grasses when they were grown in a common environmental condition. In the present study, we found that RSRs were significantly lower for invasive populations compared to native populations of Sapium, which is consistent with the result of our previous common garden study (Zou et al. 2006).
Lower RSR of invasive populations relative to native populations may reflect a genetic shift as an evolutionary response to the absence of natural enemies in the introduced range. Some studies have suggested that herbivory pressure has significant impacts on biomass allocation between below- and above-ground (Strauss & Agrawal 1999; Gassmann 2004). Higher RSRs are often found to be associated with greater shoot herbivory damage for invasive plants (Herms & Mattson 1992; Jeschke, Baig & Hilpert 1997; Shen et al. 2005). In this context, invasive populations evolved under less herbivory in the introduced range would be predicted to have lower RSR than native populations evolved under heavier herbivore pressure in the original range. This genetic shift suggests that relatively more mass was allocated to photosynthetic tissues for the invasive populations, but more mass to the root growth for the native populations.
Leaf traits have been well documented to be one of the most important characteristics of vigorously growing invasive plants (e.g. Pattison et al. 1998; Baruch & Goldstein 1999; Durand & Goldstein 2001; Smith & Knapp 2001; Grotkopp et al. 2002; McDowell 2002). Plant photosynthesis depends largely on TLA. Specific leaf area (SLA) or LAR as indicators of photosynthetic surface area per unit investment in leaf tissue or in whole plant are often positively associated with rapid growth rates. Several previous common garden studies have found differences in leaf traits between native and invasive populations of introduced plants. Although no significant differences in leaf traits were found by DeWalt et al. (2004) and Güsewell et al. (2006), for example, a 4-month greenhouse common garden experiment indicated that TLA and SLA were significantly greater for plants from invasive populations than native populations of L. salicaria (Bastlová & Květ 2002). In the present study, we also found that TLA, SLA and LAR of invasive populations were generally greater than those of native populations, which suggests that invasive Sapium plants in the introduced range have developed a strategy that minimizes carbon costs associated with photosynthesis, making more carbon available for tissue growth.
Another possible mechanism contributing to invasive plant success is through increasing net CO2 A. It is well documented that some invasive plants outperformed the co-occurring native species through maximizing photosynthesis (e.g. Baruch & Goldstein 1999; Durand & Goldstein 2001; McDowell 2002; Nagel & Griffin 2004). Although no significant difference in net CO2 A between native and invasive populations was found for the invasive tropical shrub C. hirta (DeWalt et al. 2004) or L. salicaria (Bastlová & Květ 2002), greater net CO2 A of invasive populations relative to native populations of Sapium found in this study suggests that maximizing photosynthesis might evolve as a strategy that contributes to the success of invasive plants in the introduced range. Contrary to the prediction, we found no significant difference in RD between two population types of Sapium over the whole season. Since dark respiration is often used to estimate plant tissue construction, greater A but no difference in RD suggest that at a similar cost, invasive populations were able to gain higher photosynthetic rates, which contributed to their higher growth rates than native population types.
The discriminant analysis summarizes plant variable measurements from this study. The morphological and physiological traits measured in this study proved to be powerful in discriminating between invasive and native population types of Sapium (Fig. 1), and, therefore, may be important factors contributing to its invasive success in the introduced range. In particular, RSR, TLA and A were identified as the three most powerful functional traits in the discriminant analysis. Lower RSR is supported by the result of a previous 4-month pot experiment indicating that higher soil nitrogen availability and soil nitrogen uptake by plants were associated with invasive populations rather than native populations of Sapium (Zou et al. 2006). Higher TLA and A would give invasive populations an advantage over native populations in the use of light resources. As a result, the combination of lower RSR and higher A, and TLA may have important implications for their invasive success in the introduced range.
difference in growth
It is not surprising that some plant variables (SB, TB and SLA) measured at the first harvest did not significantly differ between native and invasive population types since this experiment was initiated using seedlings of similar size. However, differences in plant variables between native and invasive populations became more apparent over time (Tables 2 and 3). Indeed, final harvest shoot mass (AGB) and total mass (TB) of the invasive US populations of Sapium were significantly greater than those of the native Chinese populations by the end of the experiment, although some growth variables such as RHR and TLN did not significantly differ. Moreover, RGRs were significantly higher for invasive populations than for native populations. Together with the previous studies indicating the higher growth rate of invasive populations relative to native populations of Sapium (Siemann & Rogers 2001, 2003a,b; Rogers & Siemann 2004, 2005; Zou et al. 2006), the results of this study are generally in support of the EICA hypothesis suggesting that Sapium has evolved to be a fast-growing plant in response to the absence of herbivores in the introduced range.
Local maladaptation (e.g. to specific attack by soil pathogens to native Chinese populations) due to non-sterilized soil from the native range used in this study could have contributed to growth differences between two population types. However, this speculation is not supported for two reasons. First, we did not find any obvious root damage over the entire experiment. On the contrary, all seedlings grew healthily until the harvest. Second, the EICA hypothesis proposes that invasive populations would be more frequently attacked than native populations because they are expected to be less well defended against soil pathogens. Indeed, the results of this study strongly suggest that the growth differences between two population types of Sapium were largely due to genetic shifts in ecological and morphological traits rather than differential attacks by soil pathogens.
Although the expression of many plant traits is environment dependent, and the performance of invasive species relative to native species, or invasive populations relative to native populations of introduced plants, can differ with environments (Schweitzer & Larson 1999; Daehler 2003; DeWalt et al. 2004; Burns 2006), we did not examine plant traits under various environmental conditions in this study. However, invasive Sapium plants have showed greater performance when they were compared with native tree species under different soil nutrients, water regimes and light conditions (Rogers & Siemann 2002; Siemann & Rogers 2003c; Butterfield, Rogers & Siemann 2004). Some previous studies on Sapium indicated that greater performance and competitive ability of invasive populations relative to native populations were independent of soil nutrients (Zou et al. 2006, Zou, Rogers & Siemann, unpublished data). Lower RSR of invasive populations relative to native populations of Sapium and no significant difference in RD in this study were consistent with a previous comparative study, but they were also found to be independent of soil resource levels (Zou et al. 2006). This suggests that other genetic shifts in morphological and physiological traits found in this study may also be independent of environmental conditions.
In the past decade, a number of studies have attempted to test the EICA hypothesis, and they have produced inconsistent results (Daehler & Strong 1997; Willis & Blossey 1999; Willis, Memmott & Forrester 2000; Thebaud & Simberloff 2001; Bossdorf et al. 2005). In these EICA studies, some approaches have been used, such as examining phenotypic plasticity across different environments, genetic analysis, or comparing performance of native and invasive populations in a common garden (Bossdorf et al. 2005). Although few studies have concentrated on changes in plant morphological and physiological traits between native and invasive populations of introduced plants, investigation of shifts in plant functional traits may provide better insights into strategies that invasive plants use to achieve their fast growing rates. Thus, it could also be an effective approach for testing the EICA hypothesis and may increase our understanding of invasion mechanisms and the invasion process.
We thank Yao Huang, Lianggang Zong, Yanyu Lu and Shutao Chen for their help in collecting seeds and taking emission samples; two anonymous referees for helpful comments on the manuscript; Nanjing Agricultural University for use of greenhouse and laboratory space; and the US National Science Foundation (DEB-0315796) for support.
- 1990) The reproductive consequences associated with inducible alkaloidal responses in wild tobacco. Ecology 71, 252–262. , & (
- 1999) Leaf construction cost, nutrient concentration, and net CO2 assimilation of native and invasive species in Hawaii. Oecologia 121, 183–192. & (
- 2002) Differences in dry weight partitioning and flowering phenology between native and non-native plants of purple loosestrife (Lythrum salicaria L.). Flora 197, 332–340. & (
- 1987) Allocating resources to reproduction and defense. Bioscience 37, 52–66. , , & (
- 1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. Journal of Ecology 83, 887–889. & (
- 2005) Phenotypic and genetic differentiation in native versus introduced plant populations. Oecologia 144, 1–11. , , , , & (
- 1997) Introduction, impact on native habitats, and management of a wood invader, the Chinese tallow tree, Sapium sebiferum (L.) Roxb. Natural Areas Journal 17, 255–260. , , & (
- 2006) Relatedness and environment affect traits associated with invasive and noninvasive introduced commelinaceae. Ecological Applications 16, 1367–1376. (
- 2005) Variation in growth pattern and response to slug damage among native and invasive provenances of four perennial Brassicaceae species. Journal of Ecology 93, 322–334. , & (
- 2004) Growth of Chinese tallow tree (Sapium sebiferum) and four native trees under various water regimes. Texas Journal of Science 56, 335–346. , & (
- 2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290, 521–523. & (
- 1987) What makes a community invasible? Colonization, Succession and Stability (eds A.J.Gray, M.J.Crawley & P.J.Edwards), pp. 429–453. Blackwell Scientific Publications, Oxford. (
- 2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Annual Review of Ecology and Systematics 34, 183–211. (
- 1997) Reduced herbivore resistance in introduced smooth cordgrass (Spartina alterniflora) after a century of herbivore-free growth. Oecologia 110, 99–108. & (
- 2000) Fluctuating resources in plant communities: a general theory of invisibility. Journal of Ecology 88, 528–534. , & (
- 2004) Biomass allocation, growth, and photosynthesis of population types from the native and introduced ranges of the tropical shrub Clidemia hirta. Oecologia 138, 521–531. , & (
- 2006) Microsatellite markers for an invasive tetraploid tree, Chinese Tallow (Triadica sebifera). Molecular Ecology Notes 6, 505–507. , & (
- 2001) Photosynthesis, photoinhibition, and nitrogen use efficiency in native and invasive tree ferns in Hawaii. Oecologia 126, 345–354. & (
- 2003) Effect of exotic plant invasion on soil nutrient cycling processes. Ecosystems 6, 503–523. (
- 1958) The Ecology of Invasion by Animals and Plants. Chapman and Hall, London. (
- 2004) Comparison of native and invasive Rhododendron ponticum populations: growth, reproduction and morphology under field conditions. Flora 199, 120–133. & (
- 2005) Invasive and native Rhododendron ponticum populations: is there evidence for genotypic differences in germination and growth? Ecography 28, 417–428. & (
- 2004) Effects of photosynthetic efficiency and water availability on tolerance of leaf removal in Amaranthus hybridus. Journal of Ecology 92, 882–892. (
- 1998) Impact of the introduced grass Agrostis stolonifera on vegetation and soil faunal communities at Marion Island, sub-Antarctic. Biological Conservation 85, 223–231. , & (
- F.S. (2000) Initial effects of experimental warming on above- and belowground components of net ecosystem CO2 exchange in artic tundra. Oecologia 125, 512–520. & ,
- 2002) Toward a causal explanation of plant invasiveness: seedling growth and life-history strategies of 29 pine (Pinus) species. American Naturalist 159, 396–419. , & (
- 2006) Native and introduced populations of Solidago gigantea differ in shoot production but not in leaf traits or litter decomposition. Functional Ecology 20, 575–584. , & (
- 1992) The dilemma of plants: to grow or defend. Quarterly Review of Biology 67, 283–335. & (
- 2004) Introduced plants of the invasive Solidago gigantea (Asteraceae) are larger and grow denser than conspecifics in the native range. Diversity and Distributions 10, 11–19. , & (
- 1997) Sink-stimulated photosynthesis, increased transpiration and increased demand-dependent stimulation of nitrate uptake: nitrogen and carbon relations in the parasitic association Cscuta reflexa–Coleus blumi. Journal of Experimental Botany 48, 915–925. , & (
- 2003) Invasive California poppies (Eschscholzia californica Cham.) grow larger than native individuals under reduced competition. Ecology Letters 6, 257–264. & (
- 2001) CO2 exchange in an organic field growing barley or grass in eastern Finland. Global Change Biology 7, 679–692. , , & (
- 2002) Photosynthetic characteristics of invasive and noninvasive species of Rubus (Rosaceae). American Journal of Botany 89, 1431–1438. (
- 2001) The evolutionary impact of invasive species. Proceedings of National Academy of Sciences of the United States of America 98, 5446–5451. & (
- 2004) Can gas-exchange characteristics help explain the invasive success of Lythrum salicaria? Biological Invasions 6, 101–111. & (
- 1998) Growth, biomass allocation and photosynthesis of invasive and native Hawaiian rainforest species. Oecologia 117, 449–459. , & (
- 1997) Predicting invasions of woody plants introduced into North America. Conservation Biology 11, 193–203. & (
- 1996) What attributes make some plant species more invasive? Ecology 77, 1655–1661. & (
- 2002) Effects of simulated herbivory and resource availability on native and invasive exotic tree seedlings. Basic and Applied Ecology 3, 297–307. & (
- 2004) Invasive ecotypes tolerate herbivory more effectively than native ecotypes of the Chinese tallow tree Sapium sebiferum. Journal of Applied Ecology 41, 561–570. & (
- 2005) Herbivory tolerance and compensatory differences in native and invasive ecotypes of Chinese tallow tree (Sapium sebiferum). Plant Ecology 181, 57–68. & (
- 1990) In search of the characteristics of plant invaders. Biological Invasions in Europe and the Mediterranean Basin (eds F. diCastri, A.J.Hansen & M.Debussche), pp. 335–352. Kluwer Academic, Doedrecht. (
- 1994) Effects of herbivory on growth and biomass allocation in native and introduced species of Lonicera. Ecology 75, 1661–1672. , & (
- 1999) Greater morphological plasticity of exotic honeysuckle species may make them better invaders than native species. Journal of the Torrey Botanical Society 126, 15–23. & (
- 2002) Plasticity and gentic diversity may allow saltcedar to invade cold climates in North America. Ecological Applications 12, 1652–1660. , & (
- 2005) Influence of the obligate parasite Cuscuta campestris on growth and biomass allocation of its host Mikania micrantha. Journal of Experimental Botany 56, 1277–1284. , , , & (
- 2001) Genetic differences in growth of an invasive tree species. Ecology Letters 4, 514–518. & (
- 2003a) Reduced resistance of invasive varieties of the alien tree Sapium sebiferum to a generalist herbivore. Oecologia 135, 451–457. & (
- 2003b) Increased competitive ability of an invasive tree may be limited by an invasive beetle. Ecological Applications 13, 1503–1507. & (
- 2003c) Changes in light and nitrogen availability under pioneer trees may indirectly facilitate tree invasions of grasslands. Journal of Ecology 91, 923–931. & (
- 2001) Physiological and morphological traits of exotic, invasive exotic, and ntive plant species in tallgrass prairie. International Journal of Plant Sciences 162, 785–792. & (
- 1999) The ecology and evolution of plant tolerance to herbivory. Trends in Ecology and Evolution 14, 179–185. & (
- 2001) Are plants really larger in their introduced ranges? American Naturalist 157, 231–236. & (
- 1998) Rapid evolution as an ecological process. Trends in Ecology and Evolution 13, 329–332. (
- 1999) The ecological consequences of changes in biodiversity: a search for general principles. Ecology 80, 1455–1474. (
- 1996) The characters of successful invaders. Biological Conservation 78, 163–170. & (
- 1999) Benign environments do not explain the increased vigour of non-indigenous plants: a cross-continental transplant experiment. Biocontrol Science and Technology 9, 567–577. & (
- 2000) Is there evidence for the post-invasion evolution of increased size among invasive plant species? Ecology Letters 3, 275–283. , & (
- 2006) Aboveground productivity and root–shoot allocation differ between native and introduced grass species. Oecologia 150, 300–309. & (
- 2004) Increased susceptibility to enemies following introduction in the invasive plant Silene latifolia. Ecology Letters 7, 813–820. , & (
- 1994) Chinese Tallow Tree. China Forestry Press, Beijing (in Chinese). & (
- 2005) Contribution of plants to N2O emissions in soil-winter wheat ecosystem: pot and field experiments. Plant and Soil 269, 205–211. , , , & (
- 2004) Static opaque chamber-based technique for determination of net exchange of CO2 between terrestrial ecosystem and atmosphere. Chinese Science Bulletin 49, 381–388. , , , & (
- 2006) The effect of Chinese tallow tree (Sapium sebiferum) ecotype on soil-plant system carbon and nitrogen processes. Oecologia 150, 272–281. , , & (