Botanical Studies (2008) 49: 385-391.

*

Corresponding author: E-mail: chen-tang@zju.edu.cn;

chenxinlab@zju.edu.cn; Tel: +86-571-88206373; Fax:

+86-571-88206373.

INTRODUCTION

The competitive performance of invasive species is

often habitat-dependent (Daehler, 2003). Some invasive

species possess higher tolerance to environmental stress

(e.g., excess cations, salinity, low temperature and

pollution), which can drive the species invasion into

new ranges (Uveges et al., 2002; Kercher and Zedler,

2004; Funk and Vitousek, 2007). Experiments have

shown that tolerance to drought (Cleverly et al., 1997),

flood (Newman et al., 1996), turbidity (Thomsen and

McGlathery, 2007), and low resources (Funk and Vitousek,

2007) allowed some invasive species to outperform natives

in a stressful environment.

An exotic plant species¡¦ ability to be highly competi-

tive is widely recognized as an important attribute in plant

invasion (Bakker and Wilson, 2001; Levine et al., 2003;

Vila and Weiner, 2004; Minchinton et al., 2006). When an

exotic species is introduced, competition for limited re-

sources is probably the first interaction that the species has

with native species in the recipient community. Studies

have shown that the magnitude and outcome of such inter-

actions may shift due to disturbance or other habitat modi-

fications (Petren and Case, 1998; D¡¦Antonio et al., 1999),

resources and fluctuations in their availability (Davis et

al., 2000; Davis and Pelsor, 2001), stressful conditions

(Claassen and Marler, 1998; Daehler, 2003), and adapta-

tion of the exotic species to its new habitat in relation to its

multiple introductions (Besnard et al., 2007; Broennimann

et al., 2007; Facon et al., 2008). Thus linking biotic inter-

actions such as competition to environmental changes may

be critical to our understanding of how and why an exotic

plant species is likely to invade successfully or expand its

range.

Competitive interaction between the invasive Solidago

canadensis and native Kummerowia striata in lead

contaminated soil

Qian ZHANG, Ruyi YANG, Jianjun TANG, and Xin CHEN*

College of Life Sciences, Agroecology Institute, Zhejiang University, Zijingang Campus, Zijinhua Road, Hangzhou

310058, P.R. China

(Received January 30, 2008; Accepted June 18, 2008)

ABSTRACT.

Higher tolerance to stressful environments may result in exotic plants being more competitive

than native ones, thus promoting plant invasion. We conducted a greenhouse experiment to test this hypoth-

esis by using invasive Solidago canadensis and native Kummerowia striata as model plant species under lead

contamination. Lead was applied as Pb(AC)

2

¡P3H

2

O in solution at three levels (0, 300 mg kg

-1

and 600 mg

kg

-1

soil) to simulate control and two pollution sites on which S. canadensis was found. Invasive Solidago

canadensis, native Kummerowia striata, and their combination were grown under each Pb treatment. Under

monoculture no differences of biomass, nitrogen (N) or phosphorus (P) contents in S. canadensis were found

among treatments, but the growth of native K. striata was significantly depressed at higher soil Pb concentra -

tion. When both species were mixed, elevated soil Pb concentrations significantly increased shoot biomass

ratio of S. canadensis to K. striata, implying that Pb enhanced the competition of S. canadensis over K. stri-

ata. Compared to monoculture, biomass and N and P contents of S. canadensis significantly increased under

mixture with K. striata in each Pb treatment. Under both monoculture and mixed culture, Pb concentrations

in shoots, roots, and rhizomes of S. canadensis increased with soil Pb content, but Pb concentrations in both

above- and below-ground tissues of S. canadensis were significantly lower in mixture than that in monoculture

under each Pb treatment. Both Pb treatments and mixture with native K. striata did not change biomass al-

location to shoot, root and rhizome of S. canadensis. Evidence from our experiment supported the hypothesis

that higher tolerance to Pb stress enabled the invasive S. canadensis to outperform the native K. striata and

may have promoted its rapid invasion in Pb contaminated soil.

Keywords: Heavy metal contaminated soil; Invasive Solidago canadensis; Native Kummerowia striata;

Monoculture; Mixture.

ECOLOGY

386

Botanical Studies, Vol. 49, 2008

In the present study, we examined whether and how

soil lead pollution affects the outcome of competitive

interaction between exotic and native species, and we

used the invasive Solidago canadensis and native Kum-

merowia striata as model species. Solidago canadensis L.

(goldenrod), one of the most destructive invasive weeds in

southeastern China, was introduced from North America.

Solidago canadensis adapted well to low pH and was tol-

erant to shading, drought, and nutrient deficiency (Dong

et al., 2006; Song et al., 2007). Its response to soil N and

P, light, temperature, and soil water differed from that

of local species (Guo and Fang, 2003; Ruan et al., 2004;

Guo, 2005; Huang and Guo, 2005; Lu et al., 2005). Our

preliminary studies also showed that S. canadensis was

highly tolerant to Pb and could easily colonize and estab-

lish itself in heavy metal polluted areas (Yang et al., 2007),

but whether heavy metal could alter the interaction of S.

canadensis with native species remains a question. Kum-

merowia striata Thumb. is a Chinese native and common

weedy species in many crop fields and natural habitats

(Chen et al., 2004, 2005). Kummerowia striata also com-

monly coexists with S. canadensis in lands invaded by the

latter (Yang et al., 2007). Understanding the effects of soil

pollution stress on the interaction of invasive and native

plants will provide insights into the invasion mechanisms

of S. canadensis and possibly also into potential methods

of controlling this species.

MATERIALS AND METHODS

Soil and plant species

The soil for experiments was collected from a citrus

orchard situated at 28¢X54¡¦ N, 118¢X30¡¦ E in southwestern

Zhejiang Province, southeastern China. It was a clayey

red soil, equivalent to Ultisols in US soil taxonomy, with a

pH of 4.59 (determined in CaCl

2

). The soil had 34.4 g kg

-1

organic matter, 28.1 mg kg

-1

extractable N, 8.99 mg kg

-1

extractable P, and 108.2 mg kg

-1

extractable K. Total lead

concentration in the soil was 23.3 mg kg

-1

.

Seeds of K. striata and propagules (un-germinated

buds) of S. canadensis were collected from their natural

populations in a field in Hangzhou city, Zhejiang Province.

Experimental design

The experiment was a two-factorial design with differ-

ent Pb levels and culture types. Three levels of Pb (0, 300

and 600 mg kg

-1

soil) were used to simulate uncontami-

nated soil and two levels of Pb pollution at sites where

S. canadensis was spreading. Culture types included two

monocultures of each plant species (invasive S. canadensis

and native K. striata) and a combination of the two species

at an equal plant number (1:1). There were four replicates

for each treatment.

Mesocosms (47.5 cm ¡Ñ 34.5 cm ¡Ñ 15.4 cm) were used

in this experiment, and each was filled with 16 kg soil.

Pb was applied as lead acetate (Pb(CH

3

COO)

2

¡P3H

2

O).

Seeds and propagules were surface sterilized with 3%

NaClO before being sown in the soil. Twelve propagules

of S. canadensis, 12 seeds of K. striata and their mixture

(6 propagules and 6 seeds, respectively) were planted in

each mesocosm, and these were arranged in a greenhouse

in a completely randomized block design. Plants were

maintained under natural light and temperature conditions.

Natural air temperature varied from 18 to 30¢XC during the

experiment from April to October. Plants were watered

daily to keep soil moisture at 70-90% of water-holding

capacity. No additional nutrients were given during the ex-

periment.

Sampling and measurements

Plants were harvested 120 days after seeding. Plant

roots were washed with tap water to remove soil particles

and separated from shoots. For S. canadensis, rhizome was

separated from root and shoot. Plant samples were oven-

dried (80¢XC for 48 h) and weighed. The oven-dried sam-

ples were milled with a stainless steel micronizing miller.

Above- and below-ground plant tissues were analyzed for

their N concentrations by Kjeldahl procedures (2200 Kjel-

dahl Auto Distillation). Plant P concentrations were mea-

sured by spectrophotometry (UV-1600 spectrophotometer,

Beijing, Murphy and Riley, 1962). The fine-ground plant

samples were dried to ash at 600¢XC for 2 h and then dis-

solved in 1:1 nitric acid (Bao, 2000). Concentrations of Pb

in the solutions extracted from plant materials (recovery

rate 99.5%) were analyzed by the AAS (Atomic Absorp-

tion Spectrometry) method using an atomic absorption

spectrometer (Shimadzu Model AA-6650).

Statistical analysis

Two-way ANOVA was done for each dependent vari-

able using the general linear model (GLM) design in the

SPSS V.10.0 (SPSS Inc., Chicago). The independent

variables were Pb concentrations and types of plant cul-

ture (monoculture or mixture). Least significant difference

(LSD) at the 5% confidence level was used for comparison

between treatments.

RESULTS

Biomass

The total biomass of invasive S. canadensis under both

monoculture and mixed culture with K. striata was not af-

fected by Pb treatments (P>0.05) (Figure 1), but elevated

Pb concentration significantly reduced total biomass of

native K. striata (P<0.05). Biomass allocation to shoots,

roots and rhizomes of S. canadensis was not significantly

affected by Pb treatments under either culture condition

(P>0.05) (Figure 2a). Compared with the control, elevated

Pb treatments significantly reduced (P<0.05) biomass al-

location to roots in K. striata (Figure 2b), but no differ-

ence (P>0.05) in biomass allocation was found between

monoculture and mixed culture under any Pb treatment

(Figure 2b). In cohabitation, the shoot biomass ratio of S.

canadensis to K. striata significantly increased (P<0.05)

ZHANG et al. ¡X Interaction of invasive and native plants in contaminated soil

387

with the soil Pb concentration (Figure 3).

N and P contents in plants of S. canadensis

Pb treatments significantly increased (P>0.05) the total

N content in plants of S. canadensis under mixed culture

but not in monoculture (Figure 4a). P content in S. ca-

nadensis was significantly higher (P<0.05) in elevated Pb

treatments than in control in both monoculture and mixture

(Figure 4b). No difference in total P content was found

between monoculture and mixture under elevated Pb treat-

ments (Figure 2b), but under control, P content was sig -

nificantly higher (P<0.05) in monoculture than in mixture

(Figure 4b).

Pb concentration in shoots and roots

Shoot and root Pb concentrations in native K. striata

were significantly higher (P<0.05) than those in the inva-

sive S. canadensis, regardless of Pb treatment and culture

mode (Figures 5 and 6). Elevated soil Pb levels signifi-

cantly increased (P<0.05) Pb concentrations of the above-

and below-ground parts in both S. canadensis and K.

striata (Figures 5 and 6). Shoot, root and rhizome Pb con-

Figure 1. Shoot, root and rhizome biomass of S. canadensis and

shoot and root biomass of K. striata as affected by soil Pb treat-

ments under monoculture and mixture. CK means no Pb addition

treatment; Pb1 means 300 mg kg

-1

treatment; Pb2 means 600 mg

kg

-1

treatment. S.C means S. canadensis; K.S means K. striata.

MONO means monoculture; MIX means mixture. IDV means

individual plant. Values are means ¡Ó S.E.

Figure 2. Biomass allocation of S. canadensis and K. striata.

MONO means monoculture; MIX means mixture. S.C means S.

canadensis; K.S means K. striata. Values are means ¡Ó S.E.

Figure 3. Total shoot biomass ratio of S. canadensis to K. stria-

ta in a mesocosm under mixture. S.C means S. canadensis; K.S

means K. striata. Values are means ¡Ó S.E.

Figure 4. Nitrogen (N) and phosphorous (P) content in shoot,

root, and rhizome of individual plant of S. canadensis plant as

affected by soil Pb treatments under monoculture and mixture.

MONO means monoculture; MIX means mixture. IDV means

individual plant. Values are means ¡Ó S.E.

388

Botanical Studies, Vol. 49, 2008

centrations of S. canadensis in mixed culture were lower

(P<0.05) than those under monoculture (Figure 5), but the

reverse was true for the shoot and root Pb concentrations

in K. striata (Figure 6).

DISCUSSION

Solidago canadensis is a successful invader with a

high tolerance to shading, drought, nutrient depletion, and

Pb contamination (Dong et al., 2006; Yang et al., 2007).

Higher soil Pb did not affect its growth, but it greatly

reduced native plants under monoculture (Yang et al.,

2007). When grown in the presence of native K striata,

Pb treatments enhanced the success of S. canadensis over

K striata in our experiments. The shoot biomass ratio of

S. canandensis to K striata was 1.8 in the control with-

out Pb addition, but under higher soil Pb concentrations

the ratio increased to 4.1 (300 mg kg

-1

treatment) and 6.1

(600 mg kg

-1

treatment). This suggested that S. canadensis

gained less advantage over K. striata in terms of biomass

in normal soil while under elevated Pb soils, it became a

superior competitor. Plant species with higher competi-

tive ability often possesses a greater capacity to acquire

resources (Thorsted et al., 2006), an ability to more rapidly

occupy space (Williams, 1963; Sekimura et al., 2000), and

a higher tolerance to disturbances or environmental stress

(del-Val and Crawley, 2004; Rogers and Siemann, 2004).

The higher competitiveness of S. canadensis is probably

attributable to its higher tolerance to soil Pb than K. striata

(Yang et al., 2007), thus higher soil Pb levels could be

a crucial selective factor that enhances the growth of S .

canandensis and drives the outcome of the competitive in-

teraction in the metal contaminated soil.

One of the strategies for tolerance to metal toxicity is

that plants avoid accumulation of heavy metals through

exclusion or reducing uptake (Wei et al., 2005). In our

experiments, S. canadensis outperforming K. striata in

higher Pb soil concentrations could be probably explained

by differential Pb accumulation in exotic and native plant

species under monoculture and mixture. Pb concentrations

in the shoots, roots, and rhizomes of S. canadensis were

significantly lower under mixture than monoculture (Fig-

ure 5), and this disparity was particularly obvious under

higher Pb treatment (600 mg kg

-1

). However, for native

K. striata, shoot and root Pb concentrations were higher

under mixture than under monoculture, particularly in the

300 and 600 mg kg

-1

treatments (Figure 6). Solidago ca-

nadensis reduced or excluded Pb uptake, which resulted

in a higher Pb concentration in rhizospheric soil. This may

have enhanced the Pb uptake and accumulation by the

neighboring K. striata in the mixture. The enhanced Pb ac-

cumulation would have inhibited the growth and nutrient

(N and P) uptake of K. striata; resulting in an increase in

resources (space and nutrients) for S. canadensis. These

alterations of the rhizosphere environment may have par-

tially contributed to the increase in biomass and N and P

contents in S. canadensis under coinhabitation. One alter-

native explanation is that S. canadensis altered the rhizo-

spheric soil environment through reducing and excluding

Pb uptake in polluted soil, which had a negative impact on

K. striata and in turn favored itself.

Differences in phenotypic plasticity in characters (e.g.,

photosynthetic rate, shoot height, leaf number and area,

and biomass allocation to shoot and root) between invasive

and native species may also attribute to the aggressiveness

of exotic species (Schweitzer and Larson, 1999; Kaufman

and Smouse, 2001) although different results were found

in other experiments (Williams and Black, 1994; DeWalt

et al., 2004). Biomass allocation to functionally distinct

tissues was thought to be important in enhancing access

to a specific resource in shoot supply (Sultan, 2003). In

our experiments, we examined the biomass allocation of

Figure 6. Lead concentration in shoot (a) and root (b) of K.

striata as affected by soil Pb treatments under monoculture and

mixture. MONO means monoculture; MIX means mixture. Val-

ues are means ¡Ó S.E.

Figure 5. Lead concentration in shoot (a), root (b), and rhizome

(c) of S. canadensis as affected by soil Pb treatments under

monoculture and mixture. MONO means monoculture; MIX

means mixture. Values are means ¡Ó S.E.

ZHANG et al. ¡X Interaction of invasive and native plants in contaminated soil

389

S. canadensis under Pb contaminated conditions, with or

without the native plant. Biomass allocation to shoots,

roots, and rhizomes did not significantly change after the

addition of Pb or in the presence of K. striata, suggesting

that plasticity in biomass allocation was not an important

driving factor in Solidago¡¦s adaptation to Pb contamina-

tion.

In conclusion, our results indicated that the invasive

S. canadensis had higher Pb tolerance than the native K.

striata, probably because the former reduced its Pb uptake.

Elevated soil Pb concentrations enhanced the growth of

S. canadensis over K. striata in mixture. Neither soil Pb

nor the presence of K. striata changed the biomass alloca-

tion to shoots, roots, and rhizomes of S. canadensis. These

results supported the hypothesis that Pb contamination af-

fects the interaction between S. canadensis and K. striata,

attributable to the greater tolerance of S. canadensis to Pb

stress.

Acknowledgements. This study was supported by the

Zhejiang Provincial Natural Science Foundation of China

(No. R505024) and the Natural Science Foundation of

China (No. 30730020 and 30870405). We thank Dr. Chu

Leemin for language revision.

LITERATURE CITED

Bakker, J. and S. Wilson. 2001. Competitive abilities of intro-

duced and native grasses. Plant Ecol. 157: 117-125.

Bao, S.D. 2000. Methods of Soil Chemistry Analysis, 3rd ed.

Chinese Agriculture Science and Technology Press, Beijing.

Besnard, G., P. Henry, L. Wille, D. Cooke, and E. Chapus. 2007.

On the origin of the invasive olives (Olea europaea L.,

Oleaceae). Heredity 99: 608-619.

Broennimann, O., U.A. Treier, H. Muller-Scharer, W. Thuiller,

A.T. Peterson, and A. Guisan. 2007. Evidence of climatic

niche s hift during biological inva sion. Ecol. Lett . 10:

701-709.

Chen, X., J.J. Tang, G.Y. Zhi, and S. Hu. 2005. Arbuscular my-

corrhizal colonization and phosphorus acquisition of plants:

effects of coexisting plant species. Appl. Soil Ecol. 28:

259-269.

Chen, X., J.J. Tang, Z.G. Fang, and K. Shimizu. 2004. Effects

of weed communities with various species numbers on soil

features in subtropical orchard ecosystem. Agric. Ecosyst.

Environ. 102: 377-388.

Claassen, V.P. and M. Marler. 1998. Annual and perennial grass

growth on nitrogen-depleted decomposed granite. Restor.

Ecol. 6: 175-180.

Cleverly, J.R., S.D. Smith, A. Sala, and D.A. Devitt. 1997. Inva-

sive capacity of Tamarix ramosissima in a Mojave Desert

floodplain: the role of drought. Oecologia 111: 12-18.

D¡¦Antonio, C.M., T.L. Dudley, and M. Mack. 1999. Disturbance

and biological invasions: Direct effects and feedbacks. In L.

Walker (ed.), Ecosystems of Disturbed Ground. Amsterdam,

Elsevier, pp. 143-452.

Daehler, C.C. 2003. Performance comparisons of co-occurring

native and alien invasive plants: implications for conser-

vation and restoration. Ann. Rev. Ecol. Evol. Syst. 34:

183-211.

Davis, M.A. and M. Pelsor. 2001. Experimental support for a

resource-based mechanistic model of invasibility. Ecol.

Lett. 4: 421-428.

Davis, M.A., J.P. Grime, and K. Thompson. 2000. Fluctuating

resources in plant communities: a general theory of invis-

ibility. J. Ecol. 88: 528-534.

Del-Val, E. and M.J. Crawley. 2004. Interspecific competition

and tolerance to defoliation in four grassland species. Can. J.

Bot. 82: 871-877.

DeWalt, S.J., J.S. Denslow, and J.L. Hamrick. 2004. Biomass

allocation, growth, and photosynthesis of genotypes from

native and introduced ranges of the tropical shrub Clidemia

hirta. Oecologia 138: 521-531.

Dong, M., J.Z. Lu, W.J. Zhang, J .K. Chen, and B. Li. 2006.

Canada goldenrod (Solidago canadensis): An invasive alien

weed rapidly spreading in China. Acta Phytotaxon. Sin. 44:

72-85.

Facon, B., J.P. Pointier, P. Jarne, V. Sarda, and P. David. 2008.

High genetic variance in life-histories strategies within in-

vasive populations by way of multiple introductions. Curr.

Biol. 18: 363-367.

Funk, J.L. and P.M. Vitousek. 2007. Resource-use efficiency

and plant invas ion in low-resource s ystems. Nature 446:

1079-1081.

Guo, S.L. 2005. Solidago canadensis niche and influences of

its invasion on plant communities. J. Biomathematics 20:

91-96.

Guo, S.L. and F. Fang. 2003. P hysiological adaptation of the

invasive plant Solidago canadensis to environments. Acta

Phytotaxon. Sin. 27: 47-52.

Huang, H. and S.L. Guo. 2005. Analysis of population genetic

differences of the invasive plant Solidago canadensis. Bull.

Bot. Res. 25: 197-204.

Kaufman, S.R. and P.E. Smouse. 2001. Comparing indigenous

and introduced populations of Melaleuca quinquenervia

(Cav.) Blake: response of seedlings to water and pH levels.

Oecologia 127: 487-494.

Kercher, S.M. and J.B. Zedler. 2004. Multiple disturbances ac-

celerate invasion of reed canary grass (Phalaris arundina-

cea L.) in a mesocosm study. Oecologia 138: 455-464.

Levine, J.M., M. Vila, C.M. D¡¦Antonio, J.S. Dukes, K. Grigulis,

and S. Lavorel. 2003. Mechanisms underlying the impacts

of exotic plant invasions. Proc. Roy. Soc. B-Biol. Sci. 270:

775-781.

Lu, J.Z., W. Qiu, J.K. Chen, and B. Li. 2005. Impact of invasive

species on soil properties: Canadian goldenrod (Solidago

canadensis) as a case study. Biodiver. Sci. 13: 347-356.

Minchinton, T.E., J.C. S impson, and M.D. Bertness . 2006.

Mechanisms of exclusion of native coastal marsh plants by

390

Botanical Studies, Vol. 49, 2008

an invasive grass. J. Ecol. l94: 342-354.

Murphy, J. and J.P. Riley. 1962. A modified single solution meth-

od for the determination of phosphate in natural waters .

Anal. Chim. Acta 27: 31-36.

Newman, S., J.B. Grace, and J.W. Koebel. 1996. Effects of Nu-

trients and hydroperiod on Typha, Cladium, and Eleocha-

ris: Implications for everglades restoration. Ecol. Appl. 6:

774-783.

P etren, K. and T.J. Case. 1998. Habitat s tructure determines

competition intensity and invasion success in gecko lizards.

Proc. Natl. Acad. Sci. USA 95: 11739-11744.

Rogers, W.E. and E. S iemann. 2004. Invasive ecotypes toler-

ate herbivory more effectively than native ecotypes of the

Chinese tallow tree Sapium sebiferum. J. Appl. Ecol. 41:

561-570.

Ruan, H.G., J. Wang, H.M. Lu, G.M. Tang, and Z.M. Pu. 2004.

Study of the biological characteristics of Solidago canaden-

sis. J. Shanghai Jiaotong Univ. (Agric. Sci.) 22: 192-195.

Schweitzer, J.A. and K.C. Larson. 1999. Greater morphological

plas ticity of exotic honeysuckle s pecies may make them

better invaders than native species. J. Torrey Bot. Soc. 126:

15-23.

Sekimura, T., T. Roose, B. Li, P.K. Maini, J. Suzuki, and T. Hara.

2000. The effect of population density on shoot morphology

of herbs in relation to light capture by leaves. Ecol. Model.

128: 51-62.

Song, L.Y., G.Y. Ni, B.M. Chen, and S.L. Peng. 2007. Energetic

cost of leaf construction in the invasive weed Mikania mi-

crantha H.B.K. and its co-occurring species: implications

for invasiveness. Bot. Stud. 48: 331-338.

Sultan, S.E. 2003. Phenotypic plasticity in plants: a case study in

ecological development. Evol. Dev. 5: 25-33.

Thomsen, M.S. and K.J. McGlathery. 2007. Stress tolerance of

the invas ive macroalgae Codium fragile and Gracilaria

vermiculophylla in a s oft-bot tom turbid lagoon. Biol.

Invasions 9: 499-513.

Thorsted, M.D., J. Weiner, and J.E. Olesen. 2006. Above- and

below-ground competition between intercropped winter

wheat Triticum aestivum and white clover Trifolium repens.

J. Appl. Ecol. 43: 237-245.

Uveges, J.L., A.L. Corbett, and T.K. Mal. 2002. Effects of lead

contamination on the growth of Lythrum salicaria (purple

loosestrife). Environ. Pollut. 120: 319-323.

Vila, M. and J. Weiner. 2004. Are invasive plant species better

competitors than native plant species. Evidence from pair-

wise experiments. Oikos 105: 229-238.

Wei, S.H., Q.X. Zhou, and X. Wang. 2005. Identification of

weed plants excluding the uptake of heavy metals. Environ.

International 31: 829-834.

Williams, D.G. and R.A. Black. 1994. Drought response of a na-

tive and introduced Hawaiian grass. Oecologia 97: 512-519.

Williams, W.A. 1963. Competition for light between annual spe-

cies of Trifolium during the vegetative phase. Ecology 44:

475-485.

Yang, R.Y., J.J. Tang, Y.S. Yang, and X. Chen. 2007. Invasive

and non-invasive plants differ in response to soil heavy

metal lead contamination. Bot. Stud. 48: 453-458.

ZHANG et al. ¡X Interaction of invasive and native plants in contaminated soil

391