Botanical Studies (2007) 48: 453-458.

*

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

+86-571-88206373; Fax: +86-571-88206373.

INTRODUCTION

Solidago canadensis L. (goldenrod), which was

introduced from North America into China in the 20th

century, has become one of the most destructive invasive

weeds in south-eastern China. Solidago canadensis was

shown to be a superior competitor by producing highly

fertile seeds and propagules in its adopted land (Guo and

Fang, 2003). Experiments have shown that S. canadensis

significantly differed from the local species in response

to soil N and P, light, temperature, and water availability

(Ruan et al., 2004; Guo, 2005; Huang and Guo, 2005a; Lu

et al., 2005). For example, Dong et al. (2006) reported that

S. canadensis was well adapted to low pH soil and tolerant

to shading, drought, and low levels of nutrients. It was

also found to have colonized well in heavy metal polluted

areas. However, whether soil heavy metals interact with

the growth and spread of S. canadensis is less well known.

Plant species have shown a great many strategies in

response to heavy metal (Gerard et al., 2000; Kochian

et al., 2002). Experiments reveal that many species have

developed a variety of mechanisms to accumulate metals

(Cu, As and Zn etc.) and to resist metal stress (Kochian et

al., 2002; Yang et al., 2005). Rigola et al. (2006) reported

that Thlaspi caerulescens has specific genes related to

zinc (Zn), cadmium (Cd), and nickel (Ni) accumulation.

Sun et al. (2005) found that glutathione (GSH) may be

involved in Zn and Pb transport, hyperaccumulation/

accumulation and tolerance in mine population of Sedum

alfredii. Basic et al. (2006) showed that Cd accumulator

Thlaspi caerulescens with high Cd hyperaccumulation

capacity had better growth by developing more and bigger

leaves, taller stems, and producing more fruits and heavier

seeds. Escaping from heavy metal toxicity by reducing

or excluding the uptake of heavy metals may be another

strategy for plants to resist metal toxicity. For example,

Wei et al. (2005) found that Oenothera biennis and

Commelina communis were Cd-excluders and Taraxacum

mongolicum was a Zn-excluder. Oenothera biennis is a

potential Cd-excluder, but also a potential Cu-excluder,

implying that these weed species survived well in heavy

metal polluted soil by avoiding the uptake of metals.

Symbiotic mycorrhizae are also believed to be a

strategy of plant response to heavy metal stress (van

Tichelen et al., 2001). Diaz et al. (1996) found that

Glomus mosseae reduced Zn and Pb accumulation of

maize (Zea mays) at higher Zn and Pb treatments. Blaudez

et al. (2000) also found that under Cu, Cd, Ni, Pb and Zn

exposure, mycorrhizae enhanced the efficiency of the N

acquisition of birch (Betula pendula) seedlings and thereby

assisted plants against this metal stress. Mycorrhizal

Invasive and non-invasive plants differ in response to

soil heavy metal lead contamination

Ru-Yi YANG

1,2

, Jian-Jun TANG

1

, Yi-Song YANG

1,3

, and Xin CHEN

1,

*

1

College of Life Sciences, Zhejiang University, Agroecology Institute, 368 Zijinghua Road, Hangzhou 310058, P.R. China

2

College of Environmental Sciences, Anhui Normal University, Wuhu 241003, P.R. China

3

Yellow River Institute of Hydraulic Research, Zhengzhou 450003, P.R. China

(Received September 27, 2006; Accepted May 23, 2007)

ABSTRACT.

A greenhouse experiment was conducted to test whether and how invasive species (Solidago

canadensis) and two non¡Vinvasive plant species (Festuca arundinacea, Kummerowia striata) differed in

response to soil heavy metal lead pollution in a mesocosm system. Metal 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 a control site and two polluted

sites where S. canadensis grows. Shoot biomass and N and P uptake of the indigenous species K. striata

decreased, but those of the introduced species F. arundinacea and the exotic invasive species S. canadensis

increased in Pb polluted soils. Mycorrhizae colonization of the three species and the nodule biomass of

K. striata were reduced by elevated soil Pb concentration compared to control. Root Pb concentration in

invasive S. canadensis only accounted for 6.42%, 5.93% and 11.21% of those in non-invasive K. striata under

corresponding Pb treatments. The results suggested that rapid growth of S. canadensis in Pb polluted soil

might be due to its ability to exclude Pb or reduce the uptake of Pb compared to non-invasive species.

Keywords: Invasive plant species; Metal lead; Mycorrhizae; N and P uptake.

eCOlOgy

454

Botanical Studies, Vol. 48, 2007

fungal structures such as vesicular and hyphae may act

as biological barriers that reduce metal Cd translocation

from root to shoot of Trifolium subterraneum (Joner et al.,

2000; Tonin et al., 2001), thus decreasing plant internal

sequestration and the negative effects on plant shoot

growth.

The main hypotheses for exotic plant invasion that

have been proposed are biotic resistance (Maron and

Vila, 2001), superior competitor (Bakker and Wilson,

2001), enemy release (Keane and Crawley, 2002), and

allelopathic advantage over resident species (Callaway

and Aschehoug, 2000; Bais et al., 2003; Callaway

and Ridenour, 2004). However, many invasive plants

have shown higher abilities to use water and nutrients

under environmental stress (Blicker et al., 2002, 2003).

This means that the adaptation or tolerance to stressful

environments (water and nutrient limitation, soil pollution)

may be an important trait of the exotic invasive plant

species.

Therefore, we hypothesize that 1) invasive S .

canadensis populations grow faster than native species

under metal lead polluted soil by excluding Pb or reducing

Pb accumulation, and 2) the development of mycorrhizae

that coexisted with different plants varies in response to

heavy metal. Our objectives were to determine (1) the

differences of growth and nitrogen and phosphorus uptake

between invasive S. canadensis and non-invasive species;

(2) the difference of Pb accumulation between invasive S.

canadensis and non-invasive species.

MATeRIAlS AND MeTHODS

Soil and plant species

The soil was collected from a citrus orchard situated

at 28¢X54¡¦ N, 118¢X30¡¦ E, in the southwestern portion of

Zhejiang Province, southeastern China. It was a clayey

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

70.50% clay, 10.63% silt, 18.79% sand, and pH 4.59

(determined in KCl). The soil had 34.39 g kg

-1

organic

matter, 1.30 g kg

-1

total N, and 0.95 g kg

-1

total P. It had

48.08 mg kg

-1

extractable N, 59.50 mg kg

-1

extractable P,

and 208.23 mg kg

-1

extractable K. Pb concentration in the

soil was 23.27 mg kg

-1

.

Plant species used in this experiment were Festuca

arundinacea Schreb., Kummerowia striata Thumb.

and Solidago canadensis. Festuca arundinacea is an

introduced species that is often used as a cover plant

for lawns, roadsides, and green belts next to freeways.

Solidago canadensis is an invasive species in southern

and eastern China (Li et al., 2001; Guo and Fang, 2003).

Kummerowia striata is an indigenous species usually

coexisting with F. arundinacea and S. canadensis in the

field.

Seeds of F. arundinacea were obtained from Zhejiang

Garden Development Co., LTD (Hangzhou, China) and

seeds of K. striata were from natural populations in the

field. For S. canadensis, propagules were used in the

experiment since most of its seedlings in the field are

generated from propagules (rhizome) and not from seeds

(Huang and Guo, 2005b).

experimental design

The experiment was a randomized complete block

design with three Pb levels and four replicates. Three

levels of Pb concentration (i.e. ambient, 300 mg kg

-1

and 600 mg kg

-1

) were setup to simulate control and two

pollution sites where S. canadensis grows. Mesocosms

(47.5 cm ¡Ñ 34.5 cm ¡Ñ 15.4 cm) were used in this

experiment, and each mesocosm was filled with 16 kg

soil. Pb was added in the form of Pb(AC)

2

¡P3H

2

O aqueous

solution, and two weeks later soil samples were collected

randomly to determine Pb concentrations using the atomic

absorption spectroscopy (AAS) method (Lu, 2000). The

actual Pb concentrations of the 300 mg kg

-1

and 600 mg

kg

-1

Pb treatments were 373.93 mg kg

-1

and 623.57 mg

kg

-1

, respectively.

Seeds and propagules were surface sterilized with 3%

NaClO before being sown in the soil. Plant total density

was thinned to 30 after seedlings emerged, and each

species density remained equal. Mesocosms were arranged

in the greenhouse randomly. The plants were maintained in

natural light and temperature conditions and were watered

daily.

Sampling

The plants were harvested 6 months after seeding. The

root nodule of K. striata was collected from root and soil.

Plant roots were washed with tap water and separated

from shoot. Half of the separated root samples were fixed

in FAA (37% Formaldehyde-Glacial Acetic Acid-50%

Ethanol, 9: 0.5: 0.5, V: V: V) for quantification of AM

fungal colonization. The remaining root samples, root

nodules, and shoots were oven-dried (80¢XC for 48 h) and

weighed.

Measurements

Root samples were stained with acid fuchsin in

lactoglycerol (modified from Koske and Gemma, 1989),

and mycorrhizal colonization was quantified from 200 root

fragments using the gridline intersect method (Giovannetti

and Mosse, 1980) under a stereomicroscope at 40¡Ñ

magnification.

The oven-dried samples of root and shoot were milled

with a stainless steel micronizing miller. The fine-ground

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

dissolved in 1:1 nitric acid (Lu, 2000). Pb concentrations

in the solutions extracted from plant materials (recovery

rate 99.5%) were analyzed by the AAS method using

a Shimadzu Model AA-6650 atomic absorption

spectrometer.

Above and belowground P concentrations of plant

sample were measured spectrophotometrically (Murphy

and Riley, 1962). Plant N concentration was analyzed by

Kjeldahl procedures (2200 Kjeldahl Auto Distillation).

YANG et al. ¡X Invasive plants and metal lead contamination

455

Statistical analysis

Mycorrhizal colonization was arcsine transformed.

Normality and homoscedasticity test were performed prior

to any treatment, and then the data were submitted to one-

way ANOVA or nonparametric analysis with SAS 8.0

for Windows software (v. 8.02, SAS Institute, Cary, NC,

USA). LSD was performed for multiple comparisons of

means derived from each treatment at a significant level of

0.05.

ReSUlTS

Plant and nodule biomass

Both aboveground (shoot) and belowground (root and

rhizome) biomass of invasive and non-invasive species

differed in response to Pb contamination. Compared

to control, the biomass of S. canadensis increased, but

that of K. striata decreased under both levels of Pb soil

contamination (Figure 1). For F. arundinacea, shoot

biomass increased under 300 mg kg

-1

but decreased under

600 mg kg

-1

. In addition, the nodule biomass of K. striata

fell by 34.38% and 59.38%, respectively, under the 300

mg kg

-1

and 600 mg kg

-1

treatments compared to control.

Mycorrhizal colonization

Mycorrhizal colonization of the three species fell

under Pb contamination, but the magnitude of reduction

for S. canadensis was significantly higher than for F.

arundinacea or K. striata (Figure 2). Compared to

control, colonization of S. canadensis and F. arundinacea

decreased in both the 300 mg kg

-1

and 600 mg kg

-1

Pb

treatments, but the colonization of K. striata did not

change at 300 mg kg

-1

.

Shoot N and P contents

Shoot N and P contents of F. arundinacea and S .

canadensis increased under both the 300 mg kg

-1

and 600

mg kg

-1

Pb treatments while those of K. striata decreased

compared to control (Figures 3 and 4).

Shoot and root Pb concentration

No significant difference of shoot Pb concentration was

found among the three species under either control or the

300 mg kg

-1

and 600 mg kg

-1

Pb treatments (Figure 5a).

Compared to control, Pb treatments significantly enhanced

Pb concentration in roots of all three species. However,

Pb concentration was significantly lower in roots of S.

canadensis than in F. arundinacea and K. striata under

both control and Pb treatments (Figure 5b).

F igure 1. Aboveground (s hoot) and belowground (root and

rhizome) biomass (g

¡P

MSC

-1

) of three species as affected by Pb

treatments. Fa, Festuca arundinacea; Ks, Kummerowia striata;

Sc, Solidago canadensis; MSC, mesocosm. Error bars represent

SE.

F igure 2. Mycorrhizal colonization of three s pe cies under

control and Pb treatments. Fa, Festuca arundinacea; Ks ,

Kummerowia str iata; S c, Solidago canade ns is ; Error ba rs

represent SE.

Figure 3. Shoot N content of three species under control and Pb

treatments. Fa, Festuca arundinacea; Ks, Kummerowia striata;

Sc, Solidago canadensis; MSC, mesocosm. Error bars represent

SE.

456

Botanical Studies, Vol. 48, 2007

DISCUSSION

Invasive plant species are often characterized by their

abilities to transcend stress conditions that constrain

native species and to compete for limited resources to

obtain rapid growth (Uveges et al., 2002; Seabloom et

al., 2003; Kercher and Zedler, 2004). This was reflected

in our experiment. Although Pb concentrations in plant

roots consistently increased with soil Pb concentration, the

magnitude differed from plant to plant. For S. canadensis,

root Pb concentrations were much lower, accounting for

only 6.42%, 5.93% and 11.21% of those in the roots of K.

striata under corresponding Pb treatments (Figure 5). It

is well known that excessive heavy metal can adversely

affect plant growth, development, and reproduction

(Monni et al., 2001; Brun et al., 2003; Kim et al., 2003;

Ryser and Sauder, 2006). Therefore, the advantages

resulting from low Pb accumulation could be dramatic in

the competition with resident species. How S. canadensis

reduces its Pb uptake is still unknown. Our results showed

that K. striata acquired higher N and P contents under

ambient soil than F. arundinacea and S. canadensis

while its N and P contents were far lower than those

of S. canadensis under elevated soil Pb (Figures 3 and

4). This evidence might be partially due to the high Pb

concentration accumulated in the root of K. striata since

heavy metals may inhibit its uptake of nutrients from the

soil (Blaudez et al., 2000).

Soil nutrient availability has a

profound effect on the invasibility of a plant community

according to the fluctuating resources availability theory

(Davis et al., 2000; Davis and Pelsor, 2001; Burns, 2004).

The theory deems that a plant community becomes more

susceptible to invasion after an increase in the amount of

unused resources. Heavy metal tended to negatively affect

nutrient mineralization, and this in turn affected nutrient

availability (Vasquez-Murrieta et al., 2006). However,

the nutrients (N and P) used by K. striata also declined

significantly under Pb treatments, and therefore the amount

of unused nutrients in the soil might have increased.

Thus, S. canadensis might utilize N and P more efficiently

and would undoubtedly dominate the community under

elevated Pb soil. As with nutrient uptake, the shoot

biomass of K. striata decreased but that of F. arundinacea

and S. canadensis increased when exposed to elevated Pb

soils (Figure 1). In addition, root nodule biomass of K.

striata fell by 34.38% and 59.38%, respectively, under

the 300 mg kg

-1

and 600 mg kg

-1

Pb treatments. The loss

of symbionts would inevitably have further influence

on nitrogen fixation. A causal relationship between Pb

accumulation, nutrient uptake, and plant growth is very

likely. Solidago canadensis gained no advantage over,

and was even inferior to, K. striata in terms of growth

and nutrient uptake under ambient soil, but it became

a superior competitor under elevated Pb soils. In other

words, ecophysiological traits and invaded soil properties

facilitated the invasion of S. canadensis. This implies that

Pb-polluted soil may be more vulnerable to invasion by S.

canadensis.

Mycorrhizae were shown to protect host plants against

metal toxicity by enhancing P uptake (van Tichelen

et al., 2001; Chen et al., 2005), but in our experiment,

mycorrhizal colonization decreased in all three plant

species under elevated Pb treatments, and the magnitude

of the mycorrhizal colonization decrease was higher in S.

canadensis than in K. striata and F. arundinacea (Figure

2). Mycorrhizal colonization did not correlate with the

nutrient uptake or Pb exclusion of S. canadensis, and this

did not support our hypothesis.

In conclusion, the invasive species S. canadensis

and non-invasive species K. striata and F. arundinacea

differed in response to soil Pb pollution. Although no

significant difference of shoot Pb concentration was

evident among the three species, Pb concentrations in

Figure 4. Shoot P content of three species under control and Pb

treatments. Fa, Festuca arundinacea; Ks, Kummerowia striata;

Sc, Solidago canadensis; MSC, mesocosm. Error bars represent

SE.

Figure 5. Shoot (a) and root (b) Pb concentration of three species

under control and Pb treatments. Fa, Festuca arundinacea;

Ks, Kummerowia striata; Sc, Solidago canadensis; Error bars

represent SE.

YANG et al. ¡X Invasive plants and metal lead contamination

457

roots of K. striata were much higher than in the roots

of S. canadensis. Mycorrhizae of all these species were

inhibited by higher Pb concentration in soils. The above

and belowground biomass and the N and P uptake of S.

canadensis increased but those of K. striata decreased

under elevated Pb soils. This suggests that rapid growth of

S. canadensis in Pb polluted soil might be due to its ability

to exclude Pb or reduce the uptake of Pb.

Acknowledgements. This study was supported by

the Natural Science Foundation of Zhejiang Province

(NSFZJ No. R 505024) and the National Natural Science

Foundation of China (NSFC, No.39870149, 30228005,

and 30030030).

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