Enhanced allelopathy and competitive ability of invasive plant Solidago canadensis in its introduced range
ABSTRACT Allelochemical contents (total phenolics, total flavones and total saponins) and allelopathic effects were greater in S. canadensis sampled from China than those from the USA as demonstrated in a field survey and a common garden experiment. Inhibition of K. striata germination using S. canadensis extracts or previously grown in soil was greater using samples from China than from the USA. The competitive ability of S. canadensis against K. striata was also greater for plants originating from China than those from the USA. Allelopathy could explain about 46% of the difference. These findings demonstrated that S. canadensis has evolved to be more allelopathic and competitive in the introduced range and that allelopathy significantly contributes to increased competitiveness for this invasive species.
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ABSTRACT: Allelopathy, plant–plant interactions mediated through chemical production, is an active area of ecological research. Despite this widespread interest, we still lack community scale information on the prevalence of this interaction and the types of species that may be expected to be allelopathic. To address this research need, the allelopathic potential of 65 plant species from all stages of succession in the Piedmont region of New Jersey, USA, was determined with laboratory bioassays. The strength of each species’ allelopathic activity was then related to life form, origin, and fundamental plant traits. The vast majority of species tested exhibited significant allelopathic effects in the bioassays, with many of these having fairly strong effects. Overall, the allelopathic potential of species decreased with life span, roughly following the successional transitions from short-lived to long-lived herbs and to woody species. Herbaceous species on average were more allelopathic than woody species, but there was no difference between native and non-native species once life form was accounted for. In a principal components analysis, allelopathy was associated with other plant traits, but these relationships differed between woody and herbaceous species. Allelopathic potential was positively associated with plant height in herbaceous species, but negatively associated with height, leaf mass, and seed mass in woody species. These results indicate that allelopathy may be a quite common ecological strategy in plants and is equally common in both native and non-native species. The linkage of allelopathy with other plant functional traits suggests that allelopathy can and should be integrated into the broader suite of plant strategies that are studied.Plant Ecology 06/2014; 215(6). · 1.64 Impact Factor
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Enhanced allelopathy and
competitive ability of invasive
plant Solidago canadensis in its
Yongge Yuan1,†, Bing Wang1,†, Shanshan Zhang1,4,†,
Jianjun Tang1, Cong Tu2, Shuijin Hu2, Jean W. H. Yong3
and Xin Chen1,*
1 College of Life Sciences, Zhejiang University, Hangzhou 310058, China
2 Department of Plant Pathogen, North Carolina State University, Raleigh, NC 27695, USA
3 Singapore University of Technology and Design, 279623 Singapore
4 Yunnan Academy of Forestry, Kunming 650200, China
*Correspondence address. College of Life Sciences, Zhejiang University, No. 866 Yuhangtang Road, Hangzhou
310058, Zhejiang Province, China. Tel: +86-571-88206373; Fax: +86-571-88206373; E-mail: email@example.com
†These authors equally contribute to this work.
Why invasive plants are more competitive in their introduced range
than native range is still an unanswered question in plant invasion
ecology. Here, we used the model invasive plant Solidago canaden-
sis to test a hypothesis that enhanced production of allelopathic
compounds results in greater competitive ability of invasive plants
in the invaded range rather than in the native range. We also exam-
ined the degree to which the allelopathy contributes increased com-
petitive ability of S. canadensis in the invaded range.
We compared allelochemical production by S. canadensis growing
in its native area (the USA) and invaded area (China) and also by
populations that were collected from the two countries and grown
together in a ‘common garden’ greenhouse experiment. We also
tested the allelopathic effects of S. canadensis collected from either
the USA or China on the germination of Kummerowia striata (a
native plant in China). Finally, we conducted a common garden,
greenhouse experiment in which K. striata was grown in monocul-
ture or with S. canadensis from the USA or China to test the effects of
allelopathy on plant–plant competition with suitable controls such
as adding activated carbon to the soil to absorb the allelochemicals
and thereby eliminating any corresponding allopathic effects.
Allelochemical contents (total phenolics, total flavones and total
saponins) and allelopathic effects were greater in S. canadensis
sampled from China than those from the USA as demonstrated in a
field survey and a common garden experiment. Inhibition of K. stri-
ata germination using S. canadensis extracts or previously grown
in soil was greater using samples from China than from the USA.
The competitive ability of S. canadensis against K. striata was also
greater for plants originating from China than those from the USA.
Allelopathy could explain about 46% of the difference. These find-
ings demonstrated that S. canadensis has evolved to be more allelo-
pathic and competitive in the introduced range and that allelopathy
significantly contributes to increased competitiveness for this inva-
Keywords: allelopathy • biogeographical approach • common
garden experiment • competition • invasion species
Received: 25 June 2012 Revised: 14 September 2012 Accepted: 29
Why invasive plants are often more competitive in their
introduced range than in their native range has been a central
question in understanding plant invasive biology (Blossey and
Nötzold 1995; Siemann and Rogers 2001; Siemann and Rogers
2003a; Wendy et al. 2008). Researchers have offered various
hypotheses to explain the increased competitive ability of
Journal of Plant Ecology Advance Access published October 31, 2012
at Zhejiang University on October 31, 2012
Page 2 of 11 Journal of Plant Ecology
invasive plant species (Elton 1958; Blossey and Nötzold 1995;
Callaway and Aschehoug 2000; Stockwell et al. 2003), and
these include phenotypic plasticity (Thompson et al. 1991a;
Thompson et al. 1991b; Thompson et al. 1991c; Williams et al.
1995), release from natural enemies (Elton 1958; Maron et al.
2004), evolution of increased competitive ability (Blossey and
Nötzold 1995; Stockwell et al. 2003) and the production of
allelopathic compounds (Callaway and Aschehoug 2000; Bais
et al. 2003).
Phenotypic plasticity of invasive plants has traditionally
been considered a key factor in helping invasive plants to
adapt to novel environments and compete against native
plants in recipient communities. For example, phenotypic
plasticity enabled the exotic plant species Spartina anglica to
invade and rapidly colonize new areas (Thompson et al. 1991a,
Thompson et al. 1991b, Thompson et al. 1991c). Similarly,
the exotic plant Pennisetum setaceum exhibited pronounced
morphological variation in different habitats, allowing itself
to become dominant across diverse habitats in the introduced
range (Williams et al. 1995).
The success of some invasive plants in the new range may
depend on the absence of natural enemies, which allows
these plants to reallocate energy and resources from produc-
ing ‘defensive weapons’ towards growth (Blossey and Nötzold
1995). Thus, in the new range, exotic plants may have evolved
a reduction in defense and an increase in growth or repro-
duction that may enhance their competitive ability (Blossey
and Nötzold 1995). Evidence for increased size and growth
in invasive species is common (Siemann and Rogers 2001,
Siemann and Rogers 2003a; Siemann and Rogers 2003b;
Wolfe 2002; Jakobs et al. 2004; Müller and Martens 2005).
Experiments have also demonstrated that about half of the
reported invasive species have greater competitive ability in
the introduced range than in the original range (Bossdorf et al.
2005). However, the trade-off between defense and growth
of invasive plants remains unclear. While Ridenour et al.
(2008) reported that the invasive species Centaurea maculosa
did not reduce investments in defense while evolving com-
petitive traits during its invasion, Feng et al. (2009) found that
the invasive species Ageratina adenophora in China evolved a
reduced allocation to cell walls (which should reduce defense)
and an increased allocation of N to photosynthesis (which
should increase growth).
Allelopathy refers to the effects of one plant on another
plant or organisms through the release of chemicals into the
environment (Muller 1969; Callaway 2002; Bais et al. 2003;
Hierro et al. 2003). Allelopathy has both defensive and com-
petitive characteristics in many invasive plants (Hubbell et al.
1983; Watling et al. 2011; Mallik and Pellissier 2000; Bais
et al. 2003; Callaway and Ridenour 2004; Prati and Bossdorf
2004; Stinson et al. 2006; Jarchow et al. 2009). Some inva-
sive plants exude allelochemicals into the soil to both inhibit
soilborne pathogens and defend against disease (Kumar et al.
2010; Wu et al. 2010; Zhang et al. 2009, Zhang et al. 2011;
Mitrovic et al. 2012); others produce allelochemicals to repel
insects (Farooq et al. 2011; Glinwood et al. 2011; Watling et al.
2011). Allelopathy can also mediate competitive interactions
between plants (Jarchow et al. 2009; Bais et al. 2003; Callaway
and Ridenour 2004; Prati and Bossdorf 2004; Stinson et al.
2006). Experiments have indicated that chemicals released
by some invasive plant species are more active against native
plant species in the introduced range than against co-evolved
species in the native range, which has suggested the ‘novel
weapons hypothesis’ or ‘allelopathic advantage against resi-
dent species hypothesis’ (Rabotnov et al. 1982; Hierro and
Callaway 2003; Cappuccino and Arnason 2006) and which
helps explain why some invasive species are able to outcom-
pete native plants in the introduced plant community. For
example, the allelochemical 8-hydroxyquinoline released by
Centaurea diffusa, (Vivanco et al. 2004), (±)-catechin released
by Centaurea maculosa (Callaway and Aschehoug 2000) and
7,8-benzoflavone released by Acroptilon repens (Alford et al.
2007) had allelopathic effects on the native plants in the intro-
duced ranges. When allelochemicals enhance the competitive
ability of invaders against native plants, they might maintain
or even enhance the production of allelopathic compounds
in the new range (Bossdorf et al. 2005; Ridenour et al. 2008).
In the current research, using Solidago canadensis L. (golden-
rod) as a model invasive plant, we tested the hypothesis that
an invasive plant may enhance its production of allelopathic
compounds and allelopathic effects and thereby enhancing its
competitive ability in the invaded land.
Solidago canadensis, originating from North America (Weber
1997), is an invasive weed of southeastern China (Dong et al.
2006). Solidago canadensis has a strong allelopathic effect on
local plants of China (Yang et al. 2007; Abhilasha et al. 2008).
We compared the contents of three major allelochemicals
(total flavones, total phenolics and total saponins, Zhang et al.
2011), the allelopathic effects and the competitive effects of
S. canadensis collected from the native area (the USA) and
from the invaded area (China) by employing a comparative
biogeographical approach (Hierro et al. 2005) that included
a field survey and experiments including common garden
The perennial herb S. canadensis forms large colonies that
reduce the abundance of native vegetation in southern China.
Although rapid growth and prolific reproduction (both sexual
and asexual) clearly contribute to its successful invasion, its
strong allelopathic effects on native plants (Yang et al. 2007),
arbuscular mycorrhizal fungi that form symbioses with native
plants (Zhang et al. 2007) and soilborne pathogens (Zhang
et al. 2009; Zhang et al. 2011) may also contribute to its
invasiveness. Here, we determined whether allelopathy of
S. canadensis is greater in the introduced range than in the
native range (field survey and Experiments 1 and 2) and the
degree to which enhanced allelopathy affects its competitive
ability (Experiment 3).
at Zhejiang University on October 31, 2012
Yuan et al. | Allelopathy and competitive ability in an invasive species Page 3 of 11
Field survey: Growth and production of
allelopathic chemical by S. canadensis in its native
and introduced range
We conducted a field survey to test whether allelopathic com-
pound production by S. canadensis is greater in the introduced
area (China) than in the native area (the USA). We sampled
14 populations from North Carolina, USA and six populations
from Zhejiang Province, China (Table S1). Average monthly
temperature and precipitation during the growth period of
S. canadensis (from March to November) in sampling areas
from two countries were similar (Fig. S1). Soil conditions of
sampling sites are shown in Table S1. Samples were carefully
identified taxonomically based on four morphological charac-
teristics that included basal leaves, triple-nerved leaves, stem
and inflorescence as described by Patricia et al. (1980).
Shoot height and population density were measured in a
1 × 1-m area in each sampling site. Ten plants at each sampling
site were collected. Shoots, seeds, and roots of these 10 plants
were separated. Shoots and roots were dried at 65°C until
constant mass was achieved, and seeds from 20 individual
plants per population were air dried and stored at 4°C until
they were used for the experiments.
The crude extracts from both belowground and above-
ground parts of S. canadensis were prepared as described by
Zhang et al. (2009) and were used to determine the concen-
trations of total flavones, total phenolics and total saponins.
Total flavones in the crude extracts were determined by the
NaNO2-Al(NO3)3-NaOH colorimetric assay with rutin as the
reference substance (Harborne 1973; Yang et al. 2007). Total
phenolic acids were measured by the Folin-Ciocalteu assay
with gallic acid as the reference substance (Harborne 1989a,
Harborne 1989b). Total saponins were detected by using van-
illin-HClO4 as the chromogenic reagent (Liang et al. 2008).
The extracts were then used in Experiment 1, as described in
the next section.
Experiment 1: Allelopathic effects of S. canadensis
(collected from China vs. the USA) extracts on
seed germination of a native plant
The effect of S. canadensis extracts collected in the field sur-
vey on seed germination was examined using sand culture
as described by Zhang et al. (2009). Briefly, the crude extracts
from S. canadensis collected in China and the USA were diluted
with sterilized water to a concentration of 3.75% (w/v), and
40 ml of the diluted extract was added to pots containing
150 g of sterilized sand; the final concentration of extract in
each pot was 1% (w/w). Thirty seeds of Kummerowia striata
(Thunb.) Schindl., which is a native plant in China, were
sown in each pot. Five replicate pots were used for each
crude extract. All pots were kept in a growth chamber (Safe
Experimental Instrument Company, Haishu, Ningbo, China)
with a 16-h-light and 8-h-dark photoperiod, 18°C (night) and
22°C (day) temperature regime, and 90% relative humid-
ity. After seeds were sown, Hoagland’s nutrient solution was
added to maintain normal seedling growth. The frequencies
of successful seed germination were recorded for 21 days.
Germination rate was calculated by dividing the number of
germinated seeds by the number of sown seeds and multiply-
ing by 100.
Data pertaining to aboveground biomass, height and con-
centrations of allelochemicals (total flavones, total pheno-
lics and total saponins) for plants in the survey as well as
allelopathic effects (seed germination rate of K. striata) in
Experiment 1 were first subjected to a homogeneity test and
then to a nested ANOVA to determine sources of variation.
We treated country (China vs. the USA) as a fixed effect and
populations within each country as random effects. When
ANOVAs were significant, mean values were compared by
least significant difference (LSD) at the 5% significance level.
SPSS (V.16.0) was used for all statistical analyses in this study.
Experiment 2: Common garden, greenhouse
experiment with plant populations collected
from the USA and China: allelochemical
production and allelopathic effects on seed
We conducted a greenhouse experiment in China to measure
the differences in allelopathy caused by S. canadensis collected
from the USA and China. As there was no significant differ-
ence of allelochemicals among the 14 US populations (total
phenolics, P = 0.725; total flavones, P = 0.246; total saponins,
P = 0.580), and among the six populations in China (total
phenolics, P = 0.18; total flavones, P =0.691; total saponins,
P = 0.114), we chose three populations from the USA and
three from China for this experiment. For China, we selected
sample 1, 2 and 6 from three habitats (river side, road site
and waste land, Table S1). For the USA, we selected sample
5, 6 and 7 also from three habitats (forest edge, rail site and
waste land, Table S1). The experimental set up had a split-plot
design, with country (the USA and China) as main plots and
populations as sub-plots. There were eight replicates for each
population, yielding a total of 48 (3 populations per country ×
2 countries × 8 replicate) pots. The soil used in the experi-
ment was collected from Cixi City, Zhejiang Province, China
(30°18′N, 121°10′E), where S. canadensis has invaded. The
soil had a pH of 5.7 (in a 2.5:1 suspension of KCl aqueous
solution:soil) and contained 29.8 g kg−1 organic matter, 1.14 g
kg−1 nitrogen and 5.7 mg kg−1 extractable phosphorus.
To ensure the consistency of plants in Experiment 2, the
seeds were germinated and pre-cultured in a plastic mesh
plate with vermiculite and peat in the greenhouse with natu-
ral light and temperature. When seedlings were 4 cm tall, they
were transplanted into 750-cm3 plastic pots containing 1 kg
soil. The pots were arranged in a completely randomized split-
plot design in the greenhouse and were irrigated with deion-
ized water every day but were not fertilized. Six months after
transplanting, the plants were harvested. Aboveground tissue
for each plant was cut at the root–shoot junction and dried at
65°C until constant mass was achieved, and then biomass was
at Zhejiang University on October 31, 2012
Page 4 of 11 Journal of Plant Ecology
determined by weighing. Pots were placed at 4°C until the
roots could be washed (within 1 week). Belowground tissue
was harvested by washing the soil particles off the roots/rhi-
zomes with water. Belowground tissue was dried at 65°C until
constant mass was achieved. The same soil type was further
used for a germination experiment as described below.
Crude extracts from aboveground and belowground tis-
sues of S. canadensis were prepared as described in the field
survey. The contents of allelochemicals (total flavones, total
phenolics and total saponins) in crude extracts in S. canaden-
sis (Experiment 2A) and the allelopathic effects on the ger-
mination of K. striata seeds in sand (Experiment 2B) were
also tested as described in the field survey. In addition, the
soil in the original pots was used in another germination test
(Experiment 2C) as described in the next paragraph.
For Experiment 2C, the soil in each pot was divided into
two parts, and activated carbon was mixed into one part but
not the other. Activated carbon is able to absorb allelochemi-
cals (Ridenour and Callaway 2001; Wurst and van Beersum
2009) and was used to create lower levels of allelochemicals in
the experiment. Seeds of K. striata were planted in each sub-
plot. This factorial experiment had two main effects—country
(the USA vs. China) and activated carbon (±). Germination
was assessed as described for the Experiment 1.
Differences in the aboveground biomass, height and
concentrations of allelochemicals (total flavones, total
phenolics and total saponins) as well as in allelopathic effects
(seed germination rate of K. striata) as affected by country of
origin were analyzed using nested ANOVAs. All factors were
considered as fixed effects except population (country), which
was analyzed as a random effect. When allelopathic effects
(seed germination rate of K. striata) within each country were
compared for pots with and without activated carbon, a two-
way ANOVA in the general liner model was used.
Germination rates were arcsine transformed to satisfy vari-
ance assumptions before ANOVAs were performed. When
ANOVAs were significant, mean values were compared by
LSD at the 5% significance level.
Experiment 3: effects of allelopathy on
A common garden, greenhouse experiment (Experiment
3) was performed to determine whether enhanced allelopa-
thy contributes to the competitive ability of S. canadensis. This
experiment used the same populations from the USA and
China that were used for Experiment 2. The forb K. striata was
used as the native competitor. K. striata is a common weed in
crop fields, orchards and abandoned land (Chen et al. 2004)
and usually occurs in areas invaded by S. canadensis. In our pre-
liminary three-year field observation in China, we found that
K. striata was replaced gradually by S. canadensis in the K. striata-
dominated weed communities (Zhang et al. 2011). Also, from
our field surveys carried out in the USA, we found that K. stri-
ata and S. canadensis coexist in weed communities. Thus, we
selected this legume as the reference native plant for this study.
The experiment had a split-plot design with country (the USA
and China) as the main plots, activated carbon (±) as the sub-
plots, population as the sub-sub-plots and culture types (mon-
ocultures of invasive or native and mixtures of invasive and
native) as the sub-sub-sub-plots. Five replicate microcosms for
each treatment yielded a total of 130 microcosms. Each micro-
cosm measured 20 × 15 × 20 cm (length × width × height) and
contained 6 kg of soil. The soil was same as used in Experiment 2.
To ensure the initial consistency of plants in the experiment,
the seeds were germinated and pre-cultured as described
in the Experiment 2. Two 4-week-old seedlings were trans-
planted into each microcosm so that the microcosm would
contain one of the following: two S. canadensis seedlings, two
K. striata seedlings or one seedling from each species. For car-
bon treatment, finely ground activated carbon was mixed into
the soil at a rate of 20 ml l−1.
Microcosms were arranged in a greenhouse in a completely
randomized block design. Plants were watered daily. No addi-
tional nutrients were added. Experiment 3 was terminated
6 months after transplanting, which coincided with floral ini-
tiation. We separated the shoots from roots. All shoots were
oven dried to obtain constant mass for the measurement of
dry shoot biomass.
The aggressivity indices of plants (Scheublin et al. 2007;
Zhang et al. 2010) were calculated using the shoot biomasses
of K. striata and S. canadensis in monoculture and mixture. The
aggressivity index is given as (Yij/Yii) – (Yji/Yji), where Yij and
Yii are the shoot biomasses of K. striata in mixture and mono-
culture and Yji and Yjj are the shoot biomasses of S. canaden-
sis in mixture and monoculture, respectively. The lower the
aggressivity index, the more competitive is S. canadensis com-
pared with K. striata.
The allelopathic contribution to S. canadensis’s competitive-
ness was calculated as the difference between K. striata bio-
mass in the ‘S. canadensis + K. striata with activated carbon’
treatment and K. striata biomass in the ‘S. canadensis + K. striata
without activated carbon’ treatment divided by the difference
between K. striata biomass in the ‘K. striata monoculture with-
out activated carbon’ treatment and K. striata biomass in the
‘S. canadensis + K. striata without activated carbon’ treatment
(Ridenour and Callaway 2001).
Aggressivity indices of S. canadensis (the USA or China) and
the effects of activated carbon on biomass under monocul-
ture or mixed culture were compared with two-way ANOVAs
using the general liner model. The effect of activated carbon
treatments on K. striata biomass was compared with a one-
way ANOVA. We used a nested ANOVA when comparing
the variation in biomass, aggressivity indices and allelopathic
contributions of S. canadensis from the USA and China with
or without activated carbon. The variation in K. striata bio-
mass, when grown with S. canadensis from the USA or when
grown with S. canadensis from China, was also compared using
a nested ANOVA. All factors were considered as fixed effects
except for the population (country) variable, which was ana-
lyzed as a random effect.
at Zhejiang University on October 31, 2012
Yuan et al. | Allelopathy and competitive ability in an invasive species Page 5 of 11
Allelopathic contributions were arcsine transformed to
satisfy the variance assumptions before ANOVAs were per-
formed. When ANOVAs were significant, mean values were
compared by using the LSD at the 5% significance level.
Growth and allelopathy of S. canadensis in or from
its non-native and native range (field survey and
Experiments 1 and 2)
In the field surveys, plants in six non-native populations of
S. canadensis from China were significantly taller and had
significantly more biomass than the plants in the 14 native
populations from the USA (for plant height, F1, 14 = 50.77,
P = 0.000; for biomass, F1, 14 = 74.50, P = 0.000) (Fig. 1).
Results from the first common garden experiment also
showed that China’s S. canadensis plants were taller and had
more biomass than S. canadensis plants from the USA (for plant
height, F1, 4= 11.439, P = 0.028; for biomass, F1, 4 = 12.735,
P = 0.024) (Fig. 1).
In the field survey, concentrations of three main groups of
allelochemicals (total phenolics, total flavones and total sapo-
nins) were greater in extracts isolated from S. canadensis plants
grown in China than those grown in the USA (P < 0.05,
Fig. 2a). The same was true when S. canadensis populations
originating from China and the USA were grown under
common garden, greenhouse conditions in Experiment 2A
(P < 0.05, Fig. 2b).
In Experiment 1, K. striata germination rates were lower
in sand treated with extracts from S. canadensis grown in
China, rather than those grown in the USA (for aboveground
extracts, F1, 14 = 11.563, P = 0.028; for belowground extracts,
F1, 14 = 12.367, P = 0.023) (Fig. 3a).
In Experiment 2B, germination rates of K. striata in sand
were also lower when the sand was previously treated with
extracts of greenhouse-grown S. canadensis of Chinese origin
rather than those of US origin (for aboveground extracts, F1, 4 =
10.243, P = 0.037; for belowground extracts, F1, 4 = 9.287,
P = 0.039) (Fig. 3b).
In the common garden Experiment 2C, K. striata germina-
tion was 13.8% lower in soil (from the Experiment 2) pre-
grown with S. canadensis from China than that from the
USA when receiving no activated carbon (P < 0.05, Fig. 4).
However, the addition of activated carbon eliminated the
differences in germination caused by S. canadensis from both
China and the USA (P > 0.05, Fig. 4) and demonstrated
increased germination rates (P < 0.05).
Effects of S. canadensis allelopathy on competition
Adding activated carbon to soil significantly reduced
S. canadensis shoot biomass in monoculture whether the plant
populations were from the USA (F1, 21 = 16.078, P = 0.001)
or China (F1, 18 = 9.429, P = 0.007) but did not change the
biomass in mixed culture with K. striata (for S. canadensis from
the USA, F1, 26 = 2.368, P = 0.136; for S. canadensis from China,
F1, 25 = 0.022, P = 0.883) (Fig. 5).
Biomass was always greater for S. canadensis from China
than those originating from the USA either under monocul-
ture (without activated carbon, F 1, 4 = 32.875, P = 0.005; with
activated carbon, F 1, 4 = 8.677, P = 0.042) or under mixed cul-
ture (without activated carbon, F 1, 4 = 8.345, P = 0.045; with
activated carbon, F 1, 4 = 5.373, P = 0.082) (Fig. 5).
Unlike the biomass of the invasive S. canadensis growing
under monoculture, the biomass of native K. striata under
monoculture was enhanced by activated carbon (F1, 7 =
Figure 1: Plant height (a) and the aboveground biomass (b) of
S. canadensis from either the USA or China in a field survey and a
common garden experiment (Experiment 1). Values are mean values
± SE; circles represent population mean values; * indicates P < 0.05;
** indicates P < 0.01.
at Zhejiang University on October 31, 2012
Page 6 of 11 Journal of Plant Ecology
9.561, P = 0.018) (Fig. 5). When grown in mixed culture with
S. canadensis from China, K. striata biomass was enhanced by
activated carbon (F1, 23 = 4.737, P = 0.040) (Fig. 5). The acti-
vated carbon treatment, however, did not affect K. striata bio-
mass when grown in mixed culture with S. canadensis from
the USA (F1, 26 = 1.031, P = 0.319) (Fig. 5).
In mixed culture, K. striata biomass differed depending
on the origin of S. canadensis. Without the addition of acti-
vated carbon, K. striata biomass was lower with S. canaden-
sis from China than with S. canadensis from the USA (F1, 4 =
69.637, P =0.002; Fig. 5). With the addition of activated
carbon, however, K. striata biomass was similar regardless
of the origin of S. canadensis plants (F1, 4 = 0.055, P = 0.825)
S. canadensis’s competitive ability can be demonstrated
using the aggressivity index, which was based on shoot bio-
mass data. A higher competitive ability is illustrated by a
more negative aggressivity index. Without adding activated
carbon, the aggressivity index was lower (more negative)
for S. canadensis from China than those from the USA (F1,
12 = 17.146, P = 0.001) (Fig. 6), indicating that S. canadensis
from China had greater competitive ability against K. striata
than S. canadensis from the USA. With the addition of acti-
vated carbon, however, the aggressivity indices did not dif-
fer between S. canadensis from China and that from the USA
(F1, 4 = 0.049, P = 0.836) because activated carbon signifi-
cantly increased the aggressivity index of S. canadensis from
China (F1, 10 = 7.353, P = 0.022) but not of S. canadensis
from the USA (F1, 22 = 0.035, P = 0.854) (Fig. 6). The latter
finding indicates that addition of activated carbon reduced
the competitive ability of S. canadensis from China.
In Experiment 3, the contribution of allelopathy to the
competitive ability of S. canadensis against K. striata was greater
for S. canadensis from China than for S. canadensis from the
USA (P <0.05), whether the assessment was based on root
biomass, shoot biomass, or total biomass (Fig. 7).
Comparative biogeographical approach offers ample opportuni-
ties to study exotic plant invasions (Hierro et al. 2005). In our
study, although S. canadensis has a number of congeners and
Figure 2: Concentrations of the three group allelochemicals (total
phenolics, TP; total flavones, TF; total saponins, TS) in aboveground
and belowground parts of S. canadensis from either the USA or
China in the field survey (a) and common garden conditions in the
Experiment 2A (b). Circles represent population mean values; values
are mean values ± SE; * indicates P < 0.05; ** indicates P < 0.01.
Figure 3: The germination rate of K. striata in sand as affected by
aboveground and belowground extracts of S. canadensis obtained from
either the USA or China in the field survey (a) and common garden
conditions in Experiment 2B (b). Circles represent population mean
values; values are mean values ± SE; * indicates P < 0.05.
at Zhejiang University on October 31, 2012
Yuan et al. | Allelopathy and competitive ability in an invasive species Page 7 of 11
the taxonomy within the genus Solidago remains complex (Wu
et al. 2005), we managed to find some unique characteristics
in S. canadensis that are reliable and helped us to distinguish
S. canadensis from congeners and some other similar species
in the field (Patricia et al. 1980). In a previous experiment, we
confirmed that the populations from USA and China were
S. canadensis by employing careful morphological studies (Zhang
2011). Thus, in this study, we identified and collected the ‘right’
samples of S. canadensis in the field using four distinctive mor-
phological characteristics (Patricia et al. 1980; Zhang 2011).
Our field survey indicated that S. canadensis grows larger in the
introduced range than in the native range, and the first com-
mon garden experiment provided some evidence to support the
genetic basis of the observed growth difference. Other studies
have shown that most invasive plant species either evolve a
more rapid growth rate or exhibit greater phenotypic plasticity
in the new habitats (Mooney and Cleland 2001; Carroll et al.
2005; Sax et al. 2007; Prentis et al. 2008). Invasive Chinese tal-
low trees, e.g., are larger in size in the introduced range than
within their native range (Siemann and Rogers 2001), and the
invasive plant Lepidium draba also has greater shoot and root
biomass and numbers of ramets in the introduced range than in
the native range (Müller and Martens 2005). As in the present
study, the latter two studies included common garden experi-
ments that indicated that these phenotypic differences had a
probable genetic basis. These post-invasion, genetic-based dif-
ferences are likely to help the invasive plants to compete against
their native neighbors. In the case of the invasive plant Solidago
gigantea (Asteraceae), the biomass is larger and the sexual and
vegetative reproductive efforts were greater when growing in
the invasive range than in the native range (Jakobs et al. 2001;
Jakobs et al. 2004). Once established in an area, the rapid veg-
etative reproduction enables S. gigantea to compete strongly
against its neighbors.
Our results from field survey and common garden experi-
ment showed that the contents of the three kinds of allelo-
pathic chemicals in S. canadensis were greater for plants in the
invaded range than in the native range. These three chemi-
cals (total flavones, total phenolics and total saponins) are the
main allelochemicals produced by S. canadensis (Zhang et al.
2006; Mert-Türk 2006), which are known to play important
roles in plant defense and allelopathic inhibition (Elliger et al.
1980; Inderjit 1996; Harborne and Williams 2000; Mert-Türk
2006; Kim and Lee 2011). For example, Kim and Lee (2011)
found that the total phenolic compounds of invasive spe-
cies reduced radicle growth of three native plant species by
60–80%. Our results also showed the allelopathic effects of
S. canadensis on native plant seedlings were greater for plants
in the invaded range than in the native range. These results
implied that the three kinds of allelopathic chemicals may in
Figure 4: The germination rate of K. striata in soil (from Experiment
2) previously planted with S. canadensis obtained from either the USA
or China that was supplemented or not supplemented with activated
carbon (AC vs. No AC) in Experiment 2C. Circles represent popula-
tion mean values; values are mean values ± SE; * indicates a signifi-
cant difference between the effects of S. canadensis origin within each
activated carbon treatment at P < 0.05; for the soil that previously
contained plants from either the USA or China, mean values with
different uppercase or lowercase letters, respectively, are significantly
different at P < 0.05; ns indicates no significance.
Figure 5: Shoot biomass of mono-S. canadensis from the USA (Mono
1) and from China (Mono 2), mono-K. striata (Mono 3), and their
mixtures (Mix 1 and Mix 2) with or without activated carbon (AC or
No AC) in the Experiment 3. Diagonal lines indicate the shoot biomass
of K. striata. Circles represent population mean values of S. canadensis.
Within each of the five treatments, * or ** indicates a significant dif-
ference between AC and No AC at P < 0.05 or P < 0.01, respectively.
In comparisons between Mono 1 and Mono 2 and between Mix 1 and
Mix 2, different uppercase or lowercase letters indicate significant dif-
ferences between the indicated mean values.
at Zhejiang University on October 31, 2012
Page 8 of 11 Journal of Plant Ecology
part contributed to the observed allelopathy effects, although
we do not rule out the plausible role(s) of some other chemi-
cals. Our competition experiment further demonstrated that
S. canadensis from China possessed a higher competitive abil-
ity than those from the USA, and that allelopathy contrib-
uted 46.1% to this enhanced competitive ability. Research
results have been inconsistent about whether allelopathy
contributes to competitive ability. Rich (2004) found no evi-
dence that the invasive plant Acer platanoides used allelopathy
to interfere with the growth of native plants, and the inva-
sive plant Centaurea maculosa outperformed the native plant
Festuca idahoensis in North America even when activated car-
bon was added to the soil (Ridenour and Callaway 2001).
Inhibition of mycorrhizal fungi by Alliaria petiolata (garlic
mustard), however, was greater in the invaded range than
in the native range, and this resulted in greater inhibition in
the invaded range where the native plants are dependent on
the fungi (Callaway et al. 2008). In our study, the enhanced
competitive ability of S. canadensis in the invaded land may be
due to the enhanced allelochemical contents and allelopathic
The mechanism(s) that whether allelopathy contributes to
plant invasion remains unclear (Hubbell et al. 1983; Watling
et al. 2011; Mallik and Pellissier 2000; Bais et al. 2003; Callaway
and Ridenour 2004; Prati and Bossdorf 2004; Stinson et al.
2006; Jarchow et al. 2009). Some studies suggested allelopathy
could be a defensive strategy during plant invasion. Release
of allelochemicals by the invasive shrub Lonicera maackii, e.g.,
protects itself against attack by local amphibian larvae (Watling
et al. 2011). Because of excreted secondary compounds, leaves of
Hymenaea courbaril L. were not predated by the leaf-cutter ant Atta
cephalotes L. (Hubbell et al. 1983). Similarly, S. canadensis reduces
attack by the soilborne pathogens Pythium ultimum and Rhizoctonia
solani through the exudation of allelochemicals (Zhang et al.
2009). Other studies suggested that allelopathy promotes plant
invasion by increasing the competitive ability of invasive plants
(Murrell et al. 2011; Rashid and Reshi 2012). An alien invasive
species Anthemis cotula, e.g., can excrete allelochemicals to inhibit
seed germination and retarding seedling growth of its native
competitors Conyza canadensis and Galinsoga parviflora (Rashid and
Reshi 2012). In our current study, the in planta concentrations of
the three kinds of allelochemicals and their allelopathic effects on
seedlings of native plants were greater in the new location than
in the original location, and as before, the first common garden
experiment demonstrated that these differences probably had a
genetic basis. Moreover, the competitive ability of S. canadensis
in the new location was enhanced when compared with that
in the original location, and allelopathy contributed 46.1% to
the enhanced competitive ability. All these results implied that
the allelopathic processes employed by S. canadensis expanded
its population spread into the new range by enhancing the
competitive ability of the species.
Figure 6: Competitive effects of S. canadensis from either the USA
or China on K. striata with or without addition of activated carbon
(AC or No AC) as indicated by aggressivity indices in the Experiment
3. Circles represent population mean values. Values are means ± SE.
Within the AC treatment or within the No AC treatment, ** indicates
that the mean values differ at P < 0.01 and ns indicates no significant
difference. For treatments with S. canadensis from the USA, mean val-
ues with different uppercase letters are significantly different at the
5% level. For treatments with S. canadensis from China, mean values
with different lowercase letters are significantly different at the 5%
Figure 7: Allelopathic contributions to the competitive ability of
S. canadensis from the USA or China against the native K. striata in the
Experiment 3. Circles represent population mean values. Values are
means ± SE. Within each category of plant biomass (root, shoot, or
total), ** indicates a significant difference between S. canadensis from
either the USA or China at P < 0.01.
at Zhejiang University on October 31, 2012
Yuan et al. | Allelopathy and competitive ability in an invasive species Page 9 of 11
Allelopathic effects for the same species may somewhat dif-
fer between greenhouse and field experiments. For example,
the allelopathic effects of Malva sylvestris and Sisymbrium irio on
wheat and barley growth in greenhouse were different from
those experiments carried out in the field (Qasem 2010). These
differences may result from the greater complexity of plant
interactions under field conditions. So far, however, few stud-
ies have investigated allelopathic effects of exotic plants in both
the greenhouse and field (Hierro et al. 2005). In our holistic
study, we studied allelopathy using field surveys and common
garden experiments. Common garden experiments were con-
ducted to determine whether differences in growth may have
resulted from genetic factors. Overall, our results are consistent
with the hypothesis that the invasive plant S. canadensis showed
increased allelopathic potential, which increases its competitive
ability in China and allowing it to colonize many new areas.
Although we have no direct evidence that the increased allelo-
pathic potential and competitive ability of S. canadensis in the
invaded range results from recent genetic evolution for this
species in the invaded range (it is possible that the populations
in China represent highly competitive populations that were
introduced from the USA or elsewhere), we suspected that the
observed growth differences may be attributed, in part, result-
ing from rapid biological adaptations in the introduced range.
Our study paved the way for future research about the popu-
lation genetics of S. canadensis in both native and introduced
ranges. Increased understanding of the evolution of invasive
plants could help us predict, understand and better manage
these invasions (Sax et al. 2007).
This study was supported by Zhejiang Provincial Natural
Science Foundation of China (No. Z5090089) and the
Research Fund for the Doctoral Program of Higher Education
of China (RFDP, No. 20110101110077).
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