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The evolution of increased competitive ability, innate
competitive advantages, and novel biochemical weapons act in
concert for a tropical invader
Rui-Min Qin1,2*, Yu-Long Zheng1,2*, Alfonso Valiente-Banuet3, Ragan M. Callaway4, Gregor F. Barclay5,
Carlos Silva Pereyra3 and Yu-Long Feng6
1
Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Kunming, 650223, China; 2Graduate University, Chinese Academy of
Sciences, Beijing, 100039, China; 3Instituto de Ecologıa, Departamento de Ecolog^oa de la Biodiversidad, Universidad Nacional Aut^onoma de Mexico, Apartado Postal 70-275, C.P. 04510,
Mexico D.F., Mexico; 4Division of Biological Sciences, University of Montana, Missoula, MT, 59812, USA; 5Department of Life Sciences, University of the West Indies, St. Augustine,
Trinidad and Tobago; 6College of Bioscience and Biotechnology, Shenyang Agricultural University, Shenyang, Liaoning Province, 110866, China
Summary
Author for correspondence:
Yu-Long Feng
Tel: +86 24 88487163
Email: [email protected]; [email protected]
Received: 13 September 2012
Accepted: 30 October 2012
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doi: 10.1111/nph.12071
Key words: Chromolaena odorata, common
garden, enemy defense, evolution, interspecific competition, nutrient, novel weapons
hypothesis, seed germination.
There are many non-mutually exclusive mechanisms for exotic invasions but few studies
have concurrently tested more than one hypothesis for the same species.
Here, we tested the evolution of increased competitive ability (EICA) hypothesis in two
common garden experiments in which Chromolaena odorata plants originating from native
and nonnative ranges were grown in competition with natives from each range, and the novel
weapons hypothesis in laboratory experiments with leachates from C. odorata.
Compared with conspecifics originating from the native range, C. odorata plants from the
nonnative range were stronger competitors at high nutrient concentrations in the nonnative
range in China and experienced far more herbivore damage in the native range in Mexico. In
both China and Mexico, C. odorata was more suppressed by species native to Mexico than by
species native to China. Species native to China were much more inhibited by leaf extracts
from C. odorata than species from Mexico, and this difference in allelopathic effects may provide a possible explanation for the biogeographic differences in competitive ability.
Our results indicate that EICA, innate competitive advantages, and novel biochemical
weapons may act in concert to promote invasion by C. odorata, and emphasize the importance of exploring multiple, non-mutually exclusive mechanisms for invasions.
Introduction
Successful biological invasions depend to a large degree on interactions between introduced organisms and species native to the
invaded systems. For example, invasive plants often outcompete
native plants (Garcia-Serrana et al., 2007; Mangla et al., 2011;
Callaway et al., 2012), and this stronger competitive ability has
been associated with higher resource capture and utilization efficiency (Feng et al., 2007), stronger allelopathic effects (Callaway
& Aschehoug, 2000; Ni et al., 2010), and release from consumer
pressure (Keane & Crawley, 2002). Furthermore, the intensity of
these interactions may be affected by their novelty in the invaded
system (Hierro et al., 2005; Lamarque et al., 2011), or evolve in
response to conditions in the nonnative range (Siemann &
Rogers, 2001; Ridenour et al., 2008; Lei et al., 2011). The ecological effects of inherent novelty versus evolution on invasions
are not likely to be mutually exclusive, but few studies have
*These authors contributed equally to this work.
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explored these ideas together or have studied multiple
mechanisms affecting exotic invasion in general (e.g. DeWalt
et al., 2004; Hierro et al., 2005; Williams et al., 2010).
Evolutionary responses to biota in the nonnative ranges of
invaders have often been explored in the context of the ‘evolution of increased competitive ability’ (EICA) hypothesis.
The EICA hypothesis posits that the release of exotic species
from consumer pressure in their nonnative ranges can lead to
decreased allocation to defense and a concomitant increase in
allocation to growth and by extension to increased competitive ability (Blossey and N€otzold, 1995). A number of experiments have supported one or both predictions of the EICA
hypothesis for some species (Siemann & Rogers, 2001;
Bossdorf et al., 2004; Maron et al., 2004; Wolfe et al., 2004;
Ridenour et al., 2008), but for other species no evidence was
found for EICA (Vila et al., 2003; Bossdorf et al., 2004).
Feng et al. (2009, 2011) reported a mechanism for the EICA
hypothesis. They found evolutionary shifts in nitrogen allocation from cell walls (defense) to photosynthesis (growth) in
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nonnative populations of an invasive species, resulting in
faster growth and poorer structural defenses.
Competitive advantages of invaders over natives have been
studied recently in the context of the novel weapons hypothesis
(NWH), the idea that constitutive and induced biochemicals that
are new to the nonnative ranges of the invader provide disproportionate allelopathic advantages against na€ıve native plant species
(Callaway & Aschehoug, 2000; Inderjit et al., 2011a), against
native soil biota through antibiotic effects (Callaway et al., 2008),
or against herbivores (Lankau et al., 2004; Schaffner et al., 2011).
For example, Callaway et al. (2012) found that the Eurasian
Acroptilon repens occurred in denser stands with far lower relative
abundances of natives in North America than in its native
Uzbekistan, and Ni et al. (2010) found that this invader also
exerted stronger competitive and allelopathic effects on North
American species than on species from Uzbekistan. Similar
results have been reported for the allelopathic effects of other
invasives, including Ageratina adenophora (Inderjit et al., 2011b),
Centaurea stoebe (Thorpe et al., 2009), Centaurea diffusa
(Callaway & Aschehoug, 2000), Foeniculum vulgare (Colvin &
Gliessman, 2011) and Prosopis juliflora (Kaur et al. 2012), for a
suite of invasive species in Korea (Kim & Lee, 2011), and in a
meta-analysis of invasive tree species (Lamarque et al., 2011).
Chromolaena odorata (L.) R. M. King and H. Robinson
(Compositae) is native to North, Central, and South America
but is a noxious invasive perennial herb or subshrub throughout
much of Asia, Oceania, and Africa. It was first introduced into
India as an ornamental plant in the middle of the 19th Century,
and now has become one of the most invasive species in southern
China. Chromolaena odorata often forms dense monocultures in
habitats such as croplands, plantations, pastures, disturbed forests, roadsides, and riverbanks, causing great economic loss and
threatening biodiversity (Zhang & Feng, 2007). More than 200
arthropod enemies have been found to attack C. odorata in its
native range, a quarter of which are specialists (Zhang & Feng,
2007), but very few generalist or specialist enemies occur in the
nonnative ranges of the invader. In this study, we tested the EICA
hypothesis and the NWH by comparing the performances of C.
odorata plants collected as seeds from different populations in the
native and nonnative ranges and then grown in common gardens
in Mexico and China. In this context, we compared interactions
between C. odorata and Eupatorium japonicum, Eupatorium
stoechadosmum, and Eupatorium heterophyllum, which are native
to China, and Eupatorium ligudtrinum, which is native to
Mexico. We chose Eupatorium species because the genus is very
closely related to the genus Chromolaena – C. odorata is synonymous with Eupatorium odoratum. Resource supply can affect the
outcomes of competition among natives and invaders (Besaw
et al., 2011) and increased soil fertility has been shown to facilitate invasion of alien species in general (Daehler, 2003) and
C. odorata specifically (Wang & Feng, 2005). Therefore we conducted the experiment in China at ambient and elevated soil
nutrient concentrations. Finally, to explore the NWH we conducted an experiment with leachates made from C. odorata leaves
and applied to seeds of eight species native to Mexico and seven
species native to China. We asked whether C. odorata plants from
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populations in the nonnative range differ in size, competitive
ability, and herbivore defense from plants from the native range;
and whether species from the nonnative range of C. odorata differ
in susceptibility to the effects of C. odorata leaf leachates from
species from the native range of C. odorata.
Materials and Methods
Study sites and materials
A common garden pot experiment and germination experiment
were conducted within the nonnative range of Chromolaena
odorata (L.) R. M. King and H. Robinson at the Xishuangbanna
Tropical Botanical Garden (21°560′ N, 101°150′ E; 570 m altitude) of the Chinese Academy of Sciences located in Mengla
County, Yunnan Province, southwest China. An outdoor common garden experiment was conducted within the native range
in Tlayacapan, Morelos, Mexico (18°57′ N, 98°58′ W; 1634 m
altitude). Chromolaena odorata grew wild around the Mexican
garden. In Xishuangbanna, the annual average temperature is
21.7°C; the mean temperature of the hottest month (July) is
25.3°C and that of the coolest month (January) is 15.6°C. The
annual average precipitation is 1557 mm with a dry period from
November to April. In Tlayacapan, the mean annual temperature
is 19.3°C; the mean temperature of the hottest month (June) is
22.9°C and that of the coolest month (January) is 16.9°C. The
mean annual precipitation is 988.8 mm with a dry period from
November to April (Garcıa, 1988).
For both common garden experiments, we collected seeds of
C. odorata from six populations in its native range (five from
Mexico and one from Trinidad; Supporting Information Table
S1) and six populations in its nonnative range (three from China,
two from Vietnam, and one from Laos) in 2009. We also
collected seeds from native Eupatorium lingustrinum DC in Mexico and from native Eupatorium japonicum Thunb., Eupatorium
stoechadosmum Hance, and Eupatorium heterophyllum DC. in
China. All of these species were sympatric, ecologically similar,
and phylogenetically related to C. odorata (syn. E. odoratum). For
each species, seeds were collected from more than 10 individuals
that were at least 20 m apart from one another. Seeds from individual plants were not mixed and thus seeds collected from each
individual comprised a ‘seed family’.
Common garden pot experiment in China
Seeds of the Chinese natives E. japonicum and E. stoechadosmum,
the Mexican native E. lingustrinum, three C. odorata populations
from the invasive range, and four C. odorata populations from
the native range (Table S1) were sown in seedling raising trays
(128 36-ml cells per tray) in a glasshouse in November 2009. We
originally chose five populations randomly from each regional
collection, but seeds from three of the ten populations did not
germinate. In February 2010, when the seedlings were c. 5 cm
tall, similar-sized vigorous seedlings were transplanted into
15-dm3 pots. Ten individuals from each C. odorata population
(two per seed family and five seed families per population) and
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10 individuals for each Eupatorium species were planted alone for
a total n of 100. We also transplanted 10 individuals of each of
the seven C. odorata populations into pots with each of the three
Eupatorium species, with plants 10 cm apart, for a total n of 210.
Pots contained a mixture of 70% forest topsoil and 30% river
sand. Topsoil was used to provide a natural supply of macro- and
micronutrients and the river sand provided a texture with adequate drainage and facilitated the harvesting of fine roots. All
seedlings were grown in shade with 50% irradiance for 4 wk to
facilitate initial survival and then were grown in full sun. Seedlings were divided into two groups; one was treated with compound fertilizer (nitrogen: phosphorus: potassium 15:15:15)
monthly from April to July at the rate of 1 g per pot (10 kg soil),
and the other group was the low-nutrient control. Five pots per
population of C. odorata (one from each seed family) or native
species for each nutrient and each competition (alone or with
neighbor) treatment were established. Pots were assigned to five
blocks in the common garden, and each block included 62 pots,
one pot for each population or species 9 nutrient 9 competition
treatment. The seedlings were watered daily with a drip irrigation
system. Pots were weeded when necessary and no pesticides were
used.
Plants did not flower and in August 2010 all plants (including
roots) were harvested, oven-dried at 60°C for 48 h, and weighed.
To evaluate competitive ability, the competitive ‘response’ of
each species was measured as the per cent change in performance
(biomass) of the species when grown with competition, that is,
((Pcomp – Psingle)/Psingle) 9 100, where Psingle is plant performance when grown without competition and Pcomp is plant performance when grown with interspecific competition. The
competitive ‘effect’ of each species was also measured as the per
cent change in the performance of its competitor. In this study,
Psingle was the average of all replicates per species or population
per treatment and Pcomp was the value of the individual replicate.
Common garden experiment in Mexico
Seeds of E. heterophyllum and E. stoechadosmum from China
and E. lingustrinum from Mexico and seeds from each of the
10 seed families of each of the five C. odorata populations
from each range (randomly selected; Table S1) were sown
into a seed bed located in a glasshouse in October 2009. In
January 2010, when the seedlings were c. 10 cm tall, similarsized vigorous seedlings were transplanted into an outdoor
garden. We grew 10 individuals of each C. odorata population (one from each seed family) and Eupatorium species
alone, and 10 individuals of each C. odorata population with
each of the three Eupatorium species (6 cm apart from each
other). All individuals and competing pairs were 60 cm from
any other plant or pair and were assigned to 10 blocks in the
common garden, 13 individuals (one from each of the 10
populations of C. odorata and the three Eupatorium species)
and 30 competing pairs (each C. odorata population with
each of the three Eupatorium species) per block. Individuals
and competing pairs were arranged randomly in each block.
Seedlings were watered every other day at the rate of 2000 ml
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per seedling or seedling pair in the dry season (January–May).
Plots were weeded and no pesticides were used.
In October 2010, five individuals (without competitors) per
population and one branch per individual (with~50 leaves) were
randomly selected for measurement of leaf herbivory. The number of damaged leaves and the total number of leaves were
counted for each individual, and the percentage of damaged
leaves was calculated as (the number of damaged leaves/the total
number of leaves) 9 100%. Total leaf area and the area damaged
by enemies were visually estimated by comparison with a paper
square of 10 cm by 10 cm dimensions (accurate to 0.1 cm) for
each leaf, and the percentage of leaf area loss was calculated for
each damaged leaf and each sample individual.
Plants did not flower, and in November 2010 the aboveground parts of all plants were harvested, oven-dried at 60°C for
48 h, and weighed. Competitive response and effect were calculated as described in the section of the Common garden pot
experiment in China.
Leachate experiment
We compared the effects of C. odorata leaf leachate on the germination and growth of species native to Mexico with the effects on
species native to China. Seeds were collected in 2010 from seven
native species from China (Carex baccans Nees, Eupatorium
japonicum, Eupatorium fortunei Turcz, E. stoechadosmum,
Polygonum molle D. Don, Vernonia cinerea (Linn.) Less, and
Vernonia volkameriifolia (Wall.) DC), and eight native species
from Mexico (Aldama dentata La Llave, Calea ternifolia Kunth,
Cosmos sulphureus Cav, Lagascea rigida (H. B. K.) Stuessy,
Lasianthaea helianthoides DC. var. helianthoides, Tagetes
tenuifolia Cav., E. ligustrinum, and Eupatorium sp.). All native
species from each range were sympatric with C. odorata. In January
2011, fully expanded leaves were collected from more than 10
C. odorata plants growing wild in the grounds of Xishuangbanna
Tropical Botanical Garden, dried in the shade at room temperature and powdered. Leaf powder was soaked in distilled water
(2.5 g of leaf powder per 100 ml of distilled water) at 4°C for
48 h, and filtered twice through double layers of gauze. The
filtrate, which represented a 2.5% leaf extract, was kept at 4°C
until used.
Seeds were soaked in 0.3% aqueous potassium permanganate solution for 15 min to sterilize them, washed twice with
distilled water, and placed on two layers of filter paper in
12-cm Petri dishes, 30 seeds per dish. Four ml of leaf extract
of C. odorata was added to each dish. Four concentrations of
leaf extract (2.5%, 1.25%, 0.25% and 0.0% (distilled water
as a control)) were used, with five replicates (Petri dishes) per
species per treatment. The number of germinated seeds
(emergence of the radicle) was recorded daily. Radicle length
was measured when no further germination of seeds occurred
for three consecutive days. The germination rate was calculated as (the number of germinated seeds/30 (total number of
seeds per Petri dish)) 9 100%. The germination rate or radicle length measured for the control was significantly different
between species. The relative values of these variables (per
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cent of control) were calculated for each species and
treatment to facilitate interspecific comparisons.
leaf extract concentration of C. odorata (Figs 6, S3) were determined using ANOVAs. All analyses were conducted using SPSS
13.0 (SPSS Inc. Chicago, IL, USA).
Statistical analyses
The effects of range, population nested within range, nutrient,
interaction of range and nutrient, and interaction of population
nested within range and nutrient on variables measured in the
common garden experiment in China were analyzed using threeway nested ANOVA, with all the factors as fixed factors (univariate
of general linear model; Table S2). The significance of
differences between plants from invasive and native populations
of C. odorata at each nutrient concentration in China and in
Mexico was determined using two-way nested ANOVAs, with
range and population nested within range as fixed factors (Figs 1,
3, 5). In this study, population nested within range was treated as
a fixed factor because of the low number of populations (Siemer
& Joormann, 2003). In Mexico, but not in China, Eupatorium
species native to Mexico suppressed C. odorata plants from both
ranges more than Eupatorium species native to China did
(Fig. S2). Thus, we also tested intraspecific differences (between
C. odorata plants from invasive and native populations) in the
competitive responses to the natives from China and Mexico separately. Neither the altitude nor the latitude at which seeds
of C. odorata were collected was used as a covariate, as neither of
them was significantly correlated with the performance of
C. odorata plants (P > 0.05). The significance of differences in
variables measured in both common garden experiments among
invasive and native populations of C. odorata, species native to
China, and species native to Mexico (Figs 2, 4), and the significance of differences in relative germination rate and relative radicle length between species native to China and Mexico at each
(a)
(c)
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Results
Common garden pot experiment in China
When grown without competition, C. odorata plants from the
native range were larger than plants from the nonnative range at
high nutrient supply (Fig. 1a). Total biomass decreased significantly with decreasing nutrient supply (Fig. 1a,b; Table S2), and
at low nutrient supply, total biomass did not differ between
plants from the two ranges (Fig. 1b). Competition from all
Eupatorium species decreased the total biomass of C. odorata
plants from both ranges at both nutrient concentrations. But,
importantly, at high nutrient supply C. odorata plants originating
from the nonnative range in China had superior competitive
responses to the Eupatorium species compared with C. odorata
plants from the native range in Mexico (Fig. 1c). In other words,
competition-driven decreases in total biomass were significantly
greater for C. odorata plants from the native range than for
C. odorata plants from the nonnative range. This did not occur at
low nutrient supply (Fig. 1d), which was consistent with the
significant interaction between range and nutrient supply
(Table S2).
At high nutrient supply, C. odorata plants from both the nonnative and native ranges were much less suppressed by the native
species from China than the native species from China were suppressed by C. odorata (Figs 2c, S1a). In other words, C. odorata
plants from both ranges had superior competitive responses and
stronger competitive effects than the native species from China
(b)
(d)
Fig. 1 Total biomass for Chromolaena
odorata plants from invasive (open bars) and
native (closed bars) populations grown
without competition at high (a) and low (b)
nutrient concentrations in the common
garden in China, and competitive response to
three Eupatorium species (two natives to
China and one native to Mexico; per cent
changes in total biomass) at high (c) and low
(d) nutrient concentrations. Narrow bars
indicate mean +SE (n = 5 for monoculture;
n = 15 for competition) for each population;
two thicker bars in the center depict mean
+SE for each range using the mean of each
population as replicates. Significant
differences between ranges according to
nested ANOVAs (Supporting Information
Table S3) at: *, P < 0.05; ***, P < 0.001.
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(a)
Fig. 2 Total biomass for plants grown
without competition (a, b), and change in
this variable caused by competition
(competitive response or effect) (c, d) for
invasive (open bars) and native (closed bars)
populations of Chromolaena odorata,
Eupatorium stoechadosmum (vertically
striped bars; native to China), Eupatorium
japonicum (hatched bars; native to China),
and Eupatorium ligustrinum (horizontally
striped bars; native to Mexico) grown at high
(a, c) and low (b, d) nutrient concentrations
in the common garden in China. For
C. odorata, change in total biomass was
caused only by natives to China. Means +SE
are shown (for monoculture, n = 5; for
competition, n = 30 for invasive populations
of C. odorata, n = 40 for native populations
of C. odorata, and n = 35 for natives).
Different letters indicate significant
differences among species at P < 0.05
according to ANOVAs (LSD test, Table S4).
(c)
when these species were interacting. In the low-nutrient treatment, the competitive advantage of the invader over the
Eupatorium species native to China decreased or even disappeared (Figs 2d, S1b). The two native Eupatorium species from
the invaded range in China were much more suppressed by
C. odorata than were the Eupatorium species from the native
range in Mexico in the high-nutrient treatment (Fig. 2c); that is,
the native species from Mexico had a superior competitive
response to C. odorata compared with natives from China. In the
low-nutrient treatment, however, the competitive effects of
C. odorata on E. stoechadosmum native to China and E.
ligustrinum native to Mexico were similar (Fig. 2d).
Common garden experiment in Mexico
Without competitors, C. odorata plants derived from populations
in the native range did not differ in aboveground mass from
plants from the nonnative ranges (Fig. 3a). Furthermore, the
competitive responses of C. odorata to Eupatorium species did
not differ between C. odorata plants from invasive and native
populations, whether tested using the responses to all natives
together (Fig. 3b) or to natives from different countries separately
(Fig. S2).
Generally consistent with the results from the pot experiment
in China (Fig. 2), C. odorata plants from both ranges were much
less suppressed by the Eupatorium species native to China than
these were suppressed by C. odorata (Figs 4, S1c). In other words,
C. odorata plants from both ranges had superior competitive
responses and stronger competitive effects compared with the
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(b)
(d)
native species from China. Most importantly, the native species
from Mexico had a superior competitive response to C. odorata
and a stronger competitive effect on C. odorata compared with
the natives from China. The two native Eupatorium species from
China were much more suppressed by C. odorata than the
Eupatorium species from Mexico (Fig. 4), and C. odorata was
much more suppressed by the native Eupatorium species from
Mexico than by the two Eupatorium species native to China (Fig. S2).
Herbivores attacked C. odorata plants from populations from
the nonnative ranges in Southeast Asia more, and did more damage to them, than plants derived from the native range. The number of damaged leaves was 107.9% higher for plants from
Southeast Asian populations of C. odorata than for plants from
native populations, and plants from the nonnative ranges experienced 174.9% more leaf area loss than plants from the native
range (Fig. 5).
Leachate experiment
Leaf extracts from C. odorata suppressed the mean relative germination rates (as percentages of the rates for the controls) of species
native to China far more than those of species native to Mexico
(also the native range of C. odorata) at all concentrations tested
(Figs 6a, S3). For comparison, inhibition proportions were
65.4% and 44.9% higher for species native to China than those
for species native to Mexico at 1.25% and 2.5% concentrations,
respectively. At the 0.25% leachate concentration, leaf extracts
from C. odorata inhibited germination by 59% for species native
to China but had no effect on species native to Mexico. The 0.25,
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(a)
(a)
(b)
(b)
Fig. 3 Aboveground mass (a) for Chromolaena odorata plants from
invasive (open bars) and native (closed bars) populations grown without
competition in the common garden in Mexico, and competitive response to
three Eupatorium species, two native to China and one native to Mexico
(per cent change in aboveground mass) (b). Narrow bars indicate mean
+SE (n = 10 without competition; n = 20 with competition) for each
population; two thicker bars in the center depict mean +SE for each range
using the mean of each population as replicates. The differences between
ranges were not significant according to nested ANOVAs (Table S5).
1.25, and 2.5% leaf extracts significantly inhibited seed germination for one (12.5% of the eight species), four (50.0%), and
seven (87.5%) of the eight species from Mexico, respectively; but
for four (57.1% of the seven species), seven (100%), and seven
(100%) of the seven species from China (Fig. S3). The lowest leaf
extract concentration (0.25%) significantly promoted seed germination (relative germination rate > 100%) for two species from
Mexico but no species from China.
Similarly, the leaf extracts from C. odorata also inhibited
seedling growth of the species native to China far more than that
of species native to Mexico (Figs 6b, S3). The mean values of relative radicle length of the species native to Mexico were much
higher than those of the species native to China at 0.25% (62.3%
vs 12.7% of the control, respectively) and 1.25% (25.2% vs 1.4%
of the control) concentrations. At the highest extract concentration (2.5%), the relative radicle length of three species native to
Mexico ranged from 22 to 43% of the control, whereas no
species native to China showed measurable growth (Fig. S3).
Discussion
Our results link apparent rapid evolutionary changes in competitive ability and herbivore defense occurring in the nonnative
range to inherently disproportionate competitive and allelopathic
advantages of the invader over native species. The latter may
derive from long-term evolutionary relationships among
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Fig. 4 Aboveground mass (a) for plants grown without competition in the
common garden in Mexico, and change in this variable caused by
competition (competitive response or effect) (b) for invasive (open bars)
and native (closed bars) populations of Chromolaena odorata, Eupatorium
stoechadosmum (vertically striped bars; native to China), Eupatorium
heterophyllum (diagonally striped bars; native to China), and Eupatorium
ligustrinum (horizontally striped bars; native to Mexico). For C. odorata,
change in aboveground mass were caused by natives only from China.
Means +SE are shown (for monoculture, n = 10; for competition, n = 100
for native species from Mexico, and n = 50 for others). Different letters
indicate significant differences among plants at P 0.05 according to
ANOVAs (LSD test; Table S6).
members of a community. Thus, we found evidence for both
EICA and the NWH. Chromolaena odorata had stronger competitive effects on Eupatorium species from China (the invaded
range) than on Eupatorium species from Mexico (the native range
of C. odorata) in two different experiments. These competitive
effects did not correspond with the biomass produced by the
competing species in China, and the germination and growth of
species native to China were far more inhibited by extracts from
C. odorata leaves than those of species native to Mexico. This is
consistent with a growing body of evidence for benefits that some
invasive species gain from the production of biochemicals to
which species native to the nonnative ranges of invaders are not
adapted, perhaps because they lack a common evolutionary
history (Callaway & Aschehoug, 2000; Ni et al., 2010; Colvin &
Gliessman, 2011; Inderjit et al., 2011b; Kim & Lee, 2011;
Lamarque et al., 2011; Kaur et al., 2012). These biogeographic
differences in allelopathic effects also provide one possible explanation, and potential integration of the effects of EICA and the
NWH, for the stronger competitive effects of C. odorata on species from China than on species from Mexico. Allelochemicals
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(a)
(b)
Fig. 5 Differences in damaged leaves per plant (a) and damaged leaf area
per plant (b) between Chromolaena odorata plants from invasive (open
bars) and native (closed bars) populations grown without competition in
the common garden in Mexico. Narrow bars indicate mean +SE (n = 5) for
each population; two thicker bars in the center depict mean +SE for each
range using the mean of each population as replicates. Significant
differences between ranges according to nested ANOVAs (Table S6):
***, P < 0.001.
(a)
(b)
Fig. 6 Relative (per cent of control) germination rate (a) and relative
radicle length (b) for native species from China (n = 7; open circles) and
Mexico (n = 8; closed circles). Means SE are shown for each range using
the mean of each species as replicate; n = 5 for each species. The
differences in the two variables between species native to China and
Mexico were significant for all treatments (P 0.001) according to
ANOVAs (Fig. S3).
Ó 2012 The Authors
New Phytologist Ó 2012 New Phytologist Trust
Research 985
released from C. odorata plants and residues have been shown to
accumulate in soils and inhibit plant growth in the field in nonnative ranges (Onwugbuta-Enyi, 2001; Singh & Angiras, 2008);
however, to our knowledge specific chemicals have not been identified and nor have the biogeographic patterns evident in our
Petri dishes been explored under field conditions where allelopathic effects may be attenuated.
At the high nutrient concentration in China, C. odorata plants
from invasive ranges demonstrated superior competitive
responses compared with C. odorata plants from native ranges.
This corresponded with other evidence that C. odorata plants
from China were more poorly defended than plants from
Mexico, and both are consistent with the hypothesis that the
stronger competitive ability of some invasive species may derive
from evolving to decrease allocation to costly structural and
chemical defenses (Blossey & N€otzold, 1995; Feng et al., 2009).
However, these competitive advantages were not associated with
greater biomass or growth rates as originally proposed. When
grown without competition, C. odorata plants from nonnativerange populations were actually 14.2% smaller than plants from
native-range populations. It was only in the presence of competitors that plants from the nonnative range demonstrated a superior response compared with conspecifics from the native range,
with Eupatorium competitors eliciting a 15.1% decline in total
mass for the nonnative-range C. odorata vs 34.9% for nativerange C. odorata. The increased interspecific competitive ability
of C. odorata plants from nonnative ranges may be associated
with directional selection for genotypes that produce higher
amounts of allelochemicals, such as indicated for the invasive
Centaurea maculosa (Ridenour et al., 2008).
Our results are consistent with other research reporting superior competitive ability for invasive populations of exotic species
relative to co-occurring natives (Vila & Weiner, 2004; Werner
et al., 2010). Our results are also consistent with evidence that
the evolution of increased competitive ability after introduction
contributes to the competitive advantage of C. odorata and other
invasive species (Ridenour et al., 2008; Barney et al., 2009).
However, to our knowledge no previous studies have explored
the importance of the evolution of increased competitive ability
and innate competitive advantages in a parallel study. Our results
indicate that innate competitive advantages contribute greatly to
the higher competitive ability for invasive populations of
C. odorata compared with natives from China (Figs 2, 4, S1).
Because we used common garden experiments, differences
among populations and ranges were not confounded by plasticity
(Reznick & Ghalambor, 2001) but we did not exclude founder
effects or maternal effects, as for most studies of the evolution of
invasives. Performing experiments in more than one environment
in each range increases the potential to detect evolutionary differences between native and nonnative populations of invasive species but this does not eliminate possible misinterpretation as a
result of founder effects. Few other biogeographic studies have
been conducted in more than one garden per range, and very few
have compared responses in invasive and native ranges (but see
Maron et al., 2007; Widmer et al., 2007; Williams et al., 2008).
By establishing comparative biogeographic experiments in both
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986 Research
ranges, our design incorporated the likelihood that population- or
regional source-based differences in competitive ability may vary
when measured in different abiotic conditions, as demonstrated
by the present study (Table S2) and Maron et al. (2004). The
overall differences in competitive ability and defense between
C. odorata plants from native and nonnative populations indicate
biogeographical differentiation, but to establish whether this differentiation is attributable to evolution after introduction, we
must compare invasive populations with their specific source populations (e.g. Dlugosch & Parker, 2008), and source populations
are rarely known with certainty. Based on internal transcribed
spacer (ITS) sequences, Scott et al. (1998) and von Senger (2002)
found significant genetic differentiation between invasive and
native populations of C. odorata, and concluded that C. odorata
populations in Asia, West Africa, and Australia originally originated from Trinidad. Evidence that C. odorata which invaded
Asia may also originate from Trinidad was also obtained by
X-Q. Yu et al. (unpublished) using nuclear (ITS) and chloroplast
(intergenetic spacers between QB protein gene and photosystem
II protein D1 gene (psbA-trnH) and between beta subunit gene of
ATP synthase and large subunit gene of ribulose-1,5-bisphosphate
carboxylase/oxygenase (atpB-rbcL)) DNA sequences. Here we
found that C. odorata plants from the likely source population
(Trinidad; the third of the four native populations from left to
right in Fig. 1c) showed an inferior competitive response compared with C. odorata plants from the invasive populations, which
further supports the likelihood that C. odorata in Asia has undergone evolutionary changes consistent with the EICA hypothesis.
In contrast to the results in the high nutrient supply treatment
in the pot experiment in China, we did not find greater competitive ability of C. odorata from nonnative populations at low
nutrient supply in China or in the common garden in Mexico. In
part, these results are consistent with the advantages invaders
often appear to gain with increasing resource availability (Daehler, 2003; Mangla et al., 2011; but see Garcia-Serrana et al.,
2007). However, the absence of regional differences in Mexico
may have occurred for several reasons, including unmeasured differences in abiotic and biotic environments between ranges (Maron et al., 2004). Furthermore, any possible novel biochemicals
produced by the invader may not have been as important in the
Mexican experiment which was conducted in the field, and thus
in the context of soil biota and herbivores.
To evaluate competitive effects and responses, we used three
Eupatorium species native to China and one Eupatorium native to
Mexico in the experiments. These choices were intended to provide a reasonable set of phylogenetically controlled competitors
but not to explicitly compare the effects and responses of Chinese
and Mexican sources of Eupatorium to C. odorata from different
regions. However, the results from these comparisons were consistent with the results from the experiment with leaf extracts,
and we found that the Eupatorium species from Mexico was a far
better competitor than the native Chinese Eupatorium species.
For example, competition from C. odorata plants caused 39.9%
and 64.5% lower decreases in aboveground mass for the
Eupatorium species from Mexico than for the Eupatorium species
from China when evaluated in China (R. Qin, unpublished data)
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and Mexico (Fig. 4), respectively. In addition, the Mexican
Eupatorium also had a much greater competitive effect on
C. odorata plants from both ranges than the Chinese Eupatorium
species when evaluated in Mexico (Fig. S2). To our knowledge,
only one other study has examined the EICA hypothesis using
phylogenetically controlled competitors from the native and nonnative ranges. McKenney et al. (2007) compared the growth of
different genotypes of Lepidium draba from its native European
and introduced western USA ranges in competition with the
North American Festuca idahoensis and the European Festuca
ovina. Contrary to our results, they found no differences in the
performances of L. draba from the different ranges under any
conditions, but corresponding to our results, F. ovina suppressed
the growth of L. draba much more than that of F. idahoensis.
In conclusion, C. odorata plants from the native range demonstrated superior competitive ability against species native to the
range it invaded, showing innate competitive advantages. Also,
native species from the invasive range in China were more vulnerable to allelochemicals presumably present in the leachate made
from C. odorata than natives from the native range in Mexico,
which is consistent with the NWH. Plants from invasive populations of C. odorata demonstrated a superior competitive ability
and inferior defensive ability against natural enemies compared
with plants from native populations, which is consistent with the
EICA hypothesis. In Mexico, however, and in the low-nutrient
treatment in China, plants from the invasive range in Asia did
not demonstrate superior competitive ability indicating
substantial biotic and abiotic conditionality for our results and
suggesting that different environments should be considered
when testing mechanisms underlying biological invasions. Our
results emphasize empirically that the different mechanisms that
drive invasions are not mutually exclusive.
Acknowledgements
This study was funded by projects of the National Natural
Science Foundation of China (30830027; 31270582) and
Knowledge Innovation Program of Chinese Academy of Sciences
(KSCX2-YW-Z-1019).
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Supporting Information
Additional supporting information may be found in the online
version of this article.
Fig. S1 Differences in competitive response or effect between
Chromolaena odorata plants originating from native range and
natives from China grown in both China and Mexico.
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Fig. S2 Differences in competitive response to Eupatorium species from China and Mexico between Chromolaena odorata plants
from invasive and native populations grown in Mexico.
Fig. S3 Differences in relative germination rate and relative radicle length between native species from China and Mexico when
treated with leaf leachate of Chromolaena odorata.
Table S1 Background information on sample populations of
Chromolaena odorata and native species from China and Mexico
used in two competition experiments
Table S2 Results from three-way nested ANOVAs presenting the
effects of range, population nested within range, and nutrient
concentration on variables of Chromolaena odorata grown in the
common garden in China
Table S4 Results from one-way ANOVAs presenting the differences among Chromolaena odorata from both ranges and native
Eupatorium species from China and Mexico grown at each nutrient concentration in China
Table S5 Results from two-way nested ANOVAs presenting the
differences between Chromolaena odorata plants from invasive
and native populations grown in Mexico
Table S6 Results from one-way ANOVAs presenting the differences among Chromolaena odorata from both ranges and native
Eupatorium species from China and Mexico grown in Mexico
Please note: Wiley-Blackwell are not responsible for the content
or functionality of any supporting information supplied by the
authors. Any queries (other than missing material) should be
directed to the New Phytologist Central Office.
Table S3 Results from two-way nested ANOVAs presenting the
differences between Chromolaena odorata plants from invasive
and native populations grown at each nutrient concentration in
China
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