Journal of
Plant Ecology
Volume 7, Number 4,
Pages 396–402
august 2014
doi:10.1093/jpe/rtt050
Advance Access publication
1 October 2013
available online at
www.jpe.oxfordjournals.org
Soil space and nutrients
differentially promote the growth
and competitive advantages of two
invasive plants
Yan Gao1,2,†, Hong-Wei Yu1,2,† and Wei-Ming He1,*
1
State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, No. 20
Nanxincun, Haidian District, Beijing 100093, China
2
University of Chinese Academy of Sciences, No. 19 Yuquan Road, Shijingshan District, Beijing 100049, China
*Correspondence address. State Key Laboratory of Vegetation and Environmental Change, Institute of Botany,
Chinese Academy of Sciences, No. 20 Nanxincun, Haidian District, Beijing 100093, China. Tel: +86-10-82595899;
Fax: +86-10-82595899; E-mail: [email protected]
†
These authors contributed equally to this work.
Abstract
Aims
Invasive plants commonly occupy disturbed soils, thereby providing a stage for understanding the role of disturbance-enhanced
resources in plant invasions. Here, we addressed how soil space
and soil nutrients affect the growth and competitive effect of invasive plants and whether this effect varies with different invaders.
Methods
We conducted an experiment in which two invasive plants (Bromus
tectorum and Centaurea maculosa) and one native species (Poa
pratensis) were grown alone or together in four habitats consisting of
two levels of soil space and nutrients. At the end of the experiment,
we determined the total biomass, biomass allocation and relative
interaction intensity of B. tectorum, C. maculosa and P. pratensis.
Important Findings
Across two invaders, B. tectorum and C. maculosa, increased soil
nutrients had greater positive effects on their growth than increased
soil space, the effects of soil space on root weight ratio were greater
than those of soil nutrients, and their competitive effect decreased
with soil space but increased with soil nutrients. These findings suggest that changing soil space and nutrients differentially influence
the growth and competitive advantages of two invaders. Bromus
tectorum benefited more from increased soil resources than C. maculosa. Soil space and nutrients affected the biomass allocation of
C. maculosa but not B. tectorum. The competitive effect of B. tectorum was unaffected by soil space and soil nutrients, but the opposite
was the case for C. maculosa. Thus, the effects of soil space and
nutrients on growth and competitive ability depend on invasive species identity.
Keywords: biomass, Bromus tectorum, Centaurea maculosa,
competitive ability, Poa pratensis, soil nutrients, soil space
Received: 13 April 2013, Revised: 23 July 2013, Accepted:
6 August 2013
Introduction
Overall disturbance plays a key role in plant invasions through
changing resource availability (Hierro et al. 2006; Kuebbing
et al. 2013; Moles et al. 2012). For example, fine-scale disturbance can create gaps and thus releases space, light, water
and soil nutrients (Buckley et al. 2007; McConnaughay and
Bazzaz 1991; Kuebbing et al. 2013). This release is commonly beneficial for invasive plants, influencing their spatial
patterns (Chen et al. 2012; Davis et al. 2000; He et al. 2011;
Kuebbing et al. 2013; Walker et al. 2005). However, it is likely
that changing resource availability has no significant effects
on invasive plants in some cases (Cui and He 2009).
Resources essential for plants can be separated into consumable resources (e.g. light, nutrients and water) and inconsumable resources (e.g. physical space; Begon et al. 2006; Casper
and Jackson 1997). In nature resource fluctuation is commonly linked to disturbance (Buckley et al. 2007; Hierro et al.,
2006). This suggests that disturbance can alter the availability
of these two groups of resources at the same time. Although
previous researchers have addressed the effects of soil space
and soil nutrients on plants or plant communities (Casper
© The Author 2013. Published by Oxford University Press on behalf of the Institute of Botany, Chinese Academy of Sciences and the Botanical Society of China.
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Gao et al. | Soil space and nutrient release promote plant invasion397
and Jackson 1997; Gurevitch et al. 1990; McConnaughay
and Bazzaz 1991; O’Brien and Brown 2008), no studies have
explicitly answered this question in the context of plant
invasions.
There is a growing body of evidence for the consequences of
consumable resources for invasive plants (Chen et al. 2012; He
et al. 2011; Jamieson and Bowers 2012; Kuebbing et al. 2013).
In contrast, there is still a gap in terms of relationships between
physical space and invasive plants. More importantly, the benefits from released resources vary with resource types and species identity because soil space and soil nutrients confer different
consequences for plants via different mechanisms (Casper
and Jackson 1997; Gurevitch et al. 1990; McConnaughay and
Bazzaz 1991; O’Brien and Brown 2008), and different invasive
plants have different responses to resource release (Feng et al.
2009; James 2008; Mazzola et al. 2008).
In nature, invasive plants commonly appear in disturbed
soils (Moles et al. 2012). This situation sets up a stage for
understanding how disturbance-enhanced soil space and
nutrients influence the performance of invasive plants,
thereby providing new insights into the invasive success in
disturbed ranges. Bromus tectorum and Centaurea maculosa, two
common invasive plants in North America, are characterized
by growth or competitive advantages over native species (He
et al. 2009, 2011). Our observation suggests that both invaders
appear to be sensitive to changing soil space and nutrients.
Here, we focused on soil space because its consequences for
plant invasions are overlooked and on soil nutrients because
they are one of the most important soil resources limiting the
growth of plants in terrestrial ecosystems (Elser et al. 2007).
Our central hypothesis was that enhanced soil space and
nutrients differentially increase the growth and competitive
ability of invasive plants because enhanced resources tend to
promote plant invasion (Davis et al. 2000; Walker et al. 2005).
Additionally, we also hypothesized that there are differences in
response to changing soil space and nutrients between B. tectorum and C. maculosa because they are different in many inherent
traits (Roché and Roché 1988; Valliant et al. 2007). We tested
these hypotheses by growing plants of B. tectorum, C. maculosa
and Poa pratensis alone or together and through determining
their biomass, root weight ratio (RWR) and competitive effect.
Materials and Methods
Study species
We selected three plant species that are common in the USA.
Bromus tectorum L. (hereafter Bromus), an annual grass, is
native to Eurasia and northern Africa and was first detected
in the USA in about 1790 (Valliant et al. 2007). Centaurea maculosa L. (hereafter Centaurea), a perennial herb, is native to
Europe and was introduced into the USA in the 1890s (Roché
and Roché 1988). Bromus is a fast-growing invader whereas
Centaurea is a slow-growing invader. Poa pratensis L. (hereafter
Poa), a perennial grass, is among the common components in
semiarid or arid grasslands throughout North America. Poa
commonly appears in those grasslands invaded by Bromus or
Centaurea (personal observations). If Bromus and Centaurea
further expand, Poa is one of the most likely competitors
that both invaders encounter during their range expansion.
Thus, Poa is an ideal target competitor for understanding
interspecific relationships between it and these two invaders.
Callaway’s laboratory collected the seeds of Bromus, Centaurea
and Poa from Montana in the USA.
Experimental design
We used a mixture of 1:1 sand and vermiculite as a growth
medium because this mixture was neutral to all study species
and could minimize the likely effects of soil biota and other
soil features. We selected soil space and soil nutrients as fixed
factors. Accordingly, we used two sizes of pots (16 cm diameter
and 20 cm deep, and 8 cm diameter and 20 cm deep) and two
levels of solutions (1 and 4 g/l of a water-soluble fertilizer) to
create four types of artificial habitats: (i) high soil nutrients and
large soil space, (ii) high soil nutrients and small soil space, (iii)
low soil nutrients and large soil space and (iv) low soil nutrients
and small soil space. Note that large soil space was four times as
big as small soil space and high soil nutrients were four times as
rich as low soil nutrients. This design allowed us to disentangle
and contrast the relative importance of soil space and soil nutrients in plant invasion under the equal amounts of resource
changes (i.e. four times of space change versus four times of
nutrient change). We created low and high levels of soil nutrients with 50 ml of 1 and 4 g/l of a water-soluble fertilizer (20%
N, 20% P2O5, 20% K2O, g/g; Peters Professional, Scotts, USA)
every 3 weeks. In other words, two sizes of pots shared the
same total amounts of nutrients for a given nutrient condition.
We planted one individual from Bromus or Centaurea with
one individual from Poa (i.e. pariwise competition) together,
testing interspecific competition (i.e. one Bromus individual
and one Poa individual per pot or one Centaurea individual and
one Poa individual per pot). Additionally, we also planted individuals from Bromus, Centaurea and Poa alone as the controls.
All plants were from seed. There were 10 replicates for each
habitat–species combination. We placed all pots on benches
and rotated them every week to minimize position effects.
We used greenhouse rather than common garden experiments to avoid nutrient loss due to rainfall pulses. During the
experiment, all plants were watered as required to maintain
adequate water supply, and other growing conditions were
identical for all plants. The experiment ran for 4 months. At
the end of the experiment, all plants were harvested and then
separated into shoots and roots. All plant materials were ovendried at 75°C for 48 h and weighed. Finally, we determined the
total dry biomass of a plant (including shoots and roots).
Data analyses
We determined RWR (the ratio of root dry biomass to the
total dry biomass of a plant) to test whether biomass allocation differs among contrasting habitats. To quantify the competitive effects (i.e. the potential of a target plant to suppress
398
Journal of Plant Ecology
its neighbours, Weigelt and Jolliffe 2003) of a given species,
we calculated relative interaction intensity (RII): RII = (C − T)/
(C + T), where C is the total biomass of plants grown with a
neighbour and T is the biomass of plants grown alone (Armas
et al. 2004). RII has values ranging from −1 to 1, and is negative for competition and positive for facilitation (Armas et al.
2004). Specifically, for the RII values of Bromus and Centaurea,
we selected Poa as a competitive neighbour; for the RII values of Poa, we selected Bromus and Centaurea as competitive
neighbours.
Our experiment was a completely factorial design, involving species identity (Bromus, Centaurea and Poa), soil space
(large space versus small space) and soil nutrients (high nutrients versus low nutrients). Accordingly, we used three-way
analysis of variance (ANOVA) to test the effects of species
identity, soil space and soil nutrients on plant growth, biomass
allocation and RII. This analysis allowed us to determine the
importance of species identity and whether species responded
differently to experimental factors. Additionally, we further
focused on how soil space and soil nutrients influence the
performance of each species. For a given species, we used
two-way ANOVA to test the effects of soil space and soil nutrients on plant growth, biomass allocation and RII. The total
biomass was transformed to the square root to meet assumptions of ANOVA. Individual means were compared with a post
hoc Tukey test. All the statistical analyses were carried out
using SPSS 15.0 (SPSS Inc., Chicago).
Results
Across four habitats consisting of soil space and soil nutrients,
total biomass differed among three species: Bromus (4.43 ± 0.31
[1 SE] g) > Poa (3.45 ± 0.18 g) > Centaurea (2.22 ± 0.18 g;
Table 1). Total biomass increased with soil space and soil
nutrients, and also varied with interactions between species
and soil resources (Table 1). When each species was analysed
separately, soil space, soil nutrients and their interactions also
affected its growth (Table 2). The biomass of Bromus increased
Table 1: three-way analyses of variance of total biomass per plant, RWR and competitive effect as affected by species identity, soil space
and soil nutrients
Total biomass
F
RWR
P
F
Competitive effect
P
F
P
144.85
<0.001
5.95
0.003
90.98
<0.001
95.52
<0.001
15.33
<0.001
8.67
0.004
576.11
<0.001
54.44
<0.001
7.60
0.007
SI × SS
10.91
<0.001
12.55
<0.001
5.88
0.004
SI × SN
42.20
<0.001
12.07
<0.001
5.53
0.005
SS × SN
34.71
<0.001
21.15
<0.001
1.02
0.315
0.51
0.603
1.67
0.192
2.61
0.077
Species identity (SI)
Soil space (SS)
Soil nutrients (SN)
SI × SS × SN
Values of P < 0.05 are in bold.
Table 2: two-way analyses of variance of total biomass per plant, RWR and competitive effect of Bromus tectorum, Centaurea maculosa or Poa
pratensis as affected by soil space and soil nutrients
Total biomass
F
RWR
P
F
Competitive effect
P
F
P
Bromus tectorum
Soil space (SS)
Soil nutrients (SN)
SS × SN
<0.001
0.52
0.473
2.05
0.164
<0.001
2.80
0.098
2.01
0.168
9.76
0.003
2.38
0.127
5.99
0.022
11.15
0.002
22.17
<0.001
22.27
<0.001
56.00
294.3
Centaurea maculosa
SS
<0.001
5.73
0.021
4.30
0.046
12.96
0.001
9.13
0.004
2.99
0.093
SS
24.68
<0.001
SN
93.91
<0.001
SS × SN
12.61
0.001
SN
SS × SN
203.2
Poa pratensis
Values of P < 0.05 are in bold.
0.217
55.69
4.612
0.644
1.705
0.196
<0.001
0.781
0.380
0.038
0.159
0.692
Gao et al. | Soil space and nutrient release promote plant invasion399
by 44, 165 and 311% with soil space, soil nutrients and their
interaction, respectively (Fig. 1A). The biomass of Centaurea
increased by 20, 151 and 204% with soil space, soil nutrients
and their interaction, respectively (Fig. 1B). The biomass of
Poa increased by 43, 109 and 177% with soil space, soil nutrients and their interaction, respectively.
Across all four habitats, Bromus (0.464 ± 0.009) and Centaurea
(0.454 ± 0.003) shared similar RWR but had greater RWR than
Poa (0.423 ± 0.011; Table 1). RWR decreased with soil space
and nutrients, and also varied with interactions between species and soil resources (Table 1). When each species was considered separately, soil space and soil nutrients yielded different
effects on its RWR (Table 2). Soil space, soil nutrients and their
interaction had no effects on RWR of Bromus (Fig. 2A; Table 2).
The reverse was true for RWR of Centaurea (Fig. 2B; Table 2).
Increased space and nutrients allowed Centaurea plants to allocate less biomass to their roots, particularly in the presence of
the coincident increase in soil resources (Fig. 2B). The RWR of
Poa significantly varied with soil nutrients and their interaction with soil space, but not soil space alone (Table 2).
Across all four habitats, Bromus (−0.780 ± 0.029) had a much
stronger competitive effect than Centaurea (−0.189 ± 0.037)
12
and Poa (−0.220 ± 0.027), but the latter two shared a similar competitive effect (Table 1). Competitive effect decreased
with soil space but increased with soil nutrients, and also
varied with interactions of species with soil space and nutrients (Table 1). For an individual species, soil space and soil
nutrients had different consequences for its competitive
effect (Table 2). Neither soil space nor soil nutrients affected
the competitive effect of Bromus, whereas their interaction
affected its competitive effect (Fig. 3A; Table 2). Soil space
or soil nutrients alone dramatically affected the competitive
effect of Centaurea, whereas their interaction had no effect on
its competitive effect (Fig. 3B; Table 2). Specifically, increased
soil space decreased the competitive effect of Centaurea by
81%, and increased soil nutrients increased that by 54%
(Fig. 3B). The competitive effect of Poa was unaffected by soil
space, soil nutrients and their interaction (Table 2).
Discussion
Effects of soil space and nutrients on invasive plants
We found that soil space alone had significant effects on the
growth, biomass allocation and competitive ability of three
0.8
(A) Bromus
a
Small soil space
9
Large soil space
0.6
Small soil space
Large soil space
a
b
6
a
a
a
0.4
c
3
0
12
d
Root weight ratio (g g-1)
Total biomass per plant (g)
(A) Bromus
(B) Centaurea
9
0.2
0.0
0.8
(B) Centaurea
a
0.6
b
6
a
b
b
0.4
b
3
c
0.2
c
c
0.0
0
Low soil nutrients
High soil nutrients
Figure 1: total biomass per plant of Bromus tectorum (A) and Centaurea
maculosa (B) grown alone in four different habitats consisting of two levels of soil space and soil nutrients. Data are means + 1 SE (n = 10). The
bars with different letters represent significant difference at P = 0.05.
Low soil nutrients
High soil nutrients
Figure 2: root weight ratio of Bromus tectorum (A) and Centaurea maculosa (B) grown alone in four different habitats consisting of two levels
of soil space and soil nutrients. Data are means + 1 SE (n = 10). The
bars with different letters represent significant difference at P = 0.05.
400
Journal of Plant Ecology
Competitive effects (Relative interaction intensity)
0.0
−0.4
a
−0.8
ab
b
Small soil space
−1.2
0.0
ab
Large soil space
(A) Bromus
a
ab
−0.4
b
c
−0.8
−1.2
(B) Centaurea
Low soil nutrients
High soil nutrients
Figure 3: competitive effects, as indicated by relative interaction
intensity, of Bromus tectorum (A) and Centaurea maculosa (B) on Poa
pratensis in four different habitats consisting of two levels of soil space
and soil nutrients. Data are means + 1 SE (n = 10). The bars with different letters represent significant difference at P = 0.05.
plant species used in our experiment (Table 1). These findings support the viewpoint that soil space is a fundamental
resource for plants (Casper and Jackson 1997; McConnaughay
and Bazzaz 1991). More importantly, our results provide
experimental evidence for the ecological role of soil space in
the context of plant invasion.
Across Bromus and Centaurea, enlarged soil space allowed
them to grow larger. This beneficial effect can be ascribed to
diverse factors, such as increased resource acquisition and
translocation to shoots (Hameed et al. 1987; Tschaplinski and
Blake 1985), increased hormone production and translocation
(Carmi and Heuer 1981), changes in root architecture and
morphology (McConnaughay and Bazzaz 1991) and a combination of these factors. Overall, enlarged soil space reduced
RWR of invasive plants, indicating that space alone also is a
limiting factor (Casper and Jackson 1997; O’Brien and Brown
2008) and increased space allows them to capture resources
more easily (Bloom et al. 1985). When Bromus and Centaurea
were considered together, their competitive effect decreased
with increased soil space. This phenomenon has been found
in previous studies (Casper and Jackson 1997). If only space is
released in nature, then the competitive exclusion of invaders
against local residents appears to reduce with space release.
We also found that increased soil nutrients dramatically
enhanced the growth of invasive plants. This effect involves
multiple mechanisms. For example, nutrient release increases
the supply of unused resources for invaders and nitrate reductase activity is usually higher in invasive species (Kourtev
et al. 1999); invaders tend to be N-efficient, thereby achieving
relatively high carbon gain per unit of N (Feng et al. 2009).
Increased soil nutrients allowed invaders to allocate less
biomass to their roots but greatly increased their competitive ability. This phenomenon can be ascribed to allelopathic
effects of invasive plants (He et al. 2009) and the fast growth
of their shoots, thereby inhibiting other neighbours.
Our findings suggest that soil space and nutrients differentially influence the growth and competitive advantages of
invasive plants. First, under the same time of resource change,
the benefits from soil space, as indicated by growth, were much
smaller than those from soil nutrients, suggesting that soil
nutrients are more important for plant growth than soil space.
Second, the relative importance of soil space was greater than
that of soil nutrients in altering RWR because the changing
magnitude of RWR was greater when soil space was increased
by three times than when soil nutrients were increased by
three times. Finally, released soil space decreased the competitive ability of invasive plants, whereas released soil nutrients
increased their competitive ability (i.e. opposite effects of soil
space versus soil nutrients). These differences imply that soil
space and nutrients may influence the inherent traits of invasive plants through different mechanisms. However, we do not
know the related mechanisms underlying these differences.
When Bromus and Centaurea were considered together or
separately, soil space and soil nutrients exhibited interactive
effects on their growth, biomass allocation and competitive
ability. In other words, soil space and soil nutrient tend to
act in concert to influence plant traits. More interestingly, the
benefits from the coincident increase in space and nutrients
were greater than the sum of benefits from individual space
and nutrient release, implying that this coincident increase
exhibits non-additive effects.
In summary, this study disentangled resources released
by disturbance into consumable and inconsumable ones and
quantified their relative importance in plant invasion. Our
findings suggest that the ability of invaders to benefit from
increased soil resources depends on the nature of resources
and also provide new insights into the success of invasive
plants in disturbed ranges.
Responses of Bromus and Centaurea to soil space
and nutrients
Although Bromus and Centaurea are noxious weeds in North
America, they exhibited contrasting responses to changing
soil space and nutrients. In terms of increased biomass, Bromus
benefited more from the co-release of soil space and nutrients than Centaurea. Annual invaders tend to grow faster than
Gao et al. | Soil space and nutrient release promote plant invasion401
perennial invaders (MacKown et al. 2009), which is consistent
with our finding that the total biomass of Bromus was about
150% greater than that of Centaurea. The biomass allocation
of Bromus was insensitive to changing soil space and nutrients,
whereas the biomass allocation of Centaurea was sensitive to
changing soil space and nutrients. Bromus did not decrease
biomass allocation to its roots under larger soil space, which
enables it to have a greater potential to absorb soil water and
nutrients to meet the demand of fast growth (James 2008).
Neither soil space nor soil nutrients affected the competitive
effect of Bromus; however, the competitive effect of Centaurea
decreased with soil space but increased with soil nutrients. In
terms of increased competitive ability, Bromus benefited less
from soil nutrient release than Centaurea. Additionally, the
interactions between soil space and soil nutrients affected the
competitive effect of Bromus but not Centaurea. A recent study
suggests that Bromus is able to co-opt nutrients in the rooting zone of the natives, enabling it to maintain competitive
advantages (Blank 2010).
Three-way ANOVA showed that the growth, biomass allocation and competitive ability of Bromus and Centaurea strongly
depend on soil space and soil nutrients, but this dependence
also varied with invasive plants per se and their functional
traits. As early as in 1991, McConnaughay and Bazzaz pointed
out that species may differ in patterns of responses to space
and nutrients. However, this issue, to date, remains not to
be answered completely, thereby awaiting more effort in this
aspect.
Although Bromus is a fast-growing invasive plant and
Centaurea is a slow-growing invasive plant, we cannot extrapolate our findings to fast- versus slow-growing plant groups.
This is because only one species of each plant group was used
in our experiment and thus there is no replication at the level
of species. However, our findings provide an initial indication
that fast- and slow-growing invasive plants may exhibit different responses to changing consumable versus inconsumable resources.
Funding
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