3.3. Reproduction effort
Culture, NTC, and CompType(Culture) had significant effects on the
number of capitula per invasive plant, and the interactions among
CompType(Culture) and PopType were also significant (Table 2). Compared
to that in the single-culture, G. quadriradiata when grown
together with competitors had significantly lower number of capitula per
plant. This effect was stronger when grown together with old
competitors. In general, central populations had significantly higher
number of capitula per plant than that of the edge population when grown
with new competitors (Figs S3, 4). However, when the invader was mixed
with the old competitor, there was no statistical difference between the
number of capitula per plant of central vs. edge populations. The
number of capitula per plant ofG. quadriradiata significantly increased with the nitrogen
addition. In the ambient nitrogen treatment, the central population
obtained lower number of capitula per plant when it was mixed with the
old competitors than that mixed with the new competitors (Fig. 4).
3.4.
Root mass ratio (RMR)
The result of the GLMM revealed that PopType, Culture, and
CompType(Culture) had significant effects on the RMR of G.
quadriradiata , and the interactions among CompType(Culture) and PopType
were also significant (Table 1). The RMR of the central population was
significantly lower than that of the edge population when grown alone
(Fig. 5). In general, the RMR of G. quadriradiata in the
mixed-culture was higher than that in the single-culture (Fig. 5, Table
1). The RMR of G. quadriradiata was significantly lower when the
invader was grown with old than with new competitors. For the central
population of G. quadriradiata , the RMR was higher when grown
with new competitors (Fig. 5). Both new and old competitors had similar
effect on the RMR on the edge populations.
3.5. Leaf nutrient
(nitrogen and phosphorus) concentration
The nitrogen addition treatments had a significant positive effect on
the leaf N content (LNC) of G. quadriradiata (Fig. 6a).
The interactions among CompType(Culture) and PopType on the LNC were
also significant (Table S2). The LNC of the central population was
significantly higher than that of the edge population when the invader
was grown with old competitors (Fig. 6b).
The GLMM revealed that Culture, NTC, and PopType had significant effects
on the leaf P content (LPC) of G. quadriradiata (Table
S2). In general, the invader LPC was higher in the single-culture than
in the mixed-culture; and it was significantly lower under nitrogen
addition treatments than when in ambient nitrogen treatment (Fig. 6c).
The LPC of the central population was higher than that of the edge
population which was further significantly reduced in the presence of
the competitors (Fig. 6d).
3.6.
Leaf construction costper unit of mass
( CCmass)
Competitor and population types (separately) had significant effects on
the leaf CCmass, and the interactions among PopType and
NTC were also significant (Table 2). The leaf CCmass was
significantly lower when G. quadriradiata was grown with old
competitors than when mixed with new competitors (Fig. 7). In general,
the leaf CCmass of the edge population was significantly
lower than that of the central population (Fig. 7), especially under
high nitrogen addition treatment (Fig. S4).
DISCUSSION
In this study, we aimed to reveal how population differentiation due
time since introduction and shared co-evolutionary history with
competitors could affect the invader’s response to increased nitrogen
deposition. The results of our experiment suggest that nitrogen addition
improves the growth and reproductive performance of the invader G.
quadriradiata , and enhances its relative competitive advantage on
competitors.
The
central population had both higher growth and reproductive performance
when compared to the edge population,
and the magnitude of response to
nitrogen addition treatments was larger in the central population when
in single-culture. In the presence of the competitors, the positive
effects of nitrogen addition on invasive plants was diminished. Old
competitors with longer shared co-evolutionary history had a stronger
competitive inhibition on G. quadriradiata performance than the
new competitors. These results suggest that the shared co-evolutionary
history between competitors and the invader plays an important role in
the plant invasion process.
Response to increased nitrogen deposition
The total mass and number of capitula per plant of G.
quadriradiata were higher under nitrogen addition treatment than in
ambient conditions (Figs 1-2). Our results then suggest that increased
nitrogen deposition improves the growth and reproduction performance ofG. quadriradiata , result which align with a number of other
invasive plants (Dawson et al., 2012; Parepa et al., 2019; Yu et al.,
2020). Invasive species generally tend to be fast-growing plants with
high nitrogen use-efficiency (Feng et al., 2009; Liu et al., 2017a).
Fast-growing plants often struggle to get enough nitrogen under natural
conditions (Bajpai & Inderjit, 2013; Liu et al., 2018). Therefore,
under increasing nitrogen deposition, the colonization and expansion ofG. quadriradiata may be further strengthened, especially in
farmlands with frequent artificial fertilization.
While nitrogen addition promoted
growth and reproductive performance of G. quadriradiata in
single-culture, in the presence of competitors this effect was weakened
(Figs 1-2). Moreover, the strength of interspecific competition ofG. quadriradiata increased with nitrogen addition (Fig. 3),
suggesting that competitors might also take advantage of the extra soil
nitrogen available and compete more intensively with co-occurring
invasive species. The competition with species might decrease the
positive effect of increased nitrogen deposition on G.
quadriradiata directly impacting its expansion rate.
Population differentiation
The growth and reproductive performance of the central population ofG. quadriradiata were higher than the edge population (Figs 2-4),
which may mainly be due to the stronger nutrient accumulation capacity
(especially in mixed culture) of the central population (Fig. 6). The
lower RCI values under ambient nitrogen treatment indicated that the
central population was also subjected to less competitive pressure when
planted with competitors (Fig. 3). These results suggest a significant
population differentiation between the central and edge population ofG. quadriradiata on growth and competitiveness. Many invasive
plants experience population differentiation in the process of range
expansion, which helps them to adapt to different environments
(Dematteis et al., 2020; Helsen et al., 2020). Generally speaking, the
central population of invasive plants may face higher competitive
pressure and for longer periods of time (Miller et al., 2020; Phillips
et al., 2010; Shine et al., 2011), and subsequently may evolve to be a
stronger competitor compared to the edge populations. Our results
indicate that, in our study area, the higher competitive ability of the
central population of G.
quadriradiata will potentially help it to better occupy the existing
habitats.
When planted alone, the total mass of the central population was
significantly higher than that of the edge population only in treatments
with nitrogen addition, with no significant differences under ambient
nitrogen (Fig. 2). This reveals that the magnitude of response of the
central population to elevated nitrogen was larger than that of the edge
population, suggesting that populations of invasive plant species with
longer time since introduction could have a larger advantage in the
context of future increased nitrogen deposition. Additionally, our
results indicate that the central population allocated more nitrogen to
growth under increased nitrogen deposition, especially when competing
with the old competitors (Fig. 6b). The literature shows that native and
invasive populations of invasive plant probably have different nitrogen
use strategies, with invasive populations generally showing a quicker
return in nitrogen use (Feng et al., 2011). What is still less explored,
and we show evidence here, is that different populations of invaders
respond uniquely to increases in nitrogen during the range expansion.
Therefore, future work should be careful to not overestimate the effects
of elevated nitrogen deposition in the range expansion of invasive
plants by sampling only the central populations or underestimate them by
studying only the edge population.
The effect of competitors with different shared
co-evolutionary history
Our results show that the extent of co-evolutionary history betweenG. quadriradiata and its competitors influenced the outcomes of
competition in our experimental setup. When G. quadriradiata was
planted with old competitors, its growth, competitive, and reproductive
performances were worse than when growing with the new competitors (Figs
2-4). These results contradict our proposed hypothesis and other studies
that have shown better performance of invaders over natives (Alexander
et al., 2015; Sun & He, 2018). This may be due to the overlooked
adaptations of other species over invasive species with a longer history
of co-evolution (Huang et al., 2018; Oduor, 2013; Strauss et al., 2006).
It has been suggested that intense competition from invasive plants is a
selective factor that eliminates native plant genotypes that cannot
tolerate such competition, leading to the accumulation of native plant
genotypes that can tolerate intense competition in native plant
populations (Leger & Espeland, 2010; Strauss et al., 2006). Genetic
variation in traits that are resistant to strong competition from
invasive plant species may enable native plants to evolve to adapt to
invasive plant species (Oduor, 2013; Strauss et al., 2006). For example,
a study on the African savannas suggests that Parthenium
hysterophorus invasions may have exerted selective pressure on native
plants, leading to the differentiation of growth and reproductive traits
between invasive and adjacent non-invasive habitats (Oduor, 2022). And
it has been found that native plants may evolve a tolerance reducing the
negative effects of invasive plants allelopathic compounds (Huang et
al., 2018). We speculate that a probable cause to this pattern in our
study is due to the lower photosynthetic capacity of G.
quadriradiata when mixed with the old competitors (Fig. S5).
With respect to the range expansion
of G. quadriradiata, the old competitors had a stronger
competitive inhibition on the central population when compared to the
new competitors (Fig. 2). This result was mainly attributed to the lower
root allocation of plants from the central population when planted with
old competitors than when planted with new competitors (Fig. 5). One
potential explanation is that due to intense aboveground competition
with the old competitor, invasive plants needed to allocate more biomass
aboveground instead of belowground (McCarthy & Enquist, 2007; Puglielli
et al., 2021). In contrast, the performance of invasive plants from edge
population ofG.
quadriradiata did not significantly differ when growing with new or old
competitors (Figs 2-4). The similar performance of the edge population
in the face of different competitors and different nitrogen conditions
may facilitate the edge population to better adapt to the uncertain
environmental factors they may face in the process of range expansion
(Alfaro & Marshall, 2019).
Our study explores the competitive relationship between an invasive
plant G. quadriradiata and eight competitors with different
co-evolutionary histories, which represents a large amount of work.
However, the conclusion about the influence of the co-evolution history
of invasive plants and competitors on their interaction still needs
careful extrapolation, because their interaction is also affected by
environmental conditions, plant rarity, functional traits and other
factors (Oduor, 2013; Zhang & van Kleunen, 2019). And this study only
inferred from the phenotypic traits that the co-evolutionary history of
competitors and G. quadriradiata influenced the relationship
between them. However, phenotypic trait expression is influenced by
heritable genetic and epigenetic factors (Oduor, 2022). Overall, future
studies need to be carried out on co-evolution history of other invasive
plants and competitors in more habitats, and multi-generation growth of
test plants can be used to test whether trait differences persist over
time, and the genetic mechanism should be further explored.
Synergisticeffect of nitrogen,
population differentiation, and co-evolutionary history
Many abiotic and biotic factors may affect the distribution and spread
of invasive plants in the context of disturbance and global climate
change (Liu et al., 2017b; Mitchell et al., 2006). These factors often
overlap in time and space, and may exert additive, synergistic, or
offsetting effects on invasive plants, resulting in complex and
unpredictable results (Darling & Cote, 2008; Kersting et al., 2015;
NeSmith et al., 2018). For example, in a field experiment in the
Californian grassland, the synergistic effect of water and fertilization
increased the growth performance of the invaders, which in the presence
of surrounding competitors greatly offset the effect (Eskelinen &
Harrison, 2014). In our study, we investigated the synergistic effects
of nitrogen addition, invasive plant population differentiation, and
co-evolutionary history of co-occuring plants on G.
quadriradiata . All three factors seem to play an important role in the
expansion of G. quadriradiata from central range to edge range in
China. Population differentiation contributed to the stronger invasion
potential of the center population, which was further enhanced by
increases in nitrogen deposition. However, the invasive species
dominance was diminished to some extent in the presence of old
competitors. Although the invasive potential of the edge population was
relatively low, it was enhanced under increases of nitrogen deposition.
Our results echo other studies showing that when studying invasive
plants, exploring the interaction of multiple influencing factors and
their cumulative effects is pressing (Darling & Cote, 2008; Kersting et
al., 2015).
CONCLUSION
In this study, we showed that the nitrogen addition significantly
promoted the growth and reproductive performance of G.
quadriradiata , while central populations had a larger magnitude of
response than the edge population when grown in single-culture. However,
in the presence of competitors, the response of G. quadriradiatato nitrogen addition was reduced. When grown in mixed settings with old
competitors that shared a longer co-evolutionary history, G.
quadriradiata both growth and reproductive performance were worse than
when growing with new competitors.
In general, the central population of G. quadriradiata had higher
population growth, reproductive performance and competitiveness than the
edge population. These results suggest that G. quadriradiata show
trait differentiation among populations in the process of range
expansion, which might benefit populations to adapt to different habitat
conditions and resident communities.
When considering both the stage of the range expansion and the
co-evolutionary history, old competitors more strongly inhibited the
central population performance via competition than the new competitors.
This effect, however, was not pronounced for the edge population. The
difference between the competition
strength of new and old competitors on the invasive G.
quadriradiata confirms that the role of co-evolutionary history between
competitors and invaders cannot be ignored when studying the range
expansion of invasive plants.