Soil nutrient limitation and natural enemies promote the establishment of alien species in native community

doi:10.21203/rs.3.rs-3035537/v1

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Soil nutrient limitation and natural enemies promote the establishment of alien species in native community

https://doi.org/10.21203/rs.3.rs-3035537/v1

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Background and Aims

The invasion of alien plant species poses a threat to native community’s composition and diversity. However, the invasiveness of alien plants and invasibility of native communities should be depended on the interactions between biotic and abiotic factors, such as natural enemies and soil nutrient availability.

Methods

We simulated the invasion of nine invasive plants into native plant communities with two levels of soil nutrient availability and natural enemies suppression. We explored how the biotic and abiotic factors affect the response of alien target species and the resistance of native communities to invasion.

Results

Enemy release (i.e., presence of enemy) increased biomass proportion of alien plants and decreased that of native community under without nutrient addition. Furthermore, the negative effect of enemy suppression on the evenness of native community and the root-to-shoot ratio of alien target species was greatest under nutrient addition.

Conclusion

Soil nutrient deficiency and natural enemies might promote the invasive success of alien species in native community, whereas nutrient addition and enemy suppression can better enhance the resistance of native plant communities to invasion.

plant invasion

natural enemies suppression

nutrient addition

nutrient deficiency

select effect

Alien species continue to rise worldwide, potentially causing far-reaching negative impacts on the economy (Bradshaw and Connolly 2016; Paini et al. 2016), ecosystem functions and services (Kumschick et al. 2015; Vilà et al. 2011), and composition and biodiversity of native communities (Bellard et al. 2016; Pyšek et al. 2020), due to trade and transportation and human activities under the globalization (Hulme 2009; Meyerson and Mooney 2007; Sax and Gaines 2008; Turbelin et al. 2017). The invasion success of alien target species might have depended on environmental conditions in invaded range, such as abiotic factors (Bradley et al. 2010; Bradley et al. 2015; Cavaleri and Sack 2010; Dostál et al. 2013; Liu et al. 2017; Sorte et al. 2013; Wang et al. 2016a; Wang et al. 2019; Wang et al. 2016b; Wang et al. 2017) and biotic factors (Huang et al. 2020; Jin et al. 2022; Korell et al. 2019; Li et al. 2022b; Shan et al. 2022; Zhao et al. 2020). Among them, it is acknowledged that availability of environmental resources and the release of enemies are what most significantly contribute to the invasion of alien target species (Davis et al. 2000; Enders et al. 2020; Keane and Crawley 2002). Resource fluctuation hypothesis suggests that when the availability of resources in the environment increases, the habitat of native communities becomes more susceptible to invasion (Davis et al. 2000). This is because invasive species may have higher plasticity than native community (Hiatt and Flory 2020; Luo et al. 2022; Martinez and Fridley 2018; Parker et al. 2003), respond to resource fluctuations more quickly (Liu et al. 2018; Liu et al. 2017), and better utilize surplus resources for their own growth to promote invasion (Garcia and Eubanks 2019; Getman-Pickering et al. 2021; Hawkes and Sullivan 2001; Zhong et al. 2021). In fact, a recent meta-analysis has shown that exotic plants are more capable of utilizing added nitrogen than native plants (Liu et al. 2017). However, there are also studies that do not support this hypothesis, namely that increased nutrient availability suppresses the invasion of exotic plants (Li et al. 2022b; Zhang et al. 2021b). Therefore, more research is needed to test the impact of resource availability and uncover the causes of the many ways that invasive plants react to resource changes, which can have an impact on outcomes.

Despite being a foundational principle in invasion ecology, the resource fluctuation hypothesis has only been tested in study systems with the same trophic level. However, plant growth can be strongly regulated by other trophic levels, such as herbivores and fungal pathogens (Agrawal et al. 2005; Beckmann et al. 2016; Heard and Sax 2013; Maron and Vila 2001). According to the enemy release hypothesis (Keane and Crawley 2002; Liu and Stiling 2006; Mitchell and Power 2003), invasive species are attacked less by specialist enemies within their invaded range, which allows them to allocate more resources to growth (Carrillo and Siemann 2016; Hierro et al. 2022; Rotter and Holeski 2018). In addition, increased availability of environmental resources may improve the quality of plant leaf tissue (Cornelis and Delvaux 2016; van der Waal et al. 2011) and increase plant palatability, which may attract more enemies to feed (Endara and Coley 2011; van Langevelde et al. 2008). Overfeeding by enemies on plants may induce compensatory growth in plants (Garcia and Eubanks 2019; Getman-Pickering et al. 2021; Hawkes and Sullivan 2001; Ramula et al. 2019). Based on the above, we speculate that at the community level, the coexistence of high resources and natural enemies may jointly promote or inhibit invasion.

Previous studies have mostly focused on testing the resource fluctuation hypothesis and the enemy release hypothesis for one or a few invasive plant species, many of which have created growth environments where the invasive species can survive alone or compete with a single native species (Liang et al. 2020; Wang et al. 2019; Zhang et al. 2022a; Zhang et al. 2022b; Zhao et al. 2023), which is not representative of the actual environment in which the invasive species invade. In fact, at the community level, invasive plants face a diverse array of native plants, which can trigger selection effects on the native community (Adomako et al. 2019; Emery and Gross 2007; Li et al. 2022a; Sun and Roderick 2019), enhance their competitive advantage, and occupy environmental resources, thereby suppressing the invasion of exotic plant species. Support for this hypothesis comes from comparisons of traits and resource allocation between invasive and native communities (Dawson et al. 2012; Wang et al. 2022b; Wilsey and Polley 2002). For example, an increase in community evenness can inhibit the invasion of exotic plants (Tracy and Sanderson 2004; but Wang et al. 2022b), and a low root-to-shoot ratio can promote the utilization of resources by exotic plants, enhancing their invasiveness (Ni et al. 2018). However, little is known about how different nutrient levels affect native communities' ability to resist invasion by herbivores.

To test the effects of nutrient availability and herbivores on the invasion of alien plant species in resident communities, we conducted a multi-species experiment with four combinations of two nutrient availabilities (low vs. high) and two natural enemies suppression treatments (with vs. without natural enemies suppression). We established a stable native community and transplanted each of nine alien invasive plant species as target species. We aimed to answer the following questions: (i) which levels of nutrient and natural enemies can promote the invasive success of alien species in native community? (ii) on the contrary, how nutrient availability and natural enemies can enhance the resistance of native plant communities to invasion?

Species selection

The species were selected in the wetlands and grasslands in Nanshuihu National Wetland Park (N24^o47’16’’, E113^o120’23’’), Guangdong Province, China, based on a field investigation of the dominant alien invasive and native species in 2016. We chose nine alien clonal plant species (i.e., Hydrocotyle verticillata, Alternanthera philoxeroides, Sphagneticola trilobata, Erigeron annuus, Trifolium repens, Eleusine indica, Paspalum dilatatum, Ambrosia artemisiifolia, Amaranthus retroflexus) as the target species, which were dominant in the investigated habitats and co-occurred in subtropical and tropical wetlands or grassland habitats in China (Ma 2014; 2020; Ma and Li 2018). We chose six plant species commonly found and dominant in the wetlands and grasslands that were investigated to construct native communities (Appendix S1: Table S1). To balance the functional diversity in communities, the six native species belonged to the different functional groups (Araliaceae, Amaranthaceae, Compositae, Lamiaceae, Oxalidaceae, Rosaceae). All the selected 15 herbaceous species co-occur in the field (Table S1).

The species used in the experiment had been collected from field sites in Guangdong Province in China. We collected ramets for alien clonal species and seeds for others alien species and all native species (Table S1). The collected ramets were cultivated in a greenhouse at Huazhong Agricultural University (Wuhan, China) to produce enough new clonal fragments for the experiment. The seeds were germinated in potting soil in the greenhouse to produce enough seedlings. Because the time required for germination were known to differ among the species, we sowed them on different dates to ensure that all species were in similar developmental stages at the start of the experiment. We placed all trays with seeds in a greenhouse under natural light conditions, with a temperature between 20 and 28°C. Each ramet and seedling had three leaves and some roots.

Experimental set-up

The experiments were carried out in a greenhouse of Huazhong Agricultural University, Wuhan, China. The greenhouse was open on the sides to allow entrance of insect herbivores and pollinators. However, a fence prevented access to larger animals (e.g., birds and mammals). For each of nine target species, we transplanted one ramet or seedling of an alien target species in the center of each pot (24 cm long × 24 cm wide × 18 cm high). The six native plant species constitute native community planted uniformly surround the alien target species with a hexagonal design. We planted selected 288 square pots filled with a 1:1 mixture of sand (0-0.5 mm) and yellow-brown soil collected from Shizishan Mountain in Wuhan, Hubei Province, China.

The nutrient content of the mixed soil was also determined in this experiment. As the nutrient addition treatment in this experiment was divided into low and high nutrient additions, we needed to ensure that the nutrient content in the pots without nutrient addition treatment was at a lower level. The main method of nutrient addition in this experiment was to use slow-release fertilizer, which mainly contains N, P, and K elements. Based on this, the total N, total P, and total K of the mixed soil were mainly measured. The total N content was 0.25 ± 0.03 g/kg, the total P content was 0.36 ± 0.04 g/kg, and the total K content was 18.24 ± 1.22 g/kg (mean ± SE, n = 10). To test the interactive effects of nutrient availability and enemy suppression on alien plant invasion into resident native communities, we assigned the 32 pots of each alien target species to two levels of nutrient availability (without vs with nutrient) treatments fully crossed with two levels of enemy suppression (without vs with enemy suppression). In other words, per alien species, we had eight pots (i.e., replicates), in each of the four treatment combinations. To create different nutrient availability treatments, the soil was evenly mixed evenly with 6 g water-soluble fertilizer (20% N, 20% P₂O₅, 20% K₂O, g⁄g, Peters Professional, Scotts, Geldermalsen, The Netherlands) as an added nutrient treatment (with nutrient). For the treatment with natural enemies suppression, we sprayed the aboveground parts of the plants with a broad-spectrum insecticide (concentration: 2 ml L^− 1 ; main ingredients: chlorpyrifos and fenvalerate; The Dow Chemical Company, Midland, USA) and also added to the soil a solution consisting of a mixture of the same broad-spectrum insecticide (concentration: 2 ml L^− 1 ) and two broad-spectrum fungicides with the main ingredients benzimidazole (1.5 g L^− 1 ; Nufarm Limited, Contatti, Italy) and copper oxychloride (1.5 g L^− 1 ; Dupont agricultural Products, Washington DE, United States) every other week (Wang et al. 2019; Zheng et al. 2015). For the control treatment without enemy suppression, we sprayed the plants with water and added corresponding amounts of water to the soil.

During the experiments, we watered all plants to meet the demand of plant growth. And the pots were randomly positioned and reshuffled every 12 days to avoid effects of possible environment differences. The experiment was conducted from August to October 2015 (70 days). Our experiment lasted for 10 weeks in a greenhouse under natural sunlight. During the experiment, the mean temperature in the greenhouse was set to 27.7°C and the relative humidity to 70.5% (measured by Amprobe TR300, Amprobe, Everett, WA, USA). Light intensity in the greenhouse was 70% of that outside.

Plant harvest and measurements

At the end of experiment, plants were harvested and separated into above-ground and below-ground parts of target species and native community in each pot. All biomass samples were dried at 65°C for 72 hours and then weighed. Moreover, we used biomass proportion as an indicator of plant growth of alien species in the whole community, and it was calculated from the proportion of total mass of the alien target plant to total biomass of the whole community (alien target species plus sum of biomass of the three native species). In addition, we calculated evenness of native community using the Shannon evenness index: J′=H′/ln(S), where H′ is the Shannon–Wiener diversity index: H′ = −Σp_iln(p_i), where p_i is the proportional biomass of each species and S is the number of species in the community (Kardol et al. 2010).

Statistical analyses

To test for differences in biomass production between target alien species and native community in response to nutrient addition and enemy suppression, we fitted a linear mixed-effects model in R 4.1.1 (R Core Team and Team 2021) using the lme function in the nlme package (Pinheiro et al. 2017; Pinheiro et al. 2020). To improve normality and homoscedasticity of the residuals, above-ground biomass production, biomass production and root/shoot ratio of alien target species and the native communities were log-transformed, biomass proportion of the alien target species and native communities in each pot was logit-transformed, and evenness of native community was asin- transformed prior to analyses. The fixed part of the model included nutrient addition (with nutrient vs. without nutrient), enemy (with enemy suppression vs. (without enemy suppression) and all their interactions. To account for non-independence of plants from the same species, and non-independence of species from the same genus, part of models included family, species (nested within genus) as random effects.

Biomass of alien target species and native community

Nutrient addition significantly increased total biomass production and above-ground biomass of alien target plant species and native community, respectively (total biomass production and above-ground biomass production-alien species vs native community: 257.6% vs 527.7%, and 320.0% vs 604.3%; Fig. 1a-b, d-e, Table 1). However, nutrient addition significantly decreased biomass proportion of alien species in comparison to the increasing of native community (alien species vs native community: -13.6% (from 58.9–45.3%) vs 13.6% (from 41.1–54.7%); Fig. 1c, f, Table 2). The presence of enemy marginally significantly increased biomass proportion of alien plants and decreased that of native community (alien target species vs native community: 6.1% (from 49.6–52.6%) vs -6.1% (from 50.4–47.4%), Fig. 1c, f, Table 2). Specially, compared to with nutrient addition treatment, the presence of enemy increased biomass proportion of alien plants 10.9% (from 54.8–60.7%) and decreased that of native community − 13.1% (from 45.2–39.3%) under without nutrient addition (Fig. 1c, f, Table 2).

The present of enemy increased above-ground biomass and total biomass of alien plants and native community under nutrient addition (24.7% vs 8.8% and 34.3% vs 11.1%, Fig. 1b, e, Table 1), whereas the opposite was true under without nutrient addition (-5.8% vs -18.0% and − 4.1% vs -16.8%, Fig. 1b, e, Table 1) (significant interaction of Nutrient × Enemy). Therefore, the positive effect of the enemy suppression (i.e., absence of enemy) was great when without nutrient addition, and the effect turned over under nutrient addition. From the results, nutrient addition promotes biomass compensation of enemies' feeding.

Table 1

Linear mixed-effect models testing the effects of the nutrient-availability (without vs with nutrient) and enemy suppression (without vs with enemy suppression) treatments and their interactions on above-ground biomass and total biomass of the alien target species and the native communities. Significant effects (P < 0.05) are in bold, while marginal significant effects (0.05 < P < 0.1) are underlined.
Explanatory variables (Fixed and random effects)		Above-ground biomass of alien target species (natural-log-transformed)		Total biomass of alien target species (natural-log-transformed)		Above-ground biomass of native communities (Natural-log-transformed)		Total biomass of native communities (natural-log-transformed)
Explanatory variables (Fixed and random effects)	Df	χ2	P	χ2	P	χ2	P	χ2	P
Nutrient availability (N)	1	218.447	0.000	171.388	0.000	356.079	0.000	322.452	0.000
Enemy suppression (ES)	1	0.851	0.851	1.980	0.159	1.034	0.309	0.515	0.473
N × ES	1	3.285	0.070	4.242	0.039	4.698	0.030	4.576	0.032
Random effects		SD		SD		SD		SD
Family		0.000		0.143		0.079		0.035
Species		0.706		0.684		0.241		0.255
Residual		0.630		0.666		0.411		0.408
R² of the model		Marginal	Conditional	Marginal	Conditional	Marginal	Conditional	Marginal	Conditional
R² of the model		0.368	0.720	0.309	0.671	0.804	0.858	0.785	0.846

* Standard deviations for individual alien species random effects for the saturated model are found in Table S4.

Table 2

Linear mixed-effect models testing the effects of the nutrient-availability (without vs with nutrient) and enemy suppression (without vs with enemy suppression) treatments and their interactions on biomass proportion of the alien target species and the native communities and the evenness of native communities. Significant effects (P < 0.05) are in bold, while marginal significant effects (0.05 < P < 0.1) are underlined.
Explanatory variables (Fixed and random effects)		Biomass proportion of the alien target species (logit-transformed)		Biomass proportion of the native communities (logit-transformed)		The evenness of native communities (asin-transformed)
Explanatory variables (Fixed and random effects)	Df	χ2	P	χ2	P		χ2	P
Nutrient availability (N)	1	27.023	0.000	27.041	0.000		110.936	0.000
Enemy suppression (ES)	1	3.301	0.069	3.314	0.069		4.844	0.028
N × ES	1	1.236	0.266	1.225	0.268		3.022	0.082
Random effects		SD		SD		SD
Family		0.150		0.150		0.000
Species		0.855		0.856		0.114
Residual		0.670		0.670		0.224
R² of the model		Marginal	Conditional	Marginal	Conditional		Marginal	Conditional
R² of the model		0.088	0.660	0.088	0.660		0.311	0.452

* Standard deviations for individual alien species random effects for the saturated model are found in Table S4.

Effects on evenness of native communities

Nutrient addition and enemy suppression significantly decreased evenness of native community (-24.3% and − 1.6%; Fig. 2, Table 2), whereas the negative effect of enemy suppression was maximal under nutrient addition (nutrient addition vs without nutrient addition: -12.1% vs -0.9%; Fig. 2, Table 2).

Effects on root-shoot ratio of alien target species and native communities

Nutrient addition significantly decreased root-shoot ratio of native community and alien target species (-30.1% vs -51.5%; Fig. 3). The presence of enemy significantly increased root-shoot ratio of native community and alien target species (2.1% vs 1.5%; Fig. 3). However, the negative effect of enemy suppression on alien target species was maximal when under nutrient addition (nutrient addition vs without nutrient addition: -55.5% vs -40.7%; Fig. 3b) (significant interaction of Nutrient × Enemy). Most clonal target alien species (A. philoxeroides, S. trilobata, T.repens) showed similar pattern of root-shoot ratio to those when all alien species were used (Figs. S1- S2).

Table 3

Linear mixed-effect models testing the effects of the nutrient-availability (without vs with nutrient) and enemy suppression (without vs with enemy suppression) treatments and their interactions on root-shoot ratio of the alien target species and the native communities. Significant effects (P < 0.05) are in bold, while marginal significant effects (0.05 < P < 0.1) are underlined.
Explanatory variables (Fixed and random effects)		Root-shoot ratio of the alien target species (natural-log-transformed)		Root-shoot ratio of native communities (natural-log-transformed)
Explanatory variables (Fixed and random effects)	Df	χ2	P	χ2	P
Nutrient availability (N)	1	58.636	0.000	81.903	0.000
Enemy suppression (ES)	1	5.027	0.025	10.282	0.001
N × ES	1	3.276	0.070	1.582	0.208
Random effects
Family		0.000		0.000
Species		0.637		0.000
Residual		0.478		0.302
R² of the model		Marginal	Conditional	Marginal	Conditional
R² of the model		0.186	0.707	0.295	0.295

* Standard deviations for individual alien species random effects for the saturated model are found in Table S4.

Our multi-species experiment showed that nutrient addition and enemy suppression (i.e., absence of enemy) significantly increased both the total biomass production and biomass proportion of native community. Conversely, enemy release (i.e., presence of enemy) and without nutrient addition were found to increase biomass proportion of alien plants while decreasing that of the native community. Therefore, the positive effect of presence of enemy on alien plants to some extent was great when without nutrient addition. The negative effect of enemy suppression on evenness of native community and on root-shoot ratio of alien target species was maximal under nutrient addition, which promoted the selected effect of native plant and competitive dominance. These findings imply that high nutrient and enemy suppression can better enhance the resistance of native communities to invasion of alien plants, and nutrient limitation and enemy release environments might promote invasive success of alien plants.

Effects on biomass production

Not surprisingly, we found that nutrient addition and enemy suppression (i.e., absence of enemies) significantly increased total biomass production and biomass proportion of native community (Fig. 1). This is consistent with findings of previous studies (Li et al., 2022b; Ren et al., 2021;van Kleunen et al., 2010; but Gao et al., 2023; Heckman et al., 2016; Meijer et al., 2016). More importantly, the presence of enemies and without nutrient supply raised biomass proportion of alien plants and decreased that of native community, in which indicated that enemies marginally positively affected the performance of alien target species in native communities when nutrient deficiency. The reason for this result may be competitive advantage and compensation effects between native communities and invasive plants under different nutrient and herbivory environments. On the one hand, under conditions of limited resources, alien target species may have higher resource utilization efficiency and growth performance than native communities (Funk and Vitousek 2007; Heberling and Fridley 2013; Li et al. 2022b; Littschwager et al. 2010; Liu et al. 2019; Wang et al. 2019; Zhang et al. 2021a). On the other hand, those that originated in fertile habitats frequently have relatively higher resource requirements and utilization skills than those that originated in poor habitats, such as sandy soils or semi-arid areas, typically have lower resource requirements. (Funk 2013; Grassein et al. 2010; Grime 1977; Wang et al. 2022a; Wright et al. 2004). Most of the alien target species used in this experiment initially invaded barren and impoverished areas (Hyun et al. 2020; Khatun et al. 2010; Marks 1983; Snaydon 1962). This may also be one of the reasons why alien invasive species have stronger competitiveness in low-nutrient environments. In addition, in the absence of nutrient additions, alien target species in invasion areas lacking specialist enemies and the preference of generalist enemies can allocate more resources to their own growth compared to native communities facing both specialist and generalist enemies (Keane and Crawley 2002; Meijer et al. 2016; Wang et al. 2019; Zhang et al. 2018). And native species in resident communities also faced more enemies than invasive target species (i.e., co-existing native herbivore) in invaded areas (Keane and Crawley 2002; Zhang et al. 2020), which also results in greater compensatory effects. Therefore, enemy release will marginally reduce the invasion resistance of native communities and promote the invasion of alien plants under without nutrient additions. Meanwhile, enemy suppress promote native community and alien target species biomass under nutrient addition, in line with previous findings that plants compensate for or tolerate enemies more when growing with nutrient supply (Gange 2000; Garcia and Eubanks 2019; Getman-Pickering et al. 2021; Hawkes and Sullivan 2001; Jin et al. 2022; Meyer 2000; Ramula et al. 2019; Wang et al. 2019; Zhong et al. 2021).

Effects on evenness of native communities

Our finding indicated that the negative impact of enemy suppression on the evenness of the native community was greatest under nutrient addition compared to without. The proportion of the native community increased (Fig. 1f), even though the evenness of the native community decreased under nutrient conditions (Fig. 2). As a result, the dominant species Glechoma longituba produced significantly more biomass (Fig. S1a, b), which marginally inhibited the invasion of alien target plants both above- and below- ground. Our results were consistent with the previous findings (Li et al. 2022b; Parepa et al. 2013; Roscher et al. 2016) that species with strong competitive abilities can better utilize available resources, leaving fewer resources for invasive species due to selection effects (Adomako et al. 2019; Li et al. 2022a; Van Ruijven and Berendse 2003), As a result of nutrient addition, some key species in native communities with high competitiveness accumulate more biomass and occupy more resources, effectively inhibiting invader invasion.

Effects on root-to-shoot ratio

We observed that after nutrient availability increased and enemy suppression, alien species exhibiting a greater decrease in root-to-shoot ratio than native community (Fig. 3), which are consistent with these findings that differences in root and shoot allocation exist between invasive alien and native species (Van Kleunen et al. 2010), and invasive species have lower root-shoot ratios than non-invasive species at a given total biomass (Schlaepfer et al. 2010). The negative effect of enemy suppression on the root-to-shoot ratio of alien target species, however, was greatest when nutrients were added. This outcome might be the result of causes both above and below ground. On the one hand, when using pesticides to suppress enemies, both invasive and native community are hardly damaged (as previously demonstrated in our lab by Wang et al., 2019). At this point, the increase in soil nutrient content triggers native community selection effects (Zhang et al. 2021a), enhancing the competitive advantage of the dominant species Glechoma longituba, which prioritizes resource allocation to its roots, thus occupying soil nutrient resources and suppressing the invasion of alien species. Under without nutrients addition and with the presence of enemies, when invasive plants grow in a competitive environment, there is no significant difference in root-to-shoot ratio between native community and invasive plants. This is mainly because the dominant species in the native community do not grow prominently under without nutrients addition. In our greenhouse experiment, the main enemies are generalist herbivores, including the larvae of the striped stem borer and the cabbage looper (Y-J Wang, personal observation), which are likely to feed on both native and invasive plants (Wang et al. 2019). On the other hand, the soil biota has a positive effect on plant growth (Jin et al. 2022; Lussenhop and BassiriRad 2005; Mehring and Levin 2015; Partsch et al. 2006). However, a higher root-to-shoot ratio is related to the ability of plants to access below-ground resources (nutrients and water) and is crucial for establishing ecosystems in competitive environments (Casper and Jackson 1997; Ferguson et al. 2015). Therefore, a larger root system in native communities and a stronger and more stable below-ground plant-biota network formed with soil biota are more conducive to nutrient acquisition and biomass growth advantages, inhibiting the invasion of exotic plants.

Potential limitations

One caveat for our study is that because our native community only used a single fixed set of native plant species, random distinction possibilities of the diversity effect were not considered (Abernathy et al. 2016; Liao et al. 2015; Qin et al. 2020). However, our native community composition and diversity were designed based on the previously field investigation. Meanwhile, our study was conducted in a greenhouse and was rather short-time. Finally, we found that not all alien target species responded to the nutrient and enemy suppression treatment in the same way.

Our results showed that enemy release (i.e., presence of enemy) increased biomass proportion of alien plants and decreased that of native community under without nutrient addition. Furthermore, the negative effect of enemy suppression on the evenness of the native community and the root-to-shoot ratio of alien target species was greatest under nutrient addition. Therefore, nutrient deficiency and natural enemies might promote the invasive success of alien species in native community, whereas nutrient addition and enemy suppression can better enhance the resistance of native plant communities to invasion. This implies that with increasing eutrophication, native communities may develop better invasiveness resistance.

Acknowledgements

We thank L. Xu for the practical assistance. This research was supported by the National Natural Science Foundation of China (32171510, 31770449).

Author contributions

Y.J.W. and Y.F.B. designed the experiment. Y.Y.L. performed the experiment. Y.H.X. and Y.J.G. carried out the statistical analysis. Y.H.X. wrote the first draft of the manuscript. Y.J.W., Y.F.B. and Z.G.Y. contributed substantially to the revisions.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Data accessibility

The raw data are available on request to the corresponding author

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Soil nutrient limitation and natural enemies promote the establishment of alien species in native community

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Introduction

Materials and methods

Species selection

Experimental set-up

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Results

Biomass of alien target species and native community

Effects on evenness of native communities

Effects on root-shoot ratio of alien target species and native communities

Discussion

Effects on biomass production

Effects on evenness of native communities

Effects on root-to-shoot ratio

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