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Xiang-Qin Li, Sai-Chun Tang, Yu-Mei Pan, Chun-Qiang Wei, Shi-Hong Lü, Increased precipitation magnifies the effects of N addition on performance of invasive plants in subtropical native communities, Journal of Plant Ecology, Volume 15, Issue 3, June 2022, Pages 473–484, https://doi.org/10.1093/jpe/rtab103
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Abstract
Nitrogen (N) deposition, precipitation and their interaction affect plant invasions in temperate ecosystems with limiting N and water resources, but whether and how they affect plant invasions in subtropical native communities with abundant N and precipitation remains unclear.
We constructed in situ artificial communities with 12 common native plant species in a subtropical system and introduced four common invasive plant species and their native counterparts to these communities. We compared plant growth and establishment of introduced invasive species and native counterparts in communities exposed to ambient (CK), N addition (N+), increased precipitation (P+) and N addition plus increased precipitation (P+N+). We also investigated the density and aboveground biomass of communities under such conditions.
P+ alone did not enhance the performance of invasive species or native counterparts. N+ enhanced only the aboveground biomass and relative density of invasive species. P+N+ enhanced the growth and establishment performance of both invasive species and native counterparts. Most growth and establishment parameters of invasive species were greater than those of native counterparts under N+, P+ and P+N+ conditions. The density and aboveground biomass of native communities established by invasive species were significantly lower than those of native communities established by native counterparts under P+N+ conditions. These results suggest that P+ may magnify the effects of N+ on performance of invasive species in subtropical native communities where N and water are often abundant, which may help to understand the effect of global change on plant invasion in subtropical ecosystems.
摘要
氮沉降、降水以及它们的交互作用会影响氮和水是限制性资源的温带生态系统中的外来植物 入侵,但它们是否会影响以及怎样影响外来植物在富氮和降水丰富的亚热带植物群落中的入侵, 仍不清楚。本研究在亚热带生态系统中,在野外用12种常见本地植物构建群落,将4种入侵植物及其近缘的4种本地植物分别引入到群落中,对群落进行氮添加(0和5 g N m−2 a−1)和降水增加(自然降水和增加降水30%)交互处理,比较了引入的入侵植物和近缘本地植物在群落中的生长和定居表现以及群落特征(包括群落密度和地上生物量等)。研究结果显示,只增加降水没有提高入侵植物或近缘本地植物的表现;氮添加仅提高入侵植物地上生物量和相对密度;氮和降水同时增加提高了入侵植物和近缘本地植物在群落中的生长和定居表现。在氮添加、降水增加和氮与降水同时增加处理下,入侵植物的大多数生长和定居参数高于近缘本地植物。在氮与降水同时增加时,入侵植物所定居本地群落的密度和地上生物量显著低于近缘本地植物所定居本地群落的密度和地上生物量。这些结果说明,在富氮和降水丰富的亚热带本地群落中,降水增加扩大了氮增加对入侵植物表现的影响。这将有助于理解在富氮和降水丰富的亚热带生态系统中,全球变化对植物入侵的影响。
INTRODUCTION
Owing to anthropogenic activities, a large number of species were introduced to new ranges, and a small proportion of them has successfully established populations and became invasive species, imposing great threats to resident community and ecosystem functions (Cordero et al. 2016; Roura-Pascual et al. 2009). Previous studies have shown that invasive plants frequently display a higher relative growth rate and final biomass than native species, as well as stronger reproductive and competitive abilities (Kołodziejek 2019; Ni et al. 2018; Schultheis and MacGuigan 2018). However, the majority of previous studies were primarily based on comparisons between invasive and native species under the background of monoculture or a mixture with each other in greenhouse experiments (Schultheis and MacGuigan 2018; Zheng et al. 2009). Few studies have compared the performance of alien invaders in situ in a community with that of native counterparts. Using this approach, the superior performance of alien invaders will be demonstrated when the growth and establishment of alien species in a community are better than those of the native plants. Alien species inevitably interact with native species in a new community (Mitchell et al. 2006; Wang et al. 2004). Alien species can become successfully established before they start spreading and invading only by becoming dominant in a new community. Plant invasions are always related to the native community (Byun et al. 2020; Geng and He 2021; Pearson et al. 2018). Therefore, understanding whether the performance of invasive plants is superior to those of native plants in a community context will help to more effectively predict the invasive potential of alien plant species in a native community.
Many studies have shown that global environmental changes, such as increased temperature, nitrogen (N) deposition and precipitation, affect the degree of plant invasion (He et al. 2012; Liu et al. 2017; Luo et al. 2020). Anthropogenic N deposition is likely to increase the availability of soil N (Gilliam 2006). High concentrations of N enhance the performance of some invasive plants more than that of some native species (He et al. 2012; Pan et al. 2016; Seabloom et al. 2015; Wan et al. 2019). For example, the increase in biomass of the North American population of invasive Centaurea stoebe L. was 72% and 168% at low and high N deposition, respectively, while that of the native species was 56% and 122%, respectively (He et al. 2012). N addition also strongly influences the competitive dynamics of invasive and native plants (He et al. 2012; Pan et al. 2016; Vasquez et al. 2008). Similarly, altered precipitation will affect the availability of soil water. Invasive plants have been found to produce less biomass in drought environments and more biomass under wet conditions compared with native plants (Liu et al. 2017). Changes in the inputs of precipitation could also influence the balance of competition between alien and native plants (Pearson et al. 2017). Lower precipitation enhanced the competitive ability of invasive species Amaranthus retroflexus against native Glycine max (Jiang et al. 2018), and drought also provided the competitive advantage to invasive A. spinosus relative to non-invasive A. tricolor (Yu et al. 2022). However, most of these studies were conducted using single factors. The effects of multifactors may differ with that of a single factor (Schuster and Dukes 2017).
Environmental factors often change simultaneously, and these changes may have opposing, additive or synergistic effects on plants (Albert et al. 2011). Some studies have shown that there was an interaction in the availability of N and precipitation that affected the performance of invasive plants (Harpole et al. 2007; Schuster and Dukes 2017). For example, the addition of a combination of N and water increased the biomass of alien species Avena fatua and Lolium multiflorum (Harpole et al. 2007). Increased precipitation counteracted the inhibitory effect of N deposition on the growth of invasive Lonicera maackii (Schuster and Dukes 2017), While N addition increased the biomass of invasive species Lepidium virginicum when the water availability was low (Liu et al. 2018). However, these studies were primarily conducted in temperate regions where N and water are the major limiting factors (Harpole et al. 2007; Liu et al. 2018). It remains unclear whether the interaction of N and precipitation can affect the performance of invasive plants in subtropical systems in which N and precipitation are abundant.
Establishment is a crucial invasion phase of alien species and determines whether introduced species can persist and spread in native communities (Blackburn et al. 2011). The interactions between plant traits and environmental conditions significantly affect the success of the establishment of invasive species (Byun et al. 2015; Moles et al. 2008). The superior growth and establishment of alien species may enhance their dominance in communities, thus, promoting the success of their invasion. The ability of an alien plant to invade a community closely correlated with the availability of N (Pearson et al. 2017) and water (Maron and Marler 2008). N, water and their interaction had significant effects on invasive plants in temperate ecosystem (Liu et al. 2018; Pearson et al. 2017). Reductions in N availability under water addition could reduce establishment of the invasive species Gypsophila paniculata and Linaria dalmatica (Blumenthal 2009). However, the manner in which N addition, increased precipitation and their interaction will affect the growth and establishment of invasive species in subtropical native communities with abundant N and precipitation remains unclear.
In this study, we selected 12 common native plant species to construct artificial communities in an in situ field experiment in a subtropical system. We then introduced four invasive plant species and their native counterparts into the artificial communities, respectively. We tested the growth and establishment performance of the introduced species by examining their growth and quantitative characteristics, including plant height, density, aboveground biomass, relative height (RH), relative coverage (RC), relative density (RD), relative aboveground biomass (RB) and importance value (IV), in communities exposed to ambient conditions, N addition and increased precipitation. We also investigated characteristics of communities with invasive species and their native counterparts, which had been introduced under these conditions. We analyzed how N deposition, precipitation and their interaction affect performance of invasive plants, as well as their impacts on native communities. We hypothesized that (i) N addition (N+), increased precipitation (P+) and N addition plus increased precipitation (P+N+) enhance the growth and establishment of the introduced species in communities; (ii) invasive plants perform better than their native counterparts in the communities exposed to N+, P+ and P+N+; and (iii) the impacts of invasive species on native communities are elevated under N+, P+ and P+N+ conditions.
MATERIALS AND METHODS
Study site and species
This experiment was conducted in a field in Yanshan Town, Guilin City, Guangxi Province, China. The study region has a subtropical climate. The mean annual rainfall was 1741.7 mm, and the evaporation was 1300 mm from 1990 to 2013 (Liu et al. 2015). The mean annual temperature is 17.8 °C, and the mean annual temperatures of the coldest (January) and warmest (July) months are 5.8 and 28 °C, respectively.
We selected 12 native plant species based on regional species pool and different functional groups (grasses, forbs and legumes) to construct artificial plant communities. These plant species included: three Poaceae species (Apluda mutica, Digitaria sanguinalis and Arthraxon hispidus), three Compositae species (Artemisia annua, Artemisia argyi and Emilia sonchifolia), two Leguminosae species (Desmodium heterocarpon and Tadehagi triquetrum), Hedyotis auricularis (Rubiaceae), Plantago asiatica (Plantaginaceae), Achyranthes bidentata (Amaranthaceae) and Acalypha australis (Euphorbiaceae). Four alien species (Bidens pilosa, Senna tora, Paspalum conjugatum and Setaria palmifolia) and their native counterparts (Bidens biternata, Desmodium gangeticum, Paspalum thunbergii and Setaria viridis) were selected as the target plants and introduced into the artificial communities. All of the species used in the experiment are common in Guilin, and most of them frequently co-occurred in the field, except S. palmifolia. The four alien species are invasive plants that have occupied large areas and caused negative effects on farms and biodiversity in Guilin (Chen et al. 2008).
Experimental design
An abandoned field in Guilin City, Guangxi Province, China (110°18′01.8″ E, 25°04′49.6″ N; 170 m a.s.l.) was ploughed in January 2015 and harrowed three times before experimental plots were established in March 2015. Fifty-two plots (2 m × 2 m) were constructed using bricks, which were separated from each other by 0.5-m wide walkways. The plots were then filled with topsoil collected from foothills in which the experimental species were absent. The top 2-cm layer of topsoil was removed to reduce the number of original seeds. The topsoil was classified as limestone soil, with a pH of 7.43 ± 0.01. The contents of organic matter and available N, P and K in the soil were 36.33 ± 1.08 g kg−1, 96.94 ± 1.92 mg kg−1, 31.5 ± 3.62 mg kg−1 and 97.68 ± 0.96 mg kg−1, respectively.
In order to make the community context similar among the plots, we provided the same 12 species for each plot and the same germination chance for each species. We sowed 100 seeds for each of the 12 plant species in each plot to construct the artificial communities in March 2015. In the same year, we removed the plant species that were not included in the experiments. In March 2016, 100 seeds of each of the invasive species were introduced into half of the plots, and 100 seeds of each of the native counterparts were introduced into the other half of the plots. Each plot was considered as one community.
To simulate N deposition and an increase in precipitation, the plots were exposed to treatments of: (i) ambient N and precipitation (CK); (ii) only N addition (N+); (iii) only an increase in precipitation (P+) and (iv) N addition plus an increase in precipitation (P+N+). During the early period of this century, the average annual N wet deposition in China was recorded to be 21.1 kg ha−1 year−1 (Liu et al. 2013). Correspondingly, N+ treatment plots received 5 g m−2 N annually. NH4NO3 has been used to simulate N deposition in many experiments (He et al. 2012; Lu et al. 2019). We added N as NH4NO3 in solution using deionized water as described by He et al. (2012). A total amount of 57.14 g NH4NO3 was added to each N+ and P+N+ plot on three dates (20 April, 20 August and 20 December) each year during the experimental period. We increased the precipitation by 30% (approximately 12 L) for each P+ and P+N+ plot every day from July to December 2016 and from July 2017 to the first 10 days of October 2017 (end of the experiment). The amount of precipitation was calculated based on the mean annual precipitation and a plot area. There were seven replicates for the CK and N+ treatments, and six replicates for the P+ and P+N+ treatments for each origin of species (native versus invasive species). There were a total of 52 plots: [(CK and N +) × 7 replicates + (P + and P + N+) × 6 replicates] × 2 species origins = 52 plots.
Vegetation harvest and measurement
We measured the plant community characteristics at the peak of plant biomass between 9 and 25 October 2017. We divided the plants into species, and then measured the mean plant height, counted the individual numbers and visually estimated the species coverage for each species. The aboveground biomass of each species from each plot was harvested and then dried at 70 °C for 72 h and weighed. The three invasive species (B. pilosa, S. tora and P. conjugatum) and three native counterparts (B. biternata, D. gangeticum and P. thunbergii) were successfully established in all the plots with the exception of P. thunbergii, which could not be found in the N+ plots. The invasive S. palmifolia and its native counterpart S. viridis did not germinate in all the plots.
Data analyses
The growth performance of introduced invasive species and their native counterparts was determined using plant height, density and aboveground biomass. The ability of the introduced species in the community to become established was determined using the RH, RC, RD, RB and IV. These parameters present the status and function of species in the community. The community characteristics were examined using the community density (CD), community aboveground biomass (CB) and diversity indices, such as the species richness (SR, number of species in each plot) and the Shannon–Wiener diversity index (H′). Since our goal was to estimate the impact of the introduced species on native communities, the values for community characteristics excluded the values of the introduced species.
The parameters were calculated as follows:
The community characteristics were determined as follows: CD = summation of density of all species in a plot; CB = summation of aboveground biomass of all species in a plot; SR = the number of species recorded in a community and , where Pi is the IV of each species in a community.
A three-way analysis of variance (ANOVA) was used to analyze the effect of N deposition, precipitation, species origin (invasive species and native counterparts) and their interactions on plant growth (plant height, density and aboveground biomass) and establishment performance (RH, RC, RD, RB and IV) of the introduced species, as well as the community characteristics (CD, CB, SR and H′). A one-way ANOVA with an LSD post hoc test was used to test the difference in the growth and establishment among treatments for invasive species or native counterparts, as well as the difference in community characteristics among treatments for communities established by invasive species or those established by native counterparts. An independent-sample t-test was used to examine the difference between invasive species and native counterparts, or the difference between communities established by invasive species and those established by native counterparts. The statistical significances of all the tests were set at P < 0.05. All the statistical analyses were performed using SPSS 18.0 (SPSS Inc., Chicago, IL, USA).
RESULTS
Growth performance of the introduced species in communities under N and precipitation treatments
Precipitation, N or species origin had no significant effects on the plant height. However, the interactive effects of the three factors on the plant height were significant (Table 1). Compared with the CK plots, P+N+ significantly increased the plant height of invasive species by 42.37%, whereas P+ and N+ significantly decreased the plant height of native counterparts by 38.93% and 33.30%, respectively (Fig. 1a). The plant height of invasive species was significantly lower than that of their native counterparts in the CK plots, but it was significantly higher than that of their native counterparts in the N+ and P+ plots. The plant height ratio of invasive species and their native counterparts was 0.72 under the CK plots, whereas the ratio increased to 1.34 and 1.33 in N+ and P+ plots, respectively (Fig. 1a).
Variable . | P . | N . | S . | P × N . | P × S . | N × S . | P × N × S . |
---|---|---|---|---|---|---|---|
Plant height | 3.57 | 0.18 | 2.65 | 14.50*** | 6.06* | 5.27* | 11.03** |
Density | 23.45*** | 15.86*** | 171.63*** | 5.00* | 2.73 | 5.31* | 2.29 |
Biomass | 89.56*** | 134.49*** | 212.34*** | 86.57*** | 58.26*** | 67.27*** | 19.31*** |
RH | 13.86** | 4.38* | 2.49 | 15.11*** | 4.90* | 1.98 | 2.66 |
RC | 1.09 | 8.79** | 41.15*** | 10.76** | 0.67 | 5.66* | 0.87 |
RD | 15.31*** | 19.91*** | 103.90*** | 0.83 | 0.34 | 14.77*** | 0.48 |
RB | 12.13** | 36.37*** | 64.53*** | 21.40*** | 16.96*** | 22.60*** | 5.13* |
IV | 1.09 | 13.92** | 88.43*** | 26.27*** | 7.38** | 18.86*** | 0.46 |
CD | 9.53** | 4.37* | 8.66** | 1.05 | 6.08* | 7.87** | 0.09 |
CB | 6.21* | 1.86 | 4.53* | 2.33 | 4.65* | 0.56 | 0.03 |
SR | 88.94*** | 3.01 | 0.82 | 1.89 | 0.82 | 0.13 | 0.13 |
H′ | 59.60*** | 0.70 | 0.59 | 2.09 | 0.14 | 0.00 | 0.20 |
Variable . | P . | N . | S . | P × N . | P × S . | N × S . | P × N × S . |
---|---|---|---|---|---|---|---|
Plant height | 3.57 | 0.18 | 2.65 | 14.50*** | 6.06* | 5.27* | 11.03** |
Density | 23.45*** | 15.86*** | 171.63*** | 5.00* | 2.73 | 5.31* | 2.29 |
Biomass | 89.56*** | 134.49*** | 212.34*** | 86.57*** | 58.26*** | 67.27*** | 19.31*** |
RH | 13.86** | 4.38* | 2.49 | 15.11*** | 4.90* | 1.98 | 2.66 |
RC | 1.09 | 8.79** | 41.15*** | 10.76** | 0.67 | 5.66* | 0.87 |
RD | 15.31*** | 19.91*** | 103.90*** | 0.83 | 0.34 | 14.77*** | 0.48 |
RB | 12.13** | 36.37*** | 64.53*** | 21.40*** | 16.96*** | 22.60*** | 5.13* |
IV | 1.09 | 13.92** | 88.43*** | 26.27*** | 7.38** | 18.86*** | 0.46 |
CD | 9.53** | 4.37* | 8.66** | 1.05 | 6.08* | 7.87** | 0.09 |
CB | 6.21* | 1.86 | 4.53* | 2.33 | 4.65* | 0.56 | 0.03 |
SR | 88.94*** | 3.01 | 0.82 | 1.89 | 0.82 | 0.13 | 0.13 |
H′ | 59.60*** | 0.70 | 0.59 | 2.09 | 0.14 | 0.00 | 0.20 |
Level of significance: *P < 0.05, **P < 0.01, ***P < 0.001.
Variable . | P . | N . | S . | P × N . | P × S . | N × S . | P × N × S . |
---|---|---|---|---|---|---|---|
Plant height | 3.57 | 0.18 | 2.65 | 14.50*** | 6.06* | 5.27* | 11.03** |
Density | 23.45*** | 15.86*** | 171.63*** | 5.00* | 2.73 | 5.31* | 2.29 |
Biomass | 89.56*** | 134.49*** | 212.34*** | 86.57*** | 58.26*** | 67.27*** | 19.31*** |
RH | 13.86** | 4.38* | 2.49 | 15.11*** | 4.90* | 1.98 | 2.66 |
RC | 1.09 | 8.79** | 41.15*** | 10.76** | 0.67 | 5.66* | 0.87 |
RD | 15.31*** | 19.91*** | 103.90*** | 0.83 | 0.34 | 14.77*** | 0.48 |
RB | 12.13** | 36.37*** | 64.53*** | 21.40*** | 16.96*** | 22.60*** | 5.13* |
IV | 1.09 | 13.92** | 88.43*** | 26.27*** | 7.38** | 18.86*** | 0.46 |
CD | 9.53** | 4.37* | 8.66** | 1.05 | 6.08* | 7.87** | 0.09 |
CB | 6.21* | 1.86 | 4.53* | 2.33 | 4.65* | 0.56 | 0.03 |
SR | 88.94*** | 3.01 | 0.82 | 1.89 | 0.82 | 0.13 | 0.13 |
H′ | 59.60*** | 0.70 | 0.59 | 2.09 | 0.14 | 0.00 | 0.20 |
Variable . | P . | N . | S . | P × N . | P × S . | N × S . | P × N × S . |
---|---|---|---|---|---|---|---|
Plant height | 3.57 | 0.18 | 2.65 | 14.50*** | 6.06* | 5.27* | 11.03** |
Density | 23.45*** | 15.86*** | 171.63*** | 5.00* | 2.73 | 5.31* | 2.29 |
Biomass | 89.56*** | 134.49*** | 212.34*** | 86.57*** | 58.26*** | 67.27*** | 19.31*** |
RH | 13.86** | 4.38* | 2.49 | 15.11*** | 4.90* | 1.98 | 2.66 |
RC | 1.09 | 8.79** | 41.15*** | 10.76** | 0.67 | 5.66* | 0.87 |
RD | 15.31*** | 19.91*** | 103.90*** | 0.83 | 0.34 | 14.77*** | 0.48 |
RB | 12.13** | 36.37*** | 64.53*** | 21.40*** | 16.96*** | 22.60*** | 5.13* |
IV | 1.09 | 13.92** | 88.43*** | 26.27*** | 7.38** | 18.86*** | 0.46 |
CD | 9.53** | 4.37* | 8.66** | 1.05 | 6.08* | 7.87** | 0.09 |
CB | 6.21* | 1.86 | 4.53* | 2.33 | 4.65* | 0.56 | 0.03 |
SR | 88.94*** | 3.01 | 0.82 | 1.89 | 0.82 | 0.13 | 0.13 |
H′ | 59.60*** | 0.70 | 0.59 | 2.09 | 0.14 | 0.00 | 0.20 |
Level of significance: *P < 0.05, **P < 0.01, ***P < 0.001.
Precipitation, N and species origin significantly affected the plant density. The interaction of N with precipitation or species origin on the density was also significant (Table 1). Compared with the control treatment, P+N+ significantly increased the plant density by 93.71% for invasive species and by 163.58% for their native counterparts (Fig. 1b). P+ also significantly increased the plant density of the native counterparts by 82.92% (Fig. 1b). The plant densities of invasive species were consistently greater than those of their native counterparts in all the treatments. The plant density ratio of invasive species and their native counterparts was 4.58, 4.11, 3.01 and 3.37 in the CK, N+, P+ and P+N+ plots, respectively (Fig. 1b).
The effects of precipitation, N, species origin and their interactions on the aboveground biomass were significant (Table 1). Compared with the CK plots, N+ and P+N+ increased the aboveground biomass of invasive species by 43.03% and 260.28%, respectively. Only P+N+ increased the aboveground biomass of their native counterparts by 47.33% (Fig. 1c). The aboveground biomass of invasive species was significantly higher than that of their native counterparts in all the treatments with the exception of the CK. The aboveground biomass ratio of the invasive species and their native counterparts was 1.28 in the CK plots, whereas the ratio increased to 2.13, 2.21 and 3.14 in the N+, P+ and P+N+ plots, respectively (Fig. 1c).
Establishment performance of the introduced species in communities under N and precipitation treatments
Precipitation and N had significant effects on the RH. The interaction of precipitation with N or species origin on the RH was also significant (Table 1). Compared with the CK plots, N+, P+ and P+N+ significantly decreased the RH of native counterparts by 37.36%, 47.44% and 39.09%, respectively, but they had no effect on the RH of invasive species (Fig. 2a). The RH of invasive species was significantly higher than that of their native counterparts in the P+ plots (Fig. 2a).
Species origin, N and their interactions significantly affected the RC (Table 1). Compared with the CK plots, P+N+ significantly increased the RC of invasive species by 96.51%, while P+ decreased that of their native counterparts by 64% (Fig. 2b). The RC of invasive species was significantly greater than that of their native counterparts in the N+, P+ and P+N+ plots. The RC ratio of invasive species and their native counterparts was 2.25 in the CK, whereas the ratio increased to 5.54, 4.29 and 3.55 in the N+, P+ and P+N+ plots, respectively (Fig. 2b).
Precipitation, N and species origin had significant effects on the RD. The interaction of N and species origin on the RD was also significant (Table 1). Compared with the CK plots, N+ and P+N+ significantly increased the RD of invasive species by 81.99% and 156.63%, respectively. P+ and P+N+ increased the RD of their native counterparts by 182.82% and 231.63%, respectively (Fig. 2c). The RD of invasive species was consistently greater than that of their native counterparts under all conditions. The RD ratio of invasive species and their native counterparts was 4.79, 7.04, 2.29 and 3.71, in the CK, N+, P+ and P+N+ plots, respectively (Fig. 2c).
The effects of precipitation, N, species origin and their interactions on the RB were significant (Table 1). P+ significantly decreased the RB of native counterparts by 47.61%, and P+N+ increased the RB of invasive species by 238.17% compared with the CK plots (Fig. 2d). The RB of invasive species was significantly greater than that of their native counterparts under all plots with the exception of the CK. The RB ratio of invasive species and their native counterparts was 1.23 in the CK, whereas the ratio increased to 2.23, 2.56 and 3.77 in the N+, P+ and P+N+ plots, respectively (Fig. 2d).
Nitrogen, species origin and their interaction significantly affected the IV. The interaction of precipitation with N or species origin on the IV was also significant (Table 1). P+N+ significantly increased the IV of invasive species by 68.02%, while P+ decreased the IV of their native counterparts (Fig. 2e). The IV of invasive species was significantly greater than that of their native counterparts in all of the plots with the exception of the CK. The IV ratio of invasive species and their native counterparts was 1.21 in the CK, whereas it increased to 2.11, 1.86 and 2.42 in the N+, P+ and P+N+ plots, respectively (Fig. 2e).
Characteristics of communities established by invasive species and their native counterparts under N and precipitation treatments
Precipitation, N and species origin significantly affected the CD. The interaction of species origin with precipitation or N on the CD was also significant (Table 1). The CD established by invasive species in the N+ and P+N+ plots was 37.04% and 32.81% lower than that in the CK, respectively. The CD established by native counterparts in the P+ and P+N+ plots was 32.83% and 25.32% lower than that in the CK, respectively (Fig. 3a). The CD established by invasive species was 44.60% and 20.84% lower than that established by native counterparts in the N+ and P+N+ plots, respectively (Fig. 3a). The ratio of CD established by invasive species and that established by native counterparts was 0.88 in the CK, whereas the ratio decreased to 0.55 and 0.79 in the N+ and P+N plots, respectively (Fig. 3a).
Precipitation and species origin had significant effects on the CB (Table 1). The CB established by invasive species in the P+N+ plots was 15.19% lower than that in the CK, but the CB established by native counterparts in the P+ and P+N+ plots was 54.01% and 36.34% greater than that in the CK, respectively (Fig. 3b). Furthermore, the CB established by invasive species in the P+N+ plots was 34.43% lower than that established by native counterparts (Fig. 3b). The ratio of CB established by invasive species and that established by native counterparts was 1.05 in the CK, whereas the ratio decreased to 0.66 in the P+N+ plots (Fig. 3b).
Precipitation significantly affected the SR and H′ (Table 1). The SR of communities established by native counterparts in the P+ and P+N+ plots was 98.65% and 108.11% higher than that in the CK, respectively. The SR of communities established by invasive species in the P+ and P+N+ plots was 89.19% and 86.04% higher than that in the CK, respectively (Fig. 3c). The H′ of communities established by native counterparts in the P+ and P+N+ plots was 51.74% and 50.48% higher than that in the CK, respectively, and that established by invasive species in the P+ and P+N+ plots was 55.40% and 49.39% higher than in the CK, respectively (Fig. 3d). There were no significant differences in the SR and H′ between communities established by invasive species and those established by native counterparts under all treatments (Fig. 3c and d).
DISCUSSION
Growth and establishment of the introduced species in communities under N and precipitation treatments
We examined the growth and establishment of the invasive species and their native counterparts following their introduction in subtropical communities at ambient conditions and with N addition and increased precipitation. We found that P+ alone did not affect the performance of invasive species, whereas it decreased all of the growth and establishment parameters of their native counterparts with the exception of plant density and RD. N+ increased the aboveground biomass and RD of invasive species but had no positive effects on their native counterparts. P+N+ greatly increased all of the growth and establishment parameters of invasive species, with the exception of RH, and also increased the plant density, aboveground biomass and RD of their native counterparts. Therefore, our results provide some support for our first hypothesis: N+ enhanced only the aboveground biomass and RD of the invasive species. P+N+ enhanced the growth and establishment performance of both the invasive species and native counterparts, but P+ alone did not enhanced the performance of the invasive species or native counterparts.
Typically, N is a major limiting factor in temperate regions, whereas it is rich in subtropical ecosystems (Du et al. 2020). We detected no impact of N addition on the native counterparts, suggesting these native counterparts did not experience N limitation in this region. Nevertheless, we found that N addition increased the aboveground biomass and RD of invasive species. A possible explanation is that invasive species have higher phenotypic plasticity, enabling them to maximize performance under conditions when the availability of resources increases (Dawson et al. 2012; Richards et al. 2006; van Kleunen et al. 2010). Our findings in subtropical native communities are consistent with those studies that were conducted in temperate regions and showed that N addition favored the invasive species over native species (Brooks 2003; He et al. 2012; Seabloom et al. 2015; Vasquez et al. 2008; Wan et al. 2019).
Our findings that P+ alone did not enhance the growth and establishment of the introduced species suggest that water is not the major limiting factor for the introduced species. In contrast, we found that increased precipitation decreased some parameters of the native counterparts, such as plant height, aboveground biomass, RH, RC, RB and IV. It is unclear whether this could be related to nutrient leaching owing to a high input of precipitation (Diao et al. 2018), since we did not examine the soil water content and nutrient characteristics during the experimental periods. A lower adaptability to nutrient changes caused by increasing precipitation may result in the inferior growth of native species under P+. Zhu et al. (2016) also found that input of high precipitation reduced the net primary production of grasslands. Further studies should focus on the relationship between plant growth and changes in soil status in subtropical ecosystems.
The effects of the availability of N and water on plants were generally interdependent (Harpole et al. 2007; Liu et al. 2018; Schuster and Dukes 2017). We found that N+ had a positive effect while P+ alone had no significant effects on invasive species, and P+N+ substantially increased all the growth and establishment parameters of invasive species. Compared with the control, the aboveground biomass and RD of the invasive species increased 43.03% and 81.99% under N+, respectively, whereas they increased 260.28% and 156.63% under P+N+, respectively. Therefore, our results indicate that the increase of precipitation stimulates N effect on the invasive species in subtropical systems. This could be owing to the increased precipitation that could enhance the efficiency of N utilization by invasive species. Schuster and Dukes (2017) also found that increased precipitation under N deposition enhanced the growth of invasive L. maackii. Further experiments should focus more closely on the relationship between the efficiency of N utilization and the availability of water to invasive species in subtropical regions.
By comparing the growth and establishment status of alien invasive species in communities with that of native counterparts, the superior performance of alien invaders will be demonstrated when the growth and establishment of alien species are better than that of their native counterparts when resource are more available. We found that the growth and establishment parameters, aside from density and RD, were not significantly greater for invasive species than for their native counterparts under the CK. However, under N+, P+ and P+N+ conditions, all the growth and quantitative characteristics of invasive species were greater than those of their native counterparts. These results support our second hypothesis that the ability of invasive species to grow and become established is superior to that of their native counterparts in a community setting under conditions of N+, P+ and P+N+.
We found that all the growth and establishment performance of invasive species were greater than those of their native counterparts under the N+, P+ and P+N+ treatments. This may be related to the superior competitive ability and more effective utilization of resources by invasive species (Dawson et al. 2014; Hinz and Schwarzlaender 2004; van Kleunen et al. 2010). Our finding is consistent with the resource availability hypothesis which posited that invasive plants could increase their performance to a greater extent than native species when resources were more available (Blumenthal 2005; González et al. 2010). Additionally, the density of invasive species was consistently greater than that of their native counterparts in all conditions. This was partly attributed to their higher reproductive capacity, germination and survival rate than their native counterparts, since we sowed 100 seeds of each species per plot to give them the same chance to germinate in native communities. The higher plant density of invasive species may increase their likelihood of becoming established, spreading and invading new areas (Gupta and Narayan 2012). The results from our analysis could be important to predict the potential of invasive species to spread in subtropical communities under scenarios of N addition and increased precipitation in relation to future global changes.
Characteristics of communities established by invasive species and their native counterparts under N addition and increased precipitation
We compared the characteristics of communities in which invasive species were introduced with those of communities in which native counterparts were introduced under ambient, N addition and precipitation conditions. Using this approach, the negative effects of invasive species will be shown when the impacts of invasive species on native communities are greater than those of their native counterparts on the communities. We found that the density and aboveground biomass did not differ significantly between communities established by invasive species and by native counterparts under control or P+. In other words, the impacts of invasive species on native communities were similar to that of native counterparts under control or P+. However, under P+N+, the density and aboveground biomass of communities established by invasive species were significantly lower than that of communities established by native counterparts. This meant that the impacts of invasive species on native communities were elevated under P+N+. These results provide partial support for our third hypothesis: P+N+ elevated the impacts of invasive species on the density and aboveground biomass of native communities. This could be related to the ability of invasive species to compete for resources (Seabloom et al. 2003). The high ability of the invasive species to compete for resource under P+N+ resulted in greater density and biomass, which enhanced their negative effects on native plants, therefore, decreased the density and biomass of native communities. Some previous studies also suggested that an increase in the availability of resources could enhance the competitive advantage of invasive species (He et al. 2012; Thomsen et al. 2006; Wan et al. 2019).
Several studies have observed shifts in the diversity of species and community composition after invasive species became established (Levine et al. 2003; Pyšek et al. 2012; Vilà et al. 2011). However, we found that the diversity indices, such as SR and H′, were similar between communities established by invasive species and that established by native counterparts under all conditions. Some time lags could exist between the establishment of alien species and their spread to become an invasive species (Simberloff 2009). Rusterholz et al. (2017) also suggested that annual invasive Impatiens glandulifera could not reduce SR in both aboveground vegetation and soil seed banks until it had grown in a community for 5 years. The negative effects of the competition between invasive and native plants would occur only when the coverage and density of invasive species attained a certain degree (Kiełtyk and Delimat 2019; Michelan et al. 2018). Since our experiment only lasted for 2 years after the target species was introduced into the native communities, this could explain our results. It is possible that more serious negative effects could occur several years after the invasive species became established in a community.
CONCLUSIONS
We found that P+ alone did not affect the performance of invasive species. N+ promoted aboveground biomass and RD, while P+N+ significantly enhanced the growth and establishment of invasive species in subtropical native communities. These results indicate that P+ magnifies the effects of N+ on plant invasions in subtropical ecosystems. In addition, like many previous studies, we found that the growth and establishment of invasive species were superior to those of their native counterparts in communities under N+, P+ and P+N+. This suggests that invasive species are more effective than their native counterparts at responding to favorable environments in subtropical systems. Our results may increase our understanding of the effects of N deposition and precipitation on plant invasions in subtropical ecosystems. Further studies are needed to examine the soil characteristics (e.g. soil temperature, water content and nutrient conditions) under changes in N deposition and precipitation in subtropical ecosystems and analyze how they relate to plant invasions.
Acknowledgements
We are grateful to the Associate Editor and two anonymous referees for providing valuable comments.
Funding
This work was funded by the National Natural Science Foundation of China (31460165, 31960282), Natural Science Foundation of Guangxi Province (2018GXNSFAA281112) and Guangxi Key Laboratory of Plant Conservation and Restoration Ecology in Karst Terrain (19-050-6).
Conflict of interest statement. The authors declare that they have no conflict of interest.