Under rapid global environmental change, the negative effects of plant invasion on the environment, economic development, and human health continue to increase (Wu and Ding, 2019; Fantle-Lepczyk et al, 2022). In natural ecosystems, limited available resources cause intense bio-interactions among plant species that have similar resource requirements, thereby weakening their growth, survival, and reproduction, which leads to interspecific competition (Prass et al., 2022; Tumber-Davila et al., 2022). Invasive plants usually have higher rates of growth, diffusion, and reproduction than native plant species, which can make them easily become the dominant or even constructive species and thus enhance their competitive advantages, and this will strongly affect the community structure and interspecific competition patterns (Gu et al., 2021; Cai et al., 2022). Recent studies have found that the competitive relationship between invasive and native plants can also change with the invasion process and species coevolution (Liu et al, 2018). For instance, the negative effect of the invasive species Heracleum mantegazzianum has decreased over time (Dostal et al., 2013), while the native species Desmodium heterocarpon and Senna tora can replace the invasive species Mikania micrantha in the field due to their strong environmental tolerance (Jia et al., 2022). Exploring the competitive relationships among invasive plants and other plants under environmental changes can help in optimizing the biocontrol measures for plant invasions.

The current amount of atmospheric nitrogen deposition around the globe has increased by four times compared to the 18th century, and China has become the third largest nitrogen deposition area in the world, following closely behind Europe and North America, with a maximum volume of 63.53 kg N ha⁻¹ yr⁻¹ in South China (Lv and Tian, 2007; Liu et al., 2013). Nitrogen is a crucial element that limits plant growth and photosynthesis, and nitrogen supply levels significantly affect the plant invasion process (Pan et al, 2016; Slate et al., 2022). Invasive plants usually have higher nitrogen utilization efficiency due to their high nitrate reductase activity, and thus have higher growth rates than native plant species (Ren et al., 2019; Ren et al., 2022). Previous studies have found that nitrogen addition enhances the competitiveness of some invasive plants, such as Centaurea stoebe, Galinsoga quadriradiata, and Ambrosia artemisiifolia (Liu et al., 2018; Ren et al., 2022; Slate et al., 2022), and promote biomass accumulation in the invasive species Plantago virginica, but has no effect on its native congener P. asiatica (Luo et al., 2020). However, different nitrogen supply levels will change the competitive advantage of invasive plants. For example, the growth advantage of the invasive species Solidago canadensis compared to the native species Artemisia argyi was found to decrease with increasing soil nitrogen availability (Ren et al., 2021), and under low nitrogen levels, the invasive species Robinia pseudoacacia strongly inhibits the growth of native accompanying species Quercus acutissima, while high nitrogen levels reduce the competitiveness of R. pseudoacacia (Lou et al., 2014). Some studies have also found that nitrogen addition inhibits the growth of both invasive and native species (Ross et al., 2011). However, studies of interspecific competition between invasive plants and noninvasive alien plants are relatively rare (but see Wang et al., 2019a). Comparing the different responses of these two plant types to nitrogen addition can help to clarify plant invasion mechanisms and predict the succession dynamics of invaded communities.

Alternanthera philoxeroides, a noxious weed native to South America with clonal growth, has widely invaded many countries including the United States, China, New Zealand, Australia, and India (Wu et al., 2016; Wu et al., 2017a). Due to its strong phenotypic plasticity, A. philoxeroides has invaded terrestrial and aquatic habitats in more than 20 provinces in China, causing serious damage to ecosystem function and native plant diversity (Tanveer et al., 2018; Yan et al., 2020). Previous studies have shown that A. philoxeroides has a strong allelopathic effect on the seed germination, seedling growth, and biomass accumulation of native plants, and the allelopathic effect of the underground parts is higher than that of the aboveground parts (Cui et al., 2022; Hu et al., 2023). Global warming increases the interspecific competitiveness of A. philoxeroides with the native co-occurring species Digitaria sanguinalis (Wu et al., 2017b). Nitrogen addition significantly increases the aboveground biomass accumulation of A. philoxeroides, which benefits its rapidly invasion in new habitats (Wang et al., 2015). A few studies have found that some native plants have a stronger resistance to A. philoxeroides invasion (Wang et al., 2021; Zhang et al., 2021). Like A. philoxeroides, Oxalis articulata is also native to South America; it has strong environmental tolerance and has been introduced into China as a horticultural and ornamental plant, and is now widely used in urban greening, landscape configuration, and ecological corridor construction (Oberlander et al., 2009). O. articulata is a typical noninvasive alien species in China; its strong tuber propagation capacity and developed root system enable it to quickly occupy vacant niches (Shiraishi et al., 2005; Li et al., 2021). In addition, O. articulata has a lower leaf construction cost and allocates more nitrogen to photosynthesis (Feng et al., 2008). In natural ecosystems, O. articulata can coexist with A. philoxeroides in large areas ( Figure 1 ). Based on niche theory, screening noninvasive plants with strong competitiveness to occupy vacant niches, thus controlling replacement by invasive plants, would be beneficial for achieving sustainable ecological management of bioinvasions (Jia et al., 2022).

Currently, there are many studies on the competition between A. philoxeroides and native plants; however, competition between A. philoxeroides and noninvasive alien plants remains unclear, and it is crucial to understand this in order to predict situations of A. philoxeroides under increasing global nitrogen deposition. We conducted a greenhouse experiment to explore the effect of nitrogen addition on the performance of these two plants under different cultivation methods (monocultures and mixed cultures). We hypothesized that nitrogen would significantly affect their interspecific competitiveness. Specifically, we posed the following questions: (1) Do the biomass, nutritional, physiological, and photosynthetic traits of A. philoxeroides and O. articulata cause them to have heterogeneous responses to nitrogen addition? (2) Does nitrogen addition increase the resistance of O. articulata to A. philoxeroides invasion?

Soil N enrichment could significantly alter the structure of ecosystems and considered as the third largest killer seriously threatening species diversity, after land-use changes and biotic exchanges (Phoenix et al., 2006). We found that nitrogen addition significantly increased the maximum stem length and leaf area of O. articulata and A. philoxeroides in this study, indicating that it could relieve the constraints of limited resources on the growth of exotic plants and thus benefit their aboveground growth, as well as expand their living space and improve light utilization efficiency (Rickey and Anderson, 2004; Pan et al, 2016; Wang et al, 2020). However, nitrogen addition could also intensify the competition between coexisting plants for light resources (Xiao et al., 2021). The root is an important organ for plants to absorb soil nutrients (Xu et al., 2017), nitrogen addition decreased the root length but increased the root area of O. articulata in mixed cultures, which might be because nitrogen addition increases the availability of nitrogen in deep soil to the plant’s root system thus the plant reduces its resource investment in root length but increases the contact areas between the root and the soil to absorb more nitrogen (Xu et al., 2017; Wang et al., 2020; Zhang et al., 2020a). Overall, nitrogen addition led to greater advantages for morphological traits of O. articulata, but also increased the root length of A. philoxeroides in mixed cultures, indicating that A. philoxeroides tends to absorb more nitrogen in deep soils to resist the competition of O. articulata.

Intuitive impact of interspecific competition on plant growth was preferentially reflected in biomass change (Poorter et al., 2012). Previous studies found that nitrogen addition could significantly promote the biomass accumulation of alien plants and thus rapidly accelerate their invasion process (Davis and Pelsor, 2001; Daehler, 2003). However, in our study we found that nitrogen addition did not increase the biomass of O. articulata and A. philoxeroides. The reason for this might be that although invasive plants usually have higher nitrogen utilization rates, once invaded, they tend to evolve similar nitrogen adaptability to the co-occurring native plant species (Godoy et al., 2012). Particularly, the two plant species in this study were both alien species, thus the effect of nitrogen addition on their biomass allocation was not significant. Similar studies also showed that nitrogen addition did not increase the biomass of some invasive weeds (e.g., Centaurea diffusa) in North America (LeJeune et al., 2006; Cleland et al., 2011). However, we found that the biomass and root/shoot ratio of O. articulata were significantly higher than those of A. philoxeroides, which demonstrates the strong individual and underground competitive advantages of O. articulata.

The C:N ratio reflects the resource utilization strategy and efficiency of plants (Zhang et al., 2020b; Liu et al, 2021a). We found that nitrogen addition significantly increased the N content of A. philoxeroides in mixed cultures, making it higher than that of O. articulata, indicating that A. philoxeroides has stronger N accumulation ability than O. articulata. This is because nitrogen addition increases soil N enrichment and thus might alleviate the interspecific competition between plants (Liu et al., 2020). Moreover, the growth of invasive plants can usually better accumulate the increased soil nutrient pool, which makes them more capable of obtaining N under fluctuating resources (Liu et al., 2019). The C:N ratio of A. philoxeroides was higher than that of O. articulata in the control treatments, indicating that A. philoxeroides tends to evolve higher N utilization efficiency in an N-limited environment. Nitrogen addition decreased the C:N ratio of A. philoxeroides, suggesting that this plant might enhance protein synthesis in vivo at the cost of reducing N utilization efficiency. This trade-off of N utilization in A. philoxeroides in our study strongly supports the adaptive growth hypothesis (AGH), which is that maintaining a high C:N ratio in a low N environment will help invasive plants to improve their nutrient utilization efficiency and prioritize survival, while maintaining a low C:N ratio in a high N environment will enable invasive plants to obtain more resources and achieve rapid growth (Sun et al., 2020; Zhang et al., 2020b; Geng et al., 2023). However, a high N content in plants will increase their palatability and thus their susceptibility to herbivores by changing the interactions with high-trophic-level organisms; this might weaken the defensive ability of A. philoxeroides to resist insect feeding compared to O. articulata in their symbiotic communities (Lu et al., 2015; Liu et al., 2018; Waterton et al., 2022).

NBI, the chlorophyll/flavonoid ratio of plants, is an important indicator for evaluating plant growth (Ilyas et al., 2022). In this study, nitrogen addition led to an increase in NBI, which increased the chlorophyll content of the plants and benefitted their absorption and transformation of light energy, thus enhancing their growth (Deng et al., 2019). Flavonoids are secondary polyphenolic metabolites that exist widely in plants and have strong antibacterial, insect-resistant, and free radical scavenging activity, which can significantly increase the stress resistance and defense ability of plants (Agati et al., 2012; Cesco et al., 2012). Flav is usually used as an important indicator for evaluating the level of plant chemical defense (Agati et al., 2012; Landi et al., 2015). Nitrogen addition significantly decreased the Flav of O. articulata, possibly because the vegetative growth of O. articulata prioritizes its secondary metabolism to obtain more resources when growing in high-nutrient environment, that is, it reduces its chemical defense ability but enhances its growth to resist A. philoxeroides invasion in high-N soil. This also supports the growth-differentiation balance hypothesis (GDBH) regarding plant defense (Liu et al., 2022). In addition, significantly increased rates of plant growth and development and protein synthesis will also inhibit the secondary metabolic pathway of phenylalanine and thus reduce flavonoid synthesis (Zaghdoud et al., 2016; Liu et al., 2021b).

Anthocyanin, a water-soluble glycoside derivative that is widely distributed in plants, plays a crucial role in plants’ resistance to exogenous abiotic stresses (e.g., ultraviolet radiation) and biotic stresses (e.g., insect feeding and interspecific competition) (Gonzalez-Teuber et al., 2017). Landi et al. (2015) found that nitrogen addition can significantly increase the content of anthocyanins, which will absorb excess light energy and dissipate it in the form of heat energy, thus protecting the photosynthetic membrane of plants. In this study, we also found that nitrogen addition significantly increased the Anth of O. articulata, indicating that this alien species could synthesize a large amount of anthocyanins in an N-enriched environment to increase its environmental tolerance, thereby effectively responding to the interspecific competition caused by A. philoxeroides invasion (Zhang et al., 2017). In addition, nitrogen addition caused a significant trade-off between the Flav and Anth of O. articulata, indicating that soil nitrogen enrichment can enhance the physiological plasticity of alien plants and thus increase their competitiveness (Wu et al., 2023). However, nitrogen addition did not have a significant effect on the Flav and Anth of A. philoxeroides in our study, which might be due to its high internal eco-stoichiometric stability (Sun et al., 2019), and this may help A. philoxeroides rapidly evolve suitable growth strategies in environments with different nutrient levels (Geng et al., 2023). Furthermore, global climate changes have exacerbated the escape of A. philoxeroides from the bio-control of its natural enemy Agasicles hygrophila, and it can thus utilize the resources it originally used to resist natural enemies to eliminate the interference of soil N fluctuations on its growth (Lu et al., 2015; Wu et al., 2016).

Chlorophyll fluorescence imaging can comprehensively reflect the primary reaction processes of photosynthesis in plants, such as light energy absorption, excitation energy transfer, and photochemical reactions (Dong et al., 2019). Previous studies showed that applying appropriate amounts of N can increase the chlorophyll content and promote photosynthesis, while N stress (including its concentration and morphology) will lead to a decline in photosynthesis (Chen et al., 2023). In addition, different plants have different levels of energy consumption in the process of absorbing, transporting, and assimilating N, which might lead to excess light energy and accumulation of reactive oxygen (ROS) and thus damage the photosynthetic electron transport chain (Landi et al., 2015; Wang et al., 2019b). F₀ and F_m represent the fluorescence yield when the PS II reaction center of plants is fully opened and closed, respectively, and they characterize the relationship between the plant’s physiological status and habitat (Noor et al., 2022). We found that nitrogen addition decreased both F₀ and F_m of A. philoxeroides in mixed cultures, and significantly weakened the advantage of F₀ and F_m of A. philoxeroides over O. articulata compared with the control, indicating that nitrogen addition reduced the light absorption capacity of A. philoxeroides in interspecific competition. This might be due to the high soil N inhibiting the electron transfer of the plant’s PS II reaction center (Cesco et al., 2012), whereas the PS II reaction center of O. articulata might be more sensitive to irritation, and can effectively respond to high soil N stress by increasing the anthocyanin content to absorb the excess energy that is dissipated in the form of heat and fluorescence under nitrogen addition (Landi et al., 2015).

QY_max represents the maximum potential photochemical quantum efficiency and utilization efficiency of the PS II reaction center, and is an important indicator for evaluating the effect of environmental stress on photosynthesis, while QY_Lss represents the light harvesting ability of plants, which reflects the actual photochemical efficiency of chloroplasts (Fei et al., 2019; Zhang et al., 2021). In our study, nitrogen addition significantly decreased both the QY_max and QY-Lss of plants compared with control, indicating that high soil N weakened the potential vitality of leaves and the electron transfer chain was interrupted due to decreased PS II activity, and the site of injury may be located at the PS II reaction center or primary electron receptor (Singh et al., 2017). qP_Lss represents the portion of light energy absorbed by the PSII reaction center that is actually used for photochemical electron transfer, which reflects the level of plant photosynthetic activity, and Rfd_Lss is used to evaluate the resistance of plants under environmental stress (Kramer et al., 2004). Nitrogen addition did not affect the qP_Lss and Rfd_Lss of O. articulata and A. philoxeroides, indicating that alien plants might have a more stable photosynthetic regulation strategy than native plants under soil nutrient fluctuations (Qing et al., 2012).

We found that nitrogen addition significantly increased the maximum stem length, root area, and leaf area of both A. philoxeroides and O. articulata, which was benefitical for enhancing their competitiveness. Nitrogen addition alleviated the nitrogen limitation in soil, leading to increased root length of A. philoxeroides but decreased root length of O. articulata in mixed cultures; however, O. articulata met the demand for nutrients and water by expanding its root area. Nitrogen addition significantly increased the total N content but decreased the C:N ratio of A. philoxeroides. Nitrogen addition significantly decreased Flav but increased Anth of O. articulata in mixed cultures. Nitrogen addition significantly decreased both F₀ and F_m in mixed cultures, which relatively the increased photosynthetic efficiency of O. articulata. These results indicate that nitrogen addition significantly affects the nutrient absorption and competition patterns of A. philoxeroides vs. O. articulata, in high soil N environment, A. philoxeroides achieves higher nitrogen enrichment capacity by increasing its root length and rapid growth by reducing its C:N ratio, while O. articulata has higher biomass accumulation and root/shoot ratios, and nitrogen addition relatively increased its root area and photosynthetic fluorescence. Moreover, nitrogen addition also promoted the physiological plasticity in the Flav–Anth trade-off for O. articulata. Therefore, under intensified global nitrogen deposition, the biotic resistance of O. articulata to A. philoxeroides invasion might be further enhanced.

The original contributions presented in the study are included in the article/supplementary material. Further inquiries can be directed to the corresponding authors.

HW and BR: conceptualization. HW and SD: methodology and formal analysis. SD, LW, YZ, and SJ: investigation and data curation. HW and SD: writing—original draft preparation and writing—review and editing. HW and BR: funding acquisition. All authors contributed to the article and approved the submitted version.