Nitrogen, Phosphorus, and Invasive Alien Plants: Comparison
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Plant invasion is significantly affected by environmental factors in the recipient habitats and affects the stability and sustainable development of society. The invasiveness of alien plants may be increased by anthropogenic-mediated disturbances, such as fluctuations in nutrients caused by excessive emissions of nitrogen (N) and phosphorus (P). 

  • plant invasion
  • eutrophication
  • biogeochemical cycle
  • nitrogen
  • phosphorus

1. Introduction

Nitrogen (N) and phosphorus (P) are the most important nutrients for plant growth [1]. In plants, N mainly contributes to the biosynthesis of amino acids, proteins, and other macromolecular bioactive substances and is widely involved in various life activities [2]. Similarly, P plays a critical role in the construction of the nucleic acid structure and energy transformation in plants [3]. Maintaining the stability of the biogeochemical cycle of N and P is therefore of great significance to entire ecosystems. However, anthropogenic-mediated disturbances of N and P can have a major influence on the structure and functioning of ecosystems; for example, excessive emissions of N and P change the element compositions and stoichiometries in regional ecosystems and the relationships between species composition and ecological processes [4][5][6]. At the same time, invasive alien species (IAS) also pose a serious threaten to ecosystems, which may cause disturbances in biogenic element cycles, reduced biodiversity, ecosystem degradation, and even destruction of the original ecosystem [7]. As the second greatest threat to biodiversity after habitat fragmentation, invasive alien plants are not dominant competitors in their natural systems but competitively exclude their new neighbors. For example, Centaurea diffusa, a Eurasian plant, has no impact on 32P uptake by other Eurasian species. However, it significantly decreases the 32P absorption of all North American grass species, due to its root activity and chemically mediated effects. On the other hand, no inhibitive effect was found on 32P uptake of C. diffusa by North American grasses, while all Eurasian species showed a great negative influence on 32P uptake by C. diffusa [8].
The composition of plant communities can be altered by the elemental compositions of their habitats [9]. Eutrophication is broadly considered a serious threat to biodiversity conservation and ecosystem functions. It is closely related to plant invasion and expansion. Thus, plant invasion may be triggered by the nutritional conditions in the recipient environment. Some researchers used molecular techniques to survey the phytogeography of two Phragmites spp., Phragmites australis and Phragmites mauritianus, and found that three haplotypes in these species are native, and both species have high genetic diversity. Meanwhile, there was no evidence of recent non-native haplotype invasion in the native region. Therefore, they suggested that the expansion of these two Phragmites species was most likely led by anthropogenic disturbance in the environment [10].
The competitive performance of invasive alien plants is often habitat dependent [11]. That is to say, resource availability in the habitat is a critical factor determining community susceptibility to alien plant invasion. It also determines the ability of alien plants to invade a particular habitat [12]. Among various factors, the coupling effect of N and P dictates the success of alien species invasion [13]. High N and P contents may promote invasion rather than being a consequence of invasion [14]. There is a positive and synergetic effect of N and P on the invasiveness of opportunistic alien species (Figure 1) [4].
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Figure 1. Spread of Alternanthera philoxeroides Griseb in eutrophic wetland. Photos were taken in a eutrophic pool invaded by A. philoxeroides Griseb next to Huilong reservoir, Zhenjiang City, Jiangsu Province, China (119°45′ E; 32°15′ N) in 2018. These pictures show spread of A. philoxeroides Griseb over 3 months (9 July to 9 October 2018).
Therefore, instead of plant invasions influencing N and P enrichment (Table 1), N and P enrichment may exacerbate plant invasion.
Table 1. Interactions between invasive alien plants and N and P.
Interactions between Invasive Alien Plants and N and P References
Effects of plant invasion on the N and P pool N and P pool in invasive alien plants Higher aboveground N and P accumulation than in native plants [6][15][16][17][18][19]
Larger N investment in photosynthetic production [20][21][22][23]
Decreased N allocation to defend structures [20]
N and P pool in invaded soil Increased NH4+ content in soil [24][25]
Increased total N and P content in soil [6][26][27]
Promotion of N and P mineralization and acceleration of N and P cycles [28][29][30][31][32]
Mechanisms of plant invasion promoted by N and P   High N and P tolerance hypothesis [33]
Growth rate hypothesis [12][13][34][35][36]
Biomass allocation hypothesis [37][38]
Enemy release hypothesis [39][40][41]

2. Interaction Mechanism between N and P and Invasive Alien Plants

2.1. Influence of Invasive Alien Plants on N and P Pool in Soil and Plants

The success of invasion is mainly the result of the soil status or growing environment of invasive alien plants. Reports have suggested that differences in element compositions and stoichiometries in soils are mainly caused by the success of invasive species in invaded regions [42][43][44][45][46][47]. For example, Hu et al. (2019) reported similar results, showing that NH4+ concentration in soil invaded by Chromolaena odorata was 1.43 times that of native soil [24], and the NH4+ concentration of soil invaded by Ageratina adenophora was 1.56–2.10 times that of native soil [25]. Moreover, soil function may also show some alterations at an early stage of invasion [48]. The differences in soil properties and functioning may point toward the contributions of root exudates [49][50][51] and high productivity litter [26] and their associated spatial variability. For example, compared with the outside areas of the crown canopy of invasive alien plants, the physical and chemical properties of soil under the crown canopy of invasive species were found to be significantly different, although it was only a few meters away [6][52]. Similarly, various other conditions can be advantageous to invasive alien plants over native plants in the acquisition of resources.
Invading plants transform pools and fluxes of N and P in the soil by accelerating N and P cycles in the ecosystem (Figure 2) [28][29][30].
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Figure 2. Interaction processes between invasive alien plants and N and P. Eco-mechanisms through which N and P promote plant invasion (left) and how plant invasion intensifies N and P enrichment (right) are shown.

2.2. The Influence of Nutrient Fluctuation Caused by N and P on the Invasiveness of Alien Plants

2.2.1. N and P Mediated Ecological Strategy and Interactions between Native and Invasive Alien Plants

There are differences in plant traits, ecological strategies, and responses to environmental nutrient conditions between invasive and native plants. For example, Dalle Fratte et al. (2019) conducted a study on plant traits in Northern Italy and showed that, due to increased soil N and P loadings in Southern Europe, plant communities are gradually shifting from “slow and conservative” to “fast and acquisitive” species, which may cause invasion by subtropical invasive alien plants and put a strain on biodiversity at the local scale [53]. Previous studies also indicate that invasive alien plants may have different N nutrition strategies compared with native plants. Invasive alien plants such as Bidens pilosa, Microstegium vimineum, and Mikania micrantha prefer to consume nitrate over ammonium [39][42][54]. This “preference” may contribute to its competition with native plants in some nitrate-rich habitats. By contrast, some invasive alien plants are reported to prefer ammonium. The African grass Andropogon gayanus was found to directly alter the understory structure of oligotrophic savannas in tropical Australia, which was attributed to the grass accelerating the ammoniation process and increasing soil ammonium availability to four times that of native plant soil, with a more than six times higher uptake rate of ammonium than native plants [55].

2.2.2. Mechanisms of N and P Promote Alien Plant Invasion

The occurrence of invasion and the growth environment also determine the allocation of resources for the functioning and existence of plants. (1) In a highly N and P polluted environment (e.g., eutrophication), invasive alien plants were found to be more tolerant than most species [33], as they increase N allocation to photosynthetic activity and promote photosynthetic tissue growth. (2) As a response to the growth rate hypothesis, plants demand more rRNA and ribosomes for increased protein synthesis. This requires more phosphorus [13][35] to contribute to higher net primary productivity (NPP) [36], and plants exhibit an increase in overall biomass [12][34]. As shown by Broadbent et al. (2018), under high N conditions, the invasiveness of Agrostis capillaris was significantly increased, and a largely negative impact on native species growth was observed: the biomass of native plants was decreased by half, and total N content in tissues was decreased by up to 75% [27]. Hence, as the fluctuating resource hypothesis describes, those plant communities, which are more sensitive to N and P fluctuations, are more vulnerable to plant invasion [37][38][56]. (3) Additionally, as a response to environmental changes, invasion plant biomass allocation also dictates the changes in N and P levels [40], and this is known as plastic response to difference in resource availability.

2.2.3. Strategies to Control Alien Plant Invasion

With ongoing deposition, N would cease to be a limiting nutrient for primary productivity; however, increased N bioavailability might result in a higher P requirement [57][58][59][60]. The accelerated growth of the tested invasive alien plants was found to be closely related to increased leaf P [57][61]. At the same time, this invasive species could selectively utilize insoluble P (Al-P) by enhancing root biomass in an environment with enriched N. A high N concentration in the soil might mean that the N demands are met for both invasive alien plants and native plants after P addition. However, with an even higher N and P demand than that of invasive species (such as Solidago canadensis), native species growth was promoted under N and P enrichment. More nutrients were allocated aboveground, and the growth of invasive alien plants was inhibited through shading. This is an argument in favor of the resource ratio hypothesis [62][63], which holds that plant distributions are determined by the availability of the resource that is most limiting, and resource demands vary among species, which in turn determines the competition effects. Altering the N and P ratio might be an alternative strategy to decrease invasive species competitiveness [61][62].

3. Conclusions and Prospects

Excessive emissions of N and P induced by human activity can reduce the resistance of native plants to invasive species. Once we understand their relationship more thoroughly, nutrient element management could serve as “chemotherapy” for invaded habitats contaminated with N and P, for instance, by artificially enhancing nutrient stresses (such as N and P) in ways that have negative influence on invasive instead of native species in a community. In most reports, there is mutual promotion between plant invasion and increased N and P. In other words, resource fluctuations resulting from N and P emissions provide more opportunities and competitiveness for the invasion of alien plants. At the same time, the biogeochemical cycles of N and P are promoted because of their efficient and higher utilization and release rates by invasive alien plants. However, there is no consensus on whether the elemental compositions of invasive species are different from those of natives. Quantitative research comparing the N and P contents of plant, litter, and soil element contents between native plants and invaders in a global context is lacking. Thus, we should further investigate the role of N and P biogeochemical behavior in native and invasive species and the soil in plant–soil ecosystems.

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