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Article

The Specific Impacts of Allelopathy and Resource Competition from Artemisia frigida on the Growth of Three Plant Species in Northern China

by
Qing Wang
1,2,
Mengqiao Kong
1,
Junwen Wang
1,
Bin Gao
1 and
Xiaoyan Ping
1,*
1
School of Grassland Science, Beijing Forestry University, No. 35 Qinghua East Road, Haidian District, Beijing 100083, China
2
College of Grassland Science and Technology, China Agricultural University, No. 2 Yuanmingyuan West Road, Haidian District, Beijing 100193, China
*
Author to whom correspondence should be addressed.
Plants 2024, 13(23), 3286; https://doi.org/10.3390/plants13233286
Submission received: 1 October 2024 / Revised: 30 October 2024 / Accepted: 20 November 2024 / Published: 22 November 2024
(This article belongs to the Special Issue Plant Chemical Ecology)
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Abstract

:
Plant interference is a key factor influencing plant coexistence and species composition. The two primary forms of plant interference—allelopathy and resource competition—are often difficult to separate. This study conducted an outdoor pot experiment to quantify the distinct contributions of resource competition and allelopathy of Artemisia frigida on seedling growth of three species: Leymus chinensis, Cleistogenes squarrosa, and Potentilla acaulis. The index of relative neighbor effect (RNE) was used to quantify the overall effect of plant interference, while the inhibition rates (IRs) of resource competition and allelopathy were utilized to determine the specific contributions of allelopathy and resource competition from A. frigida on the growth of target plant species. The interference effect of A. frigida was found to be species-specific. The allelopathic effect of A. frigida played a major role in inhibiting the belowground biomass of L. chinensis (23.97%) and C. squarrosa (58.27%), while allelopathy and resource competition from A. frigida promoted the belowground biomass (45.12%) and aboveground biomass (46.63%) of P. acaulis, respectively. The combined effect of allelopathy and resource competition from A. frigida significantly affected the aboveground biomass of C. squarrosa and P. acaulis, as well as the belowground biomass of L. chinensis and C. squarrosa. These findings contribute to a better understanding of the patterns and mechanisms of plant species composition and its relationship with grazing intensity in this grassland ecosystem.

1. Introduction

Plant interference is a central driver for plant coexistence [1]. The negative interspecific interaction can be attributed to resource competition (competing for water, nutrients, light, or space) or allelopathy (chemical interactions among species) [2,3,4]. Allelopathy can alter the dynamics of resource competition by influencing the growth of recipient species [5,6], while the intensity of resource competition can also affect the release of allelochemicals [7,8]. Traditionally, resource competition has been considered the primary driver of plant community diversity and dynamics [9]. However, other researchers have found that allelopathy can significantly influence plant community composition and succession, potentially playing a role as crucial as resource competition [4,10,11].
Numerous studies have been conducted to distinguish between the two types of plant interference [7,8,12]. For example, PVC tubes have been employed to mitigate both aboveground and root competition between two species, while activated carbon (AC) has been utilized to absorb and eliminate allelochemicals leached by donor plants [12,13,14]. Partial least squares regression or glasshouse experiments have been employed to ascertain the relative contribution of resource competition and allelopathy on the growth of winter cereals and rice [15,16]. Density-dependent experiments have been conducted to quantify the relative contributions of allelopathy and competition to overall interference [2,3,17], while some research has focused on the impact of competition and allopathy on community composition in coastal and inland ecosystems [18]. However, nature is inherently complex, where allelopathy and resource competition often coexist and interact closely [19,20]. The specific contribution of these two types of plant interference remains unknown.
Grasslands constitute approximately 40% of the global land area, offering a plethora of benefits to over 1 billion people worldwide [21]. The most prevalent and significant use of grasslands is for livestock grazing [22,23]. Extensive research has shown that plant species composition varies considerably along grazing gradients [24,25]. Artemisia frigida Willd. (Prairie Sagebrush) is a resilient perennial semi-shrub found throughout the Eurasian Steppe. It exhibits remarkable resistance to drought, grazing, trampling, and regeneration and can be used as high-quality forage, especially in spring and winter [22,23,25]. Meanwhile, Artemisia frigida is the dominant species under moderate and heavy grazing intensities in temperate grasslands of northern China [22]. Conversely, Leymus chinensis prevails in the eastern Eurasian Steppe, while Cleistogenes squarrosa and Potentilla acaulis are the dominant species under light and extreme grazing intensities, respectively [25]. Cleistogenes squarrosa is a C4 perennial bunchgrass noted for its robust drought tolerance, whereas P. acaulis is a perennial stoloniferous herb known for its pronounced allelopathy [22,24]. Both A. frigida and P. acaulis exhibit allelopathic effect, and the aqueous extracts from these two species and the volatile organic compounds (VOCs) from A. frigida markedly inhibit the growth of C. squarrosa and L. chinensis [22,25,26]. The ecological adaptation of A. frigida to prolonged continuous grazing can be attributed to its strong phenotypic plasticity [27], altered carbon allocation patterns [28], intense interspecific competitiveness [24], and allelopathy [22,25,29,30].
To assess the distinct impact of resource competition and allelopathy of A. frigida on the growth of common species within the Eurasian Steppe, we initiated an outdoor pot experiment in northern China. We hypothesized that the plant interference of A. frigida would exhibit species-specific variation among different plant species. Our study sought to address the following question: How does the interference from A. frigida differ across various target plant species, and how is this interference influenced by grazing intensity and specific plant species?

2. Results

2.1. Interference Between A. frigida and Three Target Plant Species

For the interference of A. frigida with three target plant species (AF-LC, AF-CS, and AF-PA in Table 1), A. frigida inhibited both the aboveground (LC 0.28, CS 0.45) and belowground biomass (LC 0.15, CS 0.64) of L. chinensis and C. squarrosa but promoted the root/shoot ratio (−0.16) of L. chinensis. Concurrently, A. frigida enhanced the aboveground biomass (−0.08), belowground biomass (−0.67), and root/shoot ratio (−0.64) of P. acaulis. The index of relative neighbor effect (RNE) of the aboveground biomass, belowground biomass, and root/shoot ratio were all significantly different among the three target species (aboveground biomass: df = 8, F = 19.875, P = 0.002; belowground biomass: df = 8, F = 535.398, P < 0.001; root/shoot ration: df = 8, F = 59.108, P < 0.001). Notably, the growth inhibitory effect of A. frigida on C. squarrosa was stronger, especially in terms of belowground biomass and root/shoot ratio, when compared to L. chinensis.
As for the interference of three target plant species with A. frigida (LC-AF, CS-AF and PA-AF in Table 1), in addition to the inhibitory effect of P. acaulis on the aboveground biomass (0.30) of A. frigida, the other two target plant species all promoted the aboveground biomass (LC −0.27, CS −0.64) and belowground biomass (LC −0.40, CS −0.52) of A. frigida. Meanwhile, the promoting effects of C. squarrosa on the aboveground and belowground biomass of A. frigida were both significantly greater than that of L. chinensis (df = 5, F = 136.862, P = 0.001 and df = 5, F = 18.752, P = 0.012).

2.2. Specific Contributions of Allelopathy and Resource Competition from A. frigida to the Growth of Three Target Species

For L. chinensis, allelopathy of A. frigida played a predominant role in plant interference, particularly affecting the belowground biomass (Figure 1). The resource competition from A. frigida led to a decrease in the aboveground biomass by 1.16% but increased the belowground biomass by 17.42%. Furthermore, the allelopathy of A. frigida resulted in a reduction of the belowground biomass by 23.97% yet augmented the aboveground biomass by 6.13%.
For C. squarrosa, the allelopathy exhibited by A. frigida played a major role in affecting its aboveground and belowground biomass. Specifically, resource competition initiated by A. frigida resulted in a 22.67% increase in the aboveground biomass while simultaneously causing a 30.88% decrease in the belowground biomass. Conversely, the allelopathy of A. frigida resulted in a reduction in the aboveground biomass by 48.68% and the belowground biomass by 58.27%.
As for P. acaulis, both the aboveground and belowground biomass was affected by the resource competition from A. frigida. This competition led to a 46.63% increase in the aboveground biomass and a 27.62% decrease in the belowground biomass. Additionally, the allelopathy of A. frigida contributed to a 1.27% increase in the aboveground biomass and a 45.12% increase in the belowground biomass of P. acaulis.

2.3. Effects of Allelopathy and Resource Competition and Their Coupling Effect on the Plant Growth of Three Target Species

The allelopathic effect (AE vs. CK) of A. frigida significantly reduced the belowground biomass of L. chinensis (df = 17, F = 17.319, P < 0.001), while resource competition (RC vs. AC added) did not have a significant impact (Figure 2(a1,b1)). Neither factor significantly affected the aboveground biomass of L. chinensis (Figure 2(a1)). The combined effect of allelopathy and resource competition of A. frigida did not significantly influence either the aboveground or belowground biomass of L. chinensis (AE + RC vs. CK). However, the addition of activated carbon significantly inhibited the aboveground (df = 5, F = 18.572, P = 0.013) and belowground biomass (df = 5, F = 170.763, P < 0.001) of L. chinensis (AC added vs. CK).
The allelopathic effects of A. frigida significantly reduced both the aboveground (df = 17, F = 7.083, P = 0.003) and belowground biomass (df = 17, F = 6.529, P = 0.004) of C. squarrosa (Figure 2(a2,b2)). Conversely, resource competition from A. frigida did not have a significant effect on either the aboveground or belowground biomass of C. squarrosa. However, when considering the combined effects of allelopathy and resource competition from A. frigida, there was a significant inhibition observed in both the aboveground (df = 5, F = 30.536, P = 0.005) and belowground biomass (df = 5, F = 11.170, P = 0.029) of C. squarrosa. Furthermore, the introduction of activated carbon led to a significant reduction in the aboveground (df = 5, F = 134.602, P < 0.001) and belowground biomass (df = 5, F = 8.114, P = 0.046) of C. squarrosa.
The allelopathic effects of A. frigida did not significantly affect the aboveground and belowground biomass of P. acaulis (Figure 2(a3,b3)). However, resource competition from A. frigida significantly enhanced the aboveground biomass of P. acaulis (df = 17, F = 5.870, P = 0.006). The combined effect of allelopathy and resource competition from A. frigida significantly increased the belowground biomass of P. acaulis (df = 17, F = 10.162, P = 0.001) (Figure 2(b3)). The addition of activated carbon significantly increased the belowground biomass of P. acaulis (df = 5, F = 45.518, P = 0.003).
Our study found that, compared to monocultured L. chinensis and C. squarrosa, the interference of A. frigida inhibited the plant growth of these species (LC 0.22, CS 0.55). Conversely, the interference of A. frigida promoted the growth of P. acaulis compared to its monoculture condition (−0.38). However, the interference from L. chinensis, C. squarrosa, and P. acaulis all had a positive effect on the growth of A. frigida (LC −0.34, CS −0.58, PA −0.14) (Figure 3).

3. Discussion

3.1. Interference of A. frigida with Three Target Plant Species

Our results support our hypothesis that the interference of A. frigida was species-specific. However, this study only examined the pairwise interference of A. frigida on three target plant species, leaving the specific interference of L. chinensis, C. squarrosa and P. acaulis to each other unexplained (Figure 3). The impact of interference on phenotypic plasticity can have more profound effects on species composition than above- and belowground biomass. For instance, the inhibitory effect of Plantago lanceolate on the root growth of Festuca rubra could diminish the competitive strength of F. rubra against other species within the community [31]. Similarly, the inhibitory effect of P. acaulis on the plant growth of A. frigida may alter the interference of A. frigida with other plant species at the study site (Figure 3). Therefore, to gain a comprehensive understanding of the role of plant interference on species composition, it is necessary to consider not only pairwise interactions but also the interaction chain among coexisting plant species in future research.
The interaction between two species may be conditional, depending on environmental conditions, and herbivory may also change the balance of interference among species [32]. In a multispecies community, the species interactions are the sum of all intraspecific and interspecific interactions. Moreover, the interference among species is important in shaping community dynamics and maintaining biodiversity [33]. Concurrently, plant interference may also be influenced by plant–soil feedbacks (PSFs), which can promote the growth of neighboring species in heterogeneous environments [34]. Furthermore, competition among species within the same clades tends to favor dissociation, primarily due to asymmetrical competition within the community [35]. Species with high interspecific competition ability along with grazing intensity would result in asymmetric competition. Highly dominated communities are often characterized by strongly asymmetric competition [36]. Our findings indicate that A. frigida and P. acaulis possess a relatively high degree of interspecific competition ability in comparison to L. chinensis and C. squarrosa (Figure 3). This asymmetrical competition could potentially lead to the dominance of A. frigida and P. acaulis under conditions of heavy and extreme grazing.

3.2. Separation of Allelopathy and Resource Competition from Plant Interference

Consistent with prior research, our findings validated that the plant interference of A. frigida was a synergistic effect of resource competition and allelopathy [17]. Furthermore, we established that the combined effect of allelopathy and resource competition significantly impacted plant–plant interference, with the primary type and intensity of interference from A. frigida varying among different plant species. The allelopathic effect of A. frigida became important for L. chinensis and C. squarrosa under conditions of no grazing and light grazing intensity (Figure 2). Meanwhile, both the allelopathy and resource competition of A. frigida facilitated the dominance of P. acaulis under extreme grazing intensity. Therefore, this study provides a partial explanation for the mechanism of community succession in temperate grasslands along grazing gradients.
Several methods have been developed to distinguish resource competition from allelopathy [8,19,37]. However, most prior research has overlooked the combined effect of allelopathy and resource competition [38]. This study addresses two significant limitations in allelopathy research. Firstly, we implemented a field control experiment, enhancing the credibility of our results compared to those derived from greenhouse experiments. Secondly, this study not only isolates the allelopathic effects of A. frigida from resource competition but also examines the interactive effect of resource competition and allelopathy of A. frigida on the plant growth of three target plant species.
The application of activated carbon (AC) has been widely utilized in allelopathy studies to adsorb allelochemicals and mitigate soil toxicity caused by these compounds. This method effectively separates the effects of allelopathy from resource competition [39,40]. However, the use of AC can introduce controversy due to potential side effects such as altering soil nutrient availability and plant growth [40] and affecting soil microbial activity [41]. Our study confirmed that the addition of AC can influence the plant growth of target plant species, although the specific effects varied among the three target plant species (Figure 2). In contrast to the inhibitory effect of AC on the plant growth of L. chinensis and C. squarrosa (Figure 2), the addition of AC significantly promoted the plant growth of P. acaulis (Figure 2). This discrepancy could be attributed to the fact that AC may also absorb the allelochemicals released by P. acaulis itself, which has been shown to have strong allopathic effects on the seed germination of L. chinensis and A. frigida [26]. Additionally, we used AC added to L. chinensis, C. squarrosa, and P. acaulis as controls to assess the impact of resource competition on the plant growth of three target plant species. By incorporating controls for the effect of AC in our experimental design, our results provide a clearer reflection of the relative contributions of allelopathic interference and resource competition to plant growth.

3.3. The Impact of Allelopathy and Resource Competition and Their Coupling Effects on the Dominant Status of A. frigida in Moderate Grazing Grassland

Our findings corroborate previous research indicating that allelopathy can vary among target plant species, either stimulating or inhibiting growth [42]. For instance, the aboveground biomass of L. chinensis was marginally enhanced by the allelopathy of A. frigida, while the belowground biomass was significantly suppressed [43,44]. In this study, C. squarrosa demonstrated a higher sensitivity to allelopathy of A. frigida than L. chinensis, contradicting previous results [22]. This discrepancy may be attributed to C. squarrosa’s adaptability to environments with lower precipitation levels; thus, its interference in the community is likely to increase under conditions of aridity induced by livestock grazing [45]. The heavy rainfall during the latter stages of our experiment may have heightened C. squarrosa’s sensitivity to both the allelopathy and resource competition of A. frigida. Additionally, the belowground biomass was more significantly affected by the allelopathy of A. frigida, aligning with previous findings in northern China [22].
Allelopathy, whereby the growth of neighboring plants is inhibited by donor plants, can simultaneously enhance their resource competitiveness [4]. This form of intransitive competition can lead to changes in plant species composition [33]. Our study found that the combined effect of allelopathy and resource competition significantly influenced the aboveground biomass of P. acaulis and the above- and belowground biomass of C. squarrosa (Figure 2). However, we were unable to precisely quantify the contribution of this coupling effect. Our results indicated that the coupling effect varied substantially among the three target plant species. It could increase the above- and belowground biomass of L. chinensis and C. squarrosa and the belowground biomass of P. acaulis, and it could also decrease the aboveground biomass of P. acaulis. Therefore, the coupling effect of allelopathy and resource competition could either offset or amplify the actual effect, playing an important role in regulating species composition at the study site [14].
Allelopathy can facilitate the dominance of specific plants within a community, especially for alien plants [6]. Additionally, allelopathy has been identified as a key factor driving grassland succession in northern China [22,44] and forest dynamics in Mediterranean and southern China [11,46]. Resource competition is widely recognized as one of the most significant mechanisms of plant interference in shaping species composition. Concurrently, previous research has indicated that the competition among plant species in the absence of herbivores transitions to facilitation in heavily grazed pastures [47]. In stressful habitats, positive neighbor effects become increasingly important for plant interference [48], a phenomenon that may also be reflected in our study. Along with grazing gradients, the high intensity of trampling and feeding imposed by livestock can cause mechanical damage to plants of A. frigida and increase the release of allelochemicals [49]. A prior study revealed that grazing intensity could influence the components and concentrations of allelochemicals released by A. frigida, with the maximum relative contents of 1,8-cineole and β-terpineol both occurring under heavy grazing intensity [25]. These high concentrations of allelochemicals had a strong inhibitory effect on the plant growth of C. squarrosa and a promotional effect on the plant growth of P. acaulis. However, we did not take into account the concentration of allelochemicals, particularly the VOCs released by A. frigida, throughout the entire experiment, which should be considered in future research.

4. Materials and Methods

4.1. Study Site

This study was conducted at the Hulunbuir field observation experimental station (48°55′48″ N, 119°41′26″ E, altitude 636 m) of the Chinese Academy of Environmental Sciences in Temo Huzhu, situated in the Ewenki Autonomous Banner of Hulunbuir city, China. The study site is characterized by a mid-temperate continental monsoon climate, with an annual average temperature of −2.4 to 2.2 °C and an annual average precipitation from 330 to 350 mm (mainly occurring from June to August). The grassland at the study site is part of the Eurasian Steppe, and the soil is classified as calcic chestnuts, equivalent to Kastanozems according to the soil classification system of the Food and Agriculture Organization (FAO). In the absence of grazing, L. chinensis and Stipa baicalensis are the dominant species, while Agropyron mongolicum, Achnatherum sibiricum, and Carex duriuscula are common species in the study site.

4.2. Experimental Design

An outdoor pot experiment was carried out at the study site to distinguish the specific contribution of resource competition and allelopathy of A. frigida on the seedling growth of three target species. Artemisia frigida (AF) was utilized as the donor plant, while L. chinensis (LC), C. squarrosa (CS), and P. acaulis (PA) were selected as the recipient plants. The proportion of dry matter for each of the four species within the community is detailed in Table 2.
In our pot experiment, we utilized seedlings from four plant species, all of which were collected from the same location within the study site. Seedlings of four plant species were gathered at the stem elongation stage, as defined by the BBCH scale. To ensure homogeneous growth conditions, we selected seedlings of average size, with a coefficient of variation (CV) in plant height of less than 10% for each species. We took measures to enhance the survival rate of the seedlings by preserving the integrity of their roots during excavation. Each pot was initially watered with 500 mL, and no further irrigation was provided throughout the experiment. To maintain soil consistency across the pots, we extracted 0–30 cm topsoil from the sample plot where the plants were originally collected. This soil was then sieved, meticulously mixed, and purged of any impurities. Each pot contained six seedlings: either three from both donor and recipient plants or exclusively six from recipient plants. The pots used had a capacity of 2 gallons and dimensions of 0.24 m × 0.22 m (diameter × height). We established three biological replicates for each treatment.
The experimental design is illustrated in Figure 4. Our field control experiment incorporated five treatments: allelopathy of AF(AE), resource competition of AF(RC), neither allelopathy nor resource competition of AF (No AE or RC), both allelopathy and resource competition of AF (AE + RC), and the addition of activated carbon (AC added). The allelopathic effect of A. frigida was neutralized by introducing activated carbon, a method frequently employed in previous studies (represented by black-dotted pots in Figure 4) [12,13,19]. We used analytical-grade activated carbon (charcoal-activated powder extra pure, Zhejiang Minxin Ecological Technology Company, Quzhou, China), added at a concentration of 20 mL/L according to Parepa et al. [50]. The activated carbon was divided into two portions: one was mixed into the soil to absorb allelochemicals released by the roots of A. frigida, while the other was placed on the pot surface to absorb VOCs emitted by A. frigida.
Resource competition was eliminated by introducing a PVC plastic sheet into the center of the pot (gray-shaded pots in Figure 4) [34]. Three individuals from each species were planted into a pot, with each species situated on opposite sides of the plastic sheet. The sheet was affixed to the sides of each pot, ensuring that each side had equal resources and space for plant growth. We conducted a standard partition study where both roots and shoots of each species were physically separated. The impact of activated carbon on seedling growth of the three target plant species was assessed by incorporating activated carbon into the pots under monoculture conditions (white spotted pots in Figure 4). The entire experiment spanned over 2 months, from June 2019 to September 2019. All 72 pots were placed outdoors throughout the experimental period.

4.3. Measurements

Biomass measurements were conducted at the end of the experiment. Seedlings were divided into aboveground and belowground parts by cutting at the root collar’s apex. Roots were thoroughly washed, and both aboveground and belowground samples were all oven-dried (65 °C) for a minimum of 48 h before being weighed. We also evaluated the soil nutrient contents used for the field control experiment, and the soil description of the study site is present in Supplementary Table S1.

4.4. Data Analysis

The index of relative neighbor effect (RNE) was used to quantify the interference between A. frigida and the three target plant species, as it can overcome skewed distribution and facilitate statistical analysis compared to the commonly used index of relative competitive intensity (RCI) [51,52]:
RNE = (Pmono − Pmix)/Pmax
where Pmono and Pmix represent the performance of four plant species under monoculture and mixed culture conditions, respectively. The maximum value between Pmono and Pmix is denoted as Pmax. For this research, we utilized aboveground biomass, belowground biomass, and root/shoot ratio as performance parameters. The RNE value ranged from −1 to 1, where positive and negative RNE values signify competitive and facilitatory effects, respectively.
Meanwhile, the index of inhibitory rate (IR) was used to distinguish the specific impacts of resource competition and allelopathy from A. frigida on the three target plant species:
IR = (1 − T/C) × 100%
where T represents the performance of four plant species under polyculture conditions, while C represents the performance of four plant species under monoculture conditions. The positive and negative values of IR indicate inhibitory and facilitatory effects, respectively.
We calculated the indices of IR separately for resource competition and allelopathy, noting that the values of T and C differed between resource competition and allelopathy. To calculate the indices of IR under resource competition for A. frigida, T represents the performance of the recipient species in polyculture conditions, influenced solely by interspecific competition, with allelopathy eliminated by the addition of activated carbon (RC). Conversely, C represents the performance of the recipient species in monoculture conditions with the inclusion of activated carbon (AC added), ensuring that the effect of activated carbon on plant growth was counterbalanced [40].
As for calculating the indices of IR under allelopathy of A. frigida, T represents the performance of the recipient species in polyculture conditions influenced solely by allelopathy. To eliminate resource competition, a PVC partition was introduced in the center of each pot (AE). Conversely, C denotes the performance of recipient species in monoculture conditions (CK).

4.5. Statistical Analyses

This study tried to ascertain the significance of RNE and IR among target plant species and the significance of plant growth of target plant species among five treatments (AE, RC, AE + RC, No AE or RC, AC added). ANOVA is used for significance, and the LSD is used for grouping when data show significant differences among treatments. All experimental data are reported as the mean ± standard error (SE). A significance level of α = 0.05 was adopted for all analytical determinations. Statistical analyses were performed using R statistical software version 3.6.1 (R Project for Statistical Computing, Auckland, NZ). All the graphs were generated with ggplot2.

5. Conclusions

Overall, our findings indicate that the type and intensity of plant interference significantly vary among different species. The growth of L. chinensis, C. squarrosa, and P. acaulis is primarily affected by resource competition, allelopathy, and the combined effect of allelopathy and resource competition from A. frigida, respectively. The inhibitory effect of A. frigida on L. chinensis and C. squarrosa, coupled with its promotional effect on P. acaulis, could partially elucidate the community succession observed at the study site in relation to grazing gradients. Both inhibitory and facilitation models make a substantial contribution to the process of community succession. Our results may aid in distinguishing the mechanisms involved in plant interference and community succession within grassland under long-term grazing. Future work should focus on mutual interference among L. chinensis, C. squarrosa, and P. acaulis in plant interactions.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/plants13233286/s1, Table S1: Soil description of the study site used for pot experiment.

Author Contributions

Q.W.: Writing-original draft, visualization, data curation, formal analysis, investigation, resources, software; M.K.: Visualization, formal analysis, investigation, software; J.W.: Visualization, data curation, formal analysis, investigation, software; B.G.: Conceptualization, data curation, formal analysis, investigation, methodology, resources; X.P.: Conceptualization, data curation, methodology, supervision, validation, writing—original draft, writing—review & editing, funding acquisition. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by National Natural Science Foundation of China (31700388) and Open bidding for selecting the best candidates for National Forestry and Grassland Administration (202401-06-04).

Data Availability Statement

Data is contained within the article.

Acknowledgments

We thank Xiaofan He for the technical assistance in the preparation of the manuscript. In particular, the authors would like to express their gratitude to three anonymous reviewers for their valuable comments and suggestions, which have significantly contributed to the improvement of our manuscript.

Conflicts of 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.

References

  1. Kong, C.H.; Li, Z.; Li, F.L.; Xia, X.X.; Wang, P. Chemically mediated plant-plant interactions: Allelopathy and allelobiosis. Plants 2024, 13, 626. [Google Scholar] [CrossRef] [PubMed]
  2. Liu, D.L.; An, M.; Johnson, I.R.; Lovett, J.V. Mathematical modelling of allelopathy: IV. Assessment of contributions of competition and allelopathy to interference by barley. Nonlinearity Biol. Toxicol. Med. 2005, 3, 213–224. [Google Scholar] [CrossRef] [PubMed]
  3. San Emeterio, L.; Damgaard, C.; Canals, R.M. Modelling the combined effect of chemical interference and resource competition on the individual growth of two herbaceous populations. Plant Soil 2007, 292, 95–103. [Google Scholar] [CrossRef]
  4. Hierro, J.L.; Callaway, R.M. The ecological importance of allelopathy. Annu. Rev. Ecol. Evol. Syst. 2021, 52, 25–45. [Google Scholar] [CrossRef]
  5. Meiners, S.J.; Kong, C.H.; Ladwig, L.M.; Pisula, N.L.; Lang, K.A. Developing an ecological context for allelopathy. Plant Ecol. 2012, 213, 1221–1227. [Google Scholar] [CrossRef]
  6. Zhang, Z.; Liu, Y.; Yuan, L.; Weber, E.; van Kleunen, M. Effect of allelopathy on plant performance: A meta-analysis. Ecol. Lett. 2021, 24, 348–362. [Google Scholar] [CrossRef]
  7. Inderjit; del Moral, R. Is separating resource competition from allelopathy realistic? Bot. Rev. 1997, 63, 221–230. [Google Scholar] [CrossRef]
  8. He, H.B.; Wang, H.B.; Fang, C.X.; Lin, Z.H.; Yu, Z.M.; Lin, W.X. Separation of allelopathy from resource competition using rice/barnyardgrass mixed-cultures. PLoS ONE 2012, 7, e37201. [Google Scholar] [CrossRef]
  9. Tilman, D. Resource Competition and Community Structure; Princeton University Press: Princeton, NJ, USA, 1982. [Google Scholar]
  10. Mallik, A.U. Allelopathy: Advances, Challenges and Opportunities. In Allelopathy in Sustainable Agriculture and Forestry; Zeng, R.S., Mallik, A.U., Luo, S.M., Eds.; Springer: New York, NY, USA, 2008; pp. 25–38. [Google Scholar]
  11. Fernandez, C.; Monnier, Y.; Santonja, M.; Gallet, C.; Weaton, L.A.; Prevosto, B.; Saunier, A.; Baldy, V.; Bousquet-Melou, A. The impact of competition and allelopathy on the trade-off between plant defense and growth in two contrasting tree species. Front. Plant Sci. 2016, 7, 594. [Google Scholar] [CrossRef]
  12. Qasem, J.R. A new technology separating allelopathy from competition in pot experiments. Int. J. Agric. Sci. Food Technol. 2017, 3, 19–25. [Google Scholar] [CrossRef]
  13. Nilsson, M.C. Separation of allelopathy and resource competition by the boreal dwarf shrub Empetrum hermaphroditum Hagerup. Oecologia 1994, 98, 1–7. [Google Scholar] [CrossRef] [PubMed]
  14. Bieberich, J.; Lauerer, M.; Drachsler, M.; Heinrichs, J.; Müller, S.; Feldhaar, H. Species- and developmental stage-specific effects of allelopathy and competition of invasive Impatiens glandulifera on co-occurring plants. PLoS ONE 2018, 13, e0205843. [Google Scholar] [CrossRef] [PubMed]
  15. Reiss, A.; Fomsgaard, I.S.; Mathiassen, S.K.; Stuart, R.M.; Kudsk, P. Weed suppression by winter cereals: Relative contribution of competition for resources and allelopathy. Chemoecology 2018, 28, 109–121. [Google Scholar] [CrossRef]
  16. Masum, S.M.; Hossain, M.A.; Akamine, H.; Sakagami, J.; Ishii, T.; Nakamura, I.; Asaduzzaman, M.; Bhowmik, P.C. Performance of Bangladesh indigenous rice in a weed infested field and separation of allelopathy from resource competition. Weed Biol. Manag. 2019, 19, 39–50. [Google Scholar] [CrossRef]
  17. Uddin, M.N.; Robinson, R.W. Allelopathy and resource competition: The effects of Phragmites australis invasion in plant communities. Bot. Stud. 2017, 58, 29. [Google Scholar] [CrossRef]
  18. Martines, I.P.; Kojouharov, H.V.; Grover, J.P. A chemostat model of resource competition and allelopathy. Appl. Math Comput. 2009, 215, 573–582. [Google Scholar] [CrossRef]
  19. Liu, C.; Bu, Z.J.; Mallik, A.; Rochefort, L.; Hu, X.F.; Yu, Z. Resource competition and allelopathy in two peat mosses: Implication for niche differentiation. Plant Soil 2020, 446, 229–242. [Google Scholar] [CrossRef]
  20. Mougi, A. Allelopathic adaptation can cause competitive coexistence. Theor. Ecol. 2013, 6, 165–171. [Google Scholar] [CrossRef]
  21. Bai, Y.; Cotrufo, M.F. Grassland soil carbon sequestration: Current understanding, challenges, and solutions. Science 2022, 377, 603–608. [Google Scholar] [CrossRef]
  22. Li, X.F.; Wang, J.; Huang, D.; Wang, L.X.; Wang, K. Allelopathic potential of Artemisia frigida and successional changes of plant communities in the northern China steppe. Plant Soil 2011, 341, 383–398. [Google Scholar] [CrossRef]
  23. Schönbach, P.; Wan, H.; Gierus, M.; Bai, Y.F.; Müller, K.; Lin, L.J.; Susenbeth, A.; Taube, F. Grassland responses to grazing: Effects of grazing intensity and management system in an Inner Mongolian steppe ecosystem. Plant Soil 2011, 340, 103–115. [Google Scholar] [CrossRef]
  24. Gao, Y.Z.; Wang, S.P.; Han, X.G.; Patton, B.D.; Nyren, P.E. Competition between Artemisia frigida and Cleistogenes squarrosa under different clipping intensities in replacement series mixtures at different nitrogen levels. Grass Forage Sci. 2005, 60, 119–127. [Google Scholar] [CrossRef]
  25. Wang, Q.; Zhang, H.; Yang, Q.; Wang, T.M.; Zhang, Z.W.; Liu, J.L.; Shi, M.M.; Ping, X.Y. The impact of grazing intensity on the allelopathic effect of Artemisia frigida in a temperate grassland in northern China. Flora 2022, 288, 152005. [Google Scholar] [CrossRef]
  26. Zhang, Y.; Tang, S.; Liu, K.; Li, X.; Huang, D.; Wang, K. The allelopathic effect of Potentilla acaulis on the changes of plant community in grassland, northern China. Ecol. Res. 2015, 30, 41–47. [Google Scholar] [CrossRef]
  27. Li, J.H.; Li, Z.; Ren, J.Z. Effect of grazing intensity on clonal morphological plasticity and biomass allocation patterns of Artemisia frigida and Potentilla acaulis in the Inner Mongolia steppe. New Zealand J. Agric. Res. 2005, 48, 57–61. [Google Scholar]
  28. Li, F.R.; Zhao, A.F.; Zhou, H.Y.; Zhang, T.H.; Zhao, X. Effects of simulated grazing on growth and persistence of Artemisia frigida in a semiarid sandy rangeland. Grass Forage Sci. 2002, 57, 239–246. [Google Scholar] [CrossRef]
  29. Zhang, R.M.; Zuo, Z.J.; Gao, P.J.; Hou, P.; Wen, G.S.; Gao, Y. Allelopathic effects of VOCs of Artemisia frigida Willd. on the regeneration of pasture grasses in Inner Mongolia. J. Arid Environ. 2012, 87, 212–218. [Google Scholar] [CrossRef]
  30. Zhang, R.; Zhang, W.; Zuo, Z.J.; Li, R.; Wu, J.; Gao, Y. Inhibition effects of volatile organic compounds from Artemisia frigida Willd: On the pasture grass intake by lambs. Small Rumin. Res. 2014, 121, 248–254. [Google Scholar] [CrossRef]
  31. Padilla, F.M.; Mommer, L.; de Caluwe, H.; Smit-Tiekstra, A.E.; Wagemaker, C.A.M.; Ouborg, N.J.; de Kroon, H. Early root overproduction not triggered by nutrients decisive for competitive success belowground. PLoS ONE 2013, 8, e55805. [Google Scholar] [CrossRef]
  32. Callaway, R.M.; Pennings, S.C.; Richards, C.L. Phenotypic plasticity and interactions among plants. Ecology 2003, 84, 1115–1128. [Google Scholar] [CrossRef]
  33. Aschehoug, E.T.; Brooker, R.; Atwater, D.Z.; Maron, J.L.; Callaway, R.M. The mechanisms and consequences of interspecific competition among plants. Annu. Rev. Ecol. Evol. Syst. 2016, 47, 263–281. [Google Scholar] [CrossRef]
  34. Wang, S.; Callaway, R.M. Plasticity in response to plant-plant interactions and water availability. Ecology 2021, 102, e03361. [Google Scholar] [CrossRef] [PubMed]
  35. Freckleton, R.P.; Watkinson, A.R. Asymmetric competition between plant species. Funct. Ecol. 2001, 15, 615–623. [Google Scholar] [CrossRef]
  36. Wang, L.; Delgado-Baquerizo, M.; Wang, D.; Isbell, F.; Liu, J.; Feng, C.; Liu, J.; Zhong, Z.; Zhu, H.; Yuan, X.; et al. Diversifying livestock promotes multidiversity and multifunctionality in managed grasslands. Proc. Natl. Acad. Sci. USA 2019, 116, 6187. [Google Scholar] [CrossRef]
  37. Falquet, B.; Roux, D.; Henriet, L.; Tschuy, F.; Wirth, J. Simple method to separate resource competition from allelopathic root interactions. Allelopath. J. 2014, 34, 227–240. [Google Scholar]
  38. Inderjit, K.M.; Foy, C.L. On the significance of field studies in allelopathy. Weed Technol. 2001, 15, 792–797. [Google Scholar] [CrossRef]
  39. Ridenour, W.M.; Callaway, R.M. The relative importance of allelopathy in interference: The effects of an invasive weed on a native bunchgrass. Oecologia 2001, 126, 444–450. [Google Scholar] [CrossRef]
  40. Lau, J.A.; Puliafico, K.P.; Kopshever, J.A.; Setltzer, H.; Jarvis, E.P.; Schwarzländer, M.; Strauss, S.Y.; Hufbauer, R.A. Inference of allelopathy is complicated by effects of activated carbon on plant growth. New Phytol. 2008, 178, 412–423. [Google Scholar] [CrossRef]
  41. Meynet, P.; Hale, S.E.; Davenport, R.J.; Cornelissen, G.; Breedveld, G.D.; Werner, D. Effect of activated carbon amendment on bacterial community structure and functions in a PAH impacted urban soil. Environ. Sci. Technol. 2012, 46, 5057–5066. [Google Scholar] [CrossRef]
  42. Wu, C.; Chen, Y.; Grenier-Héon, D. Effects of allelopathy and availability of nutrients and water resources on the survival and growth of plant species in a natural Dacrydium forest. Can. J. For. Res. 2021, 52, 100–108. [Google Scholar] [CrossRef]
  43. Ninkovic, V. Volatile communication between barley plants affects biomass allocation. J. Exp. Bot. 2003, 54, 1931–1939. [Google Scholar] [CrossRef] [PubMed]
  44. Zuo, Z.J.; Zhang, R.M.; Gao, P.J.; Wen, G.S.; Gao, Y. Allelopathic effects of Artemisia frigida Willd. on growth of pasture grasses in Inner Mongolia, China. Biochem. Syst. Ecol. 2011, 39, 377–383. [Google Scholar]
  45. Xu, Y.; Hao, Y. A review of ecological research on Cleistogenes squarrosa. Acta Agrestia Sin. 2016, 24, 726–730. (In Chinese) [Google Scholar]
  46. Qin, F.; Liu, S.; Yu, S. Effects of allelopathy and competition for water and nutrients on survival and growth of tree species in Eucalyptus urophylla plantations. For. Ecol. Manag. 2018, 424, 387–395. [Google Scholar] [CrossRef]
  47. Callaway, R.M.; Kikodze, D.; Chiboshvili, M.; Khetsuriani, L. Unpalatable plants protect neighbors from grazing and increase plant community diversity. Ecology 2005, 86, 1856–1862. [Google Scholar] [CrossRef]
  48. Maestre, F.; Bautista, S.; Cortina, J. Positive, negative, and net effects in grass-shrub interactions in Mediterranean semiarid grasslands. Ecology 2003, 84, 3186–3197. [Google Scholar] [CrossRef]
  49. Weston, L.A.; Barney, J.N.; DiTommaso, A. A review of the biology and ecology of three invasive perennials in New York State: Japanese knotweed (Polygonum cuspidatum), mugwort (Artemisia vulgaris) and pale swallow-wort (Vincetoxicum rossicum). Plant Soil 2005, 277, 53–69. [Google Scholar] [CrossRef]
  50. Parepa, M.; Bossdorf, O. Testing for allelopathy in invasive plants: It all depends on the substrate! Biol. Invasions 2016, 18, 2975–2982. [Google Scholar] [CrossRef]
  51. Callaway, R.M.; Brooker, R.W.; Choler, P.; Kikvidze, Z.; Lortie, C.; Michalet, R.; Paolini, L.; Pugnaire, F.; Newingham, B.; Aschehoug, E.T.; et al. Positive interactions among alpine plants increase with stress. Nature 2002, 417, 844–848. [Google Scholar] [CrossRef]
  52. Weigelt, A.; Jolliffe, P. Indices of plant competition. J. Ecol. 2003, 91, 707–720. [Google Scholar] [CrossRef]
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Figure 1. Specific contribution of allelopathy and resource competition from Artemisia frigida to the growth of three target species (LC: Leymus chinensis, AF: Artemisia frigida, CS: Cleistogenes squarrosa, PA: Potentilla acaulis; RC: resource competition; AE: allelopathy; and CK: monoculture. Red font in the figure indicates a growth-inhibiting effect, while blue font indicates a growth-promoting effect. The green arrows in the figure indicate aboveground biomass, and the brown arrows indicate belowground biomass).
Figure 1. Specific contribution of allelopathy and resource competition from Artemisia frigida to the growth of three target species (LC: Leymus chinensis, AF: Artemisia frigida, CS: Cleistogenes squarrosa, PA: Potentilla acaulis; RC: resource competition; AE: allelopathy; and CK: monoculture. Red font in the figure indicates a growth-inhibiting effect, while blue font indicates a growth-promoting effect. The green arrows in the figure indicate aboveground biomass, and the brown arrows indicate belowground biomass).
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Figure 2. Effects of allelopathy and resource competition of Artemisia frigida on the growth of three target plant species (All the data are shown as mean ± SE (n = 3). (a): Effects of allelopathy and resource competition of Artemisia frigida on the aboveground biomass of L. chinensis (a1), C. squarrosa (a2), P. acaulis (a3). (b): Effects of allelopathy and resource competition of Artemisia frigida on the belowground biomass of L. chinensis (b1), C. squarrosa (b2), P. acaulis (b3). CK: monoculture; AE + RC: both allelopathy and resource competition; RC: resource competition; AE: allelopathy of A. frigida; No AE or RC: neither allelopathy nor resource competition of A. frigida; and AC added: activated carbon was added to evaluate the specific impact of activated carbon on plant growth of three target plant species). Different lowercase letters show the significant differences in biomass of the same plant specie between different treatments (P < 0.05).
Figure 2. Effects of allelopathy and resource competition of Artemisia frigida on the growth of three target plant species (All the data are shown as mean ± SE (n = 3). (a): Effects of allelopathy and resource competition of Artemisia frigida on the aboveground biomass of L. chinensis (a1), C. squarrosa (a2), P. acaulis (a3). (b): Effects of allelopathy and resource competition of Artemisia frigida on the belowground biomass of L. chinensis (b1), C. squarrosa (b2), P. acaulis (b3). CK: monoculture; AE + RC: both allelopathy and resource competition; RC: resource competition; AE: allelopathy of A. frigida; No AE or RC: neither allelopathy nor resource competition of A. frigida; and AC added: activated carbon was added to evaluate the specific impact of activated carbon on plant growth of three target plant species). Different lowercase letters show the significant differences in biomass of the same plant specie between different treatments (P < 0.05).
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Figure 3. Interference of Artemisia frigida with the plant growth of three target species (We used the average RNE of aboveground and belowground biomass to represent the interference of A. frigida with three target species (red arrows). Meanwhile, the interference of three target species with A. frigida was also marked in the figure (blue arrows). The blue values signify a promotional effect, while the red values denote an inhibitory effect).
Figure 3. Interference of Artemisia frigida with the plant growth of three target species (We used the average RNE of aboveground and belowground biomass to represent the interference of A. frigida with three target species (red arrows). Meanwhile, the interference of three target species with A. frigida was also marked in the figure (blue arrows). The blue values signify a promotional effect, while the red values denote an inhibitory effect).
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Figure 4. Design of outdoor pot experimental to differentiate between allelopathy and resource competition of Artemisia frigida in a temperate grassland in northern China. The allelopathic effect of A. frigida was eliminated by adding activated carbon to absorb allelochemicals both in the soil and air, represented by black dots on the pots. Resource competition was mitigated by introducing a PVC partition in the center of the pot, depicted as gray-shaded pots in the figure. The four plant species used in this study included LC, Leymus chinensis; CS, Cleistogenes squarrosa; AF, Artemisia frigida; and PA, Potentilla acaulis, representing the dominant species under non-grazing, light grazing, moderate grazing, and extreme grazing intensities at the study site, respectively. The experimental conditions were categorized as follows: AE (allelopathy), RC (resource competition), No AE or RC (neither allelopathy nor resource competition), AE + RC (both allelopathy and resource competition), AC added (activated carbon was added to assess its impact on plant growth), and CK (three target species planted individually).
Figure 4. Design of outdoor pot experimental to differentiate between allelopathy and resource competition of Artemisia frigida in a temperate grassland in northern China. The allelopathic effect of A. frigida was eliminated by adding activated carbon to absorb allelochemicals both in the soil and air, represented by black dots on the pots. Resource competition was mitigated by introducing a PVC partition in the center of the pot, depicted as gray-shaded pots in the figure. The four plant species used in this study included LC, Leymus chinensis; CS, Cleistogenes squarrosa; AF, Artemisia frigida; and PA, Potentilla acaulis, representing the dominant species under non-grazing, light grazing, moderate grazing, and extreme grazing intensities at the study site, respectively. The experimental conditions were categorized as follows: AE (allelopathy), RC (resource competition), No AE or RC (neither allelopathy nor resource competition), AE + RC (both allelopathy and resource competition), AC added (activated carbon was added to assess its impact on plant growth), and CK (three target species planted individually).
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Table 1. Interference between Artemisia frigida and three target plant species at the study site.
Table 1. Interference between Artemisia frigida and three target plant species at the study site.
Indexes of Plant InterferenceRNE
Aboveground BiomassBelowground BiomassRoot/Shoot Ratio
AF-LC0.28 ± 0.10 a0.15 ± 0.04 b−0.16 ± 0.08 b
AF-CS0.45 ± 0.10 a0.64 ± 0.07 a0.30 ± 0.08 a
AF-PA−0.08 ± 0.04 b−0.67 ± 0.01 c−0.64 ± 0.05 c
LC-AF−0.27 ± 0.07 b−0.40 ± 0.07 a−0.18 ± 0.05 b
CS-AF−0.64 ± 0.02 c−0.52 ± 0.04 b0.23 ± 0.09 a
PA-AF0.30 ± 0.06 a−0.59 ± 0.04 b−0.71 ± 0.02 c
Note: Different lowercase letters in the same column indicate significant differences in the RNE among three target plant species. All the data are shown as mean ± SE (n = 3). AF-LC: interference of Artemisia frigida with Leymus chinensis; LC-AF: interference of L. chinensis with A. frigida; AF-CS: interference of A. frigida with Cleistogenes squarrosa; CS-AF: interference of C. squarrosa with A. frigida; AF-PA: interference of A. frigida with Potentilla acaulis; and PA-AF: interference of P. acaulis with A. frigida.
Table 2. The dry matter proportion of four plant species at the study site along with grazing gradients.
Table 2. The dry matter proportion of four plant species at the study site along with grazing gradients.
Plant SpeciesDry Matter Proportion (%)
No GrazingLight Grazing Medium Grazing Extreme Grazing
Leymus chinensis35.34 ± 1.45 a26.32 ± 1.89 b15.53 ± 1.23 c6.12 ± 0.78 d
Cleistogenes squarrosa5.61 ± 0.32 d43.64 ± 3.27 a25.25 ± 2.32 b13.42 ± 1.62 c
Artemisia frigida3.26 ± 0.25 c10.25 ± 1.67 b38.21 ± 2.87 a28.02 ± 2.98 a
Potentilla acaulis0.08 ± 0.03 c2.35 ± 0.08 bc7.30 ± 1.12 b32.75 ± 4.25 a
Note: Different lowercase letters in the same line indicate significant differences in the dry matter proportion of four plan species among four grazing intensities. All the data are shown as mean ± SE (n = 3).
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Wang, Q.; Kong, M.; Wang, J.; Gao, B.; Ping, X. The Specific Impacts of Allelopathy and Resource Competition from Artemisia frigida on the Growth of Three Plant Species in Northern China. Plants 2024, 13, 3286. https://doi.org/10.3390/plants13233286

AMA Style

Wang Q, Kong M, Wang J, Gao B, Ping X. The Specific Impacts of Allelopathy and Resource Competition from Artemisia frigida on the Growth of Three Plant Species in Northern China. Plants. 2024; 13(23):3286. https://doi.org/10.3390/plants13233286

Chicago/Turabian Style

Wang, Qing, Mengqiao Kong, Junwen Wang, Bin Gao, and Xiaoyan Ping. 2024. "The Specific Impacts of Allelopathy and Resource Competition from Artemisia frigida on the Growth of Three Plant Species in Northern China" Plants 13, no. 23: 3286. https://doi.org/10.3390/plants13233286

APA Style

Wang, Q., Kong, M., Wang, J., Gao, B., & Ping, X. (2024). The Specific Impacts of Allelopathy and Resource Competition from Artemisia frigida on the Growth of Three Plant Species in Northern China. Plants, 13(23), 3286. https://doi.org/10.3390/plants13233286

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