The Soil pH and Micronutrients Drive  Ageratina Adenophora  Invasion in Areas with Acidic and Nutrient-Poor Soils

doi:10.21203/rs.3.rs-8012262/v1

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The Soil pH and Micronutrients Drive Ageratina Adenophora Invasion in Areas with Acidic and Nutrient-Poor Soils

https://doi.org/10.21203/rs.3.rs-8012262/v1

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Ageratina adenophora poses significant threats to agricultural and forestry production and biodiversity conservation worldwide. However, its expansion mechanism in highly acidic environments has not been studied in depth. To address this issue, we investigated the impacts of A. adenophorainvasion on soil nutrient content and enzyme activity levels across 24 samples from Yunnan Province, China. The sampling sites were categorized into four invasion levels, namely, noninvaded (C), lightly invaded (L), moderately invaded (M), and severely invaded (S). Our findings revealed that the soil pH in severely invaded areas was 8.37% greater than that in noninvaded areas, with pH values ranging from 4.8 to 5.3. Notably, severely invaded soils demonstrated relatively high levels of soil organic carbon (SOC), available potassium (AK), aluminum (Al), available iron (Fe), available zinc (Zn), available copper (Cu), available manganese (Mn), exchangeable calcium (Ca), and exchangeable magnesium (Mg). However, the levels of available Al, boron (B), and phosphorus were significantly lower in these areas. Additionally, variations in the total nitrogen (TN), total potassium (TK), sucrase, and nitrate reductase activity levels were observed across the areas with different invasion levels. Correlation analysis underscored the pivotal role of pH in regulating soil nutrient availability and microbial activity levels. The random forest model (RFM) and structural equation modeling (SEM) results indicated that available Mn, AK, and available Zn are the dominant factors in noninvaded areas (p < 0.05), while Mg, B, and available Cu were the main factors in severely invaded areas (p < 0.05). These findings collectively demonstrate that A. adenophora invasion establishes favorable habitat conditions by altering soil pH, nutrient cycling, and enzyme activity levels, thereby suppressing the growth of native plants and ultimately displacing them from their ecological niches. This study provides a sound foundation for the formulation of stage-specific control strategies against A. adenophora invasion.

Level of invasion

Ageratina adenophora

soil pH

soil nutrients

soil enzyme activity

structural equation model

Invasive alien plants pose a significant threat to global ecological security, with the potential to reduce regional biodiversity and drastically alter the structure and function of natural ecosystems (Yang et al., 2013; Xu et al., 2023). Owing to intensified global climate change and increased international exchanges, the spread of invasive plants continues to increase (Osunkoya and Perrett, 2011; Ren et al., 2021). Such plants compete with native flora for essential resources, including water, light, and soil nutrients (Jones et al., 2019; Puissant et al., 2019; DeForest and Moorhead, 2020). A substantial body of evidence indicates that invasive species can alter microbial community composition and soil enzyme activity through root secretions, litter decomposition, and allelopathy, thus creating nutrient environments favorable for their proliferation (Esch et al., 2017; Ahmad Dar et al., 2023; Guo et al., 2023). Changes in soil environments subsequently enhance the competitive advantage of these species, thereby influencing the dynamics between exotic and native plants (Esch et al., 2017; Ahmad Dar et al., 2023; Guo et al., 2023). The complex feedback relationships between invasive alien plants and soil nutrient cycling continue to attract broad research interest (Gasch et al., 2013; Wu et al., 2020; Kumar et al., 2021).

Ageratina adenophora, a perennial herbaceous or semishrubby plant native to Mexico, is recognized globally as a highly pernicious invasive species (Wu et al., 2020; Kumar et al., 2021). This plant exhibits significant environmental adaptability and has been demonstrated to substantially increase soil fertility after prolonged establishment (Zhao et al., 2019; Zhang et al., 2023). It has been demonstrated that A. adenophora can mitigate unfavorable soil conditions, thereby increasing its uptake of essential nutrients such as carbon (C), nitrogen (N), and phosphorus (P) (Bojórquez-Quintal et al., 2017; Ahmad Dar et al., 2023). This, in turn, accelerates its growth and development (Zhao et al., 2019; Verma et al., 2023). In addition to macronutrients, A. adenophora requires various micronutrients for optimal growth and development of physiological functions. Notably, nutrient deficiency can significantly impair health (Bojórquez-Quintal et al., 2017; Wu et al., 2023). Compared with native flora, invasive species typically exhibit accelerated growth and increased biomass, necessitating greater intake of micronutrients and consequently intensifying the activation or depletion of soil micronutrient pools (Pizzeghello et al., 2011; Wu et al., 2023). For example, invasion by Acacia dealbata and Lantana camara L. significantly increases soil calcium (Ca) and magnesium (Mg) levels while altering the concentrations of iron (Fe), copper (Cu), manganese (Mn), and sulfur (S) (Osunkoya and Perrett, 2011; Pizzeghello et al., 2011; Kaur et al., 2012; Souza-Alonso et al., 2014). These findings suggest that there may occur positive feedback between these two plants and soil micronutrients, in turn facilitating their invasion (Esch et al., 2017; Kim et al., 2018; Puissant et al., 2019). Unfortunately, research on soil micronutrient dynamics during A. adenophora invasion, particularly in nutrient-poor soils, remains scarce (Bursali et al., 2009; Wu et al., 2020; Chen et al., 2022).

The soil pH is closely associated with nutrient biogeochemical processes and availability (Zhao et al., 2019; Xiao et al., 2023). Under acidic soil conditions, salt-based ions such as Zn, Mg, and Ca are readily displaced by acid ions (H⁺ and Al³⁺), resulting in their loss through leaching or precipitation events (Merry et al., 2002; Bojórquez-Quintal et al., 2017). Concurrently, Mo can form iron phosphate precipitates, which results in a reduction in availability (Jones et al., 2019; Wu et al., 2020). High acidity can even lead to aluminum and manganese toxicity issues, which inhibits plant growth. In response to low soil pH values, plants effectively neutralize or buffer soil acidity during growth by promoting ammonification reactions in the soil, thus inhibiting nitrification reactions and regulating organic components within their own tissues. (Xiao et al., 2017; Zhao et al., 2019). Previous studies have indicated that A. adenophora may exhibit a similar ability (Bills et al., 2010; Kim et al., 2018), which becomes increasingly important as invasion deepens or expands over time. For example, Xiao et al. (2017) revealed that pH promoted the colonization of A. adenophora, thus increasing soil fertility, as indicated by elevated organic carbon (C_org), nitrate (NO₃⁻), ammonium (NH₄⁺), available potassium (AK), and available phosphorus (AP) contents. Additionally, Jones et al. (2019) indicated that pH is the main factor regulating the carbon utilization efficiency, and Puissant et al. (2019) reported that pH can affect enzyme activity, which can increase the activities of key soil enzymes such as urease (SUE), phosphatase, and invertase (Zhao et al., 2019). Moreover, Wu et al. (2020) demonstrated that the soil pH and enzyme activity levels were notably greater in areas invaded by A. adenophora than in uninvaded areas (Wu et al., 2020). Nevertheless, the precise manner in which increasing the soil pH contributes to changes in soil nutrient contents to match the increased invasion of A. adenophora remains unclear (DeForest and Moorhead, 2020; Lhamo et al., 2023).

Starting during the 1940s, the range of A. adenophora increased from Burma to Yunnan Province in China, and this invasive plant rapidly proliferated throughout Southwest China. Presently, A. adenophora has emerged as one of the most formidable threats to biodiversity and agricultural production in inland China (Pizzeghello et al., 2011; Fan et al., 2022). Pinus yunnanensis, an endemic tree species in Southwest China, dominates the regional forested landscape. These forests, which mainly encompass homogeneous stands, are characterized by notable soil acidification (with soil pH values typically ranging from 4 to 6) (Merry et al., 2002; Kabała and Łabaz, 2018) underneath the canopy and limited soil nutrient availability, which significantly restricts plant growth (Esch et al., 2017; Darji et al., 2021). Interestingly, over the past two decades, field surveys have identified Pinus yunnanensis forests as primary sites for A. adenophora invasion, and invasive populations continue to expand, posing a serious threat to forest regeneration and subcanopy biodiversity. (Wang et al., 2015; Sun et al., 2021; Zhang et al., 2022). Although a few studies have revealed changes in soil nutrient levels and interspecific associations (Hu et al., 2021; Xiao et al., 2023; Niu et al., 2007; Liu et al., 2023) after A. adenophora invasion into Pinus yunnanensis forests, the nutrient dynamics throughout the spread process have not yet been explored in depth. In our study, we considered different invasion levels of A. adenophora in Pinus yunnanensis forests to explore changes in the levels of major soil nutrients, micronutrients, and enzyme activity. Specifically, we aimed to determine (1) whether the soil pH increases with increasing invasion level; (2) how the contents of major soil micronutrients change with increasing invasion level; and (3) the mechanisms through which changes in soil pH and micronutrient levels may facilitate increased invasion. We aimed to enhance the understanding of the expansion mechanisms of A. adenophora in areas with acidic soil conditions and to provide a theoretical basis for developing preventive and control strategies.

2.1 Study area

The research site is located in Jiyi town, Wuding County, Yunnan Province, Southwest China, at coordinates of 26°6′N and 102°14′E. Jiyi town is situated on the banks of the Jinsha River and exhibits an average elevation of 1900 m (Fig. 1). The study area experiences a dry-hot valley climate characterized by abundant sunshine, high evaporation rates and an average annual temperature of 15.2°C. Precipitation occurs mainly from May to October, with annual totals ranging from 800 to 1000 mm (Wu et al., 2020). Previous studies have identified the soil type at the research site as dry red soil (Chen et al., 2013). Specifically, the sampling site is located in the upper-middle part of a Pinus yunnanensis forest with slope gradients ranging from 25° to 40° and faces northeast. The average height of this forest is approximately 10.5 m, and the average diameter at breast height is approximately 13.5 cm. The canopy density levels range from 0.6 to 0.9 units per unit area (m²). Resident surveys indicate that A. adenophora has been invading the understory of this forest for more than two decades.

2.2 Sampling method

In August 2023, the extent of A. adenophora invasion was quantified by assessing the relative projected area covered by this species with reference to previous studies (Fig. 1). Sample plots were selected randomly and categorized into four invasion levels on the basis of the percentage of the area covered by A. adenophora, namely, noninvaded (C, 0.2%-1.2%), lightly invaded (L, 25%-35%), moderately invaded (M, 50%-70%), and severely invaded (S, 88%-97%) (Table 1) (Xiao et al., 2017; Wu et al., 2020; Zhang et al., 2023). For each invasion level, six plots were established, each measuring 1×1 m, characterized by similar topographic features and canopy closure conditions. The plots were spaced at least 20 m apart to avoid spatial overlap. The plant composition varied according to the invasion level (refer to Table 1 for details).

Table 1
Distribution of plants in the *A. adenophora* sample plots under different invasion levels.
Invasion level	Community overview	Coverage of A. adenophora %
Noninvaded (C)	Pogonatherum crinitum Thunb.; Artemisia lavandulifolia DC.; Grona heterocarpos L.; Scutellaria indica L.; Cynoglossum amabile Stapf & Drummond; Pararuellia delavayana Baill.; Paspalum scrobiculatum Var.; Polygala persicariifolia DC.; Dodonaea viscosa Jacquem.; Origanum vulgare L.; Reinwardtia indica Dumort.	0.68 ± 0.35
Lightly invaded (L)	Ageratina adenophora Spreng.; Artemisia lavandulifolia DC.; Ainsliaea spicata Vaniot, Pogonatherum crinitum Thunb.; Clinopodium megalanthum Diels; Oxalis corniculata L.; Dioscorea subcalva Prain & Burkill	29.83 ± 3.39
Moderately invaded (M)	Ageratina adenophora Spreng.; Elsholtzia rugulosa Hemsl.; Reinwardtia indica Dumort.; Pogonatherum crinitum Thunb.; Grona heterocarpos L.; Pimpinella candolleana Wight & Arn.; Arisaema erubescens Wall.	60 ± 6.51
Severely invaded (S)	Ageratina adenophora Spreng.; Elsholtzia rugulosa Hemsl.; Reinwardtia indica Dumort.; Pogonatherum crinitum Thunb.	92.67 ± 3.04

To assess soil properties, aboveground vegetation and litter were removed in each plot, and five soil samples were collected from the top 20 cm with a soil auger (5-cm diameter) following the five-point sampling method. The samples were thoroughly mixed, transported to the laboratory, and sieved through a 2-mm mesh. The sieved samples were then divided into two portions: one was dried naturally for the analysis of soil physicochemical properties and micronutrient contents, while the other was refrigerated at a temperature of 4°C for two weeks to analyze soil enzyme activity and alkaline dissolved nitrogen levels.

2.3 Soil analysis

Soil physicochemical properties encompass a comprehensive range of parameters, including the soil pH, soil organic carbon (SOC), total nitrogen (TN), total phosphorus (TP), total potassium (TK), available nitrogen (AN), available phosphorus (AP), and AK (Xiao et al., 2017). In addition, the analysis was extended to soil total microelements, such as Fe, Mn, zinc (Zn), Cu, boron (B), Ca, Mg, and aluminum (Al) (Osunkoya and Perrett, 2011; DeForest and Moorhead, 2020), as well as soil available microelements, including available Fe, available Mn, available Zn, available Cu, available B, exchangeable Ca, exchangeable Mg, and available Al (Osunkoya and Perrett, 2011; Fan et al., 2022). Furthermore, the activity of soil enzymes, including SUE, alkaline phosphatase (ALP), sucrase (SSC), nitrate reductase (NR), and catalase (CAT) activities, was evaluated (Kim et al., 2018; Zhang et al., 2022). In this study, macronutrient indices were determined according to the method of Xiao et al. (2017), micronutrient indices were determined according to the methods of Osunkoya and Perrett (2011), DeForest and Moorhead (2020) and Fan et al. (2022), and enzyme activity indices were determined according to the methods of Kim et al. (2018) and Zhang et al. (2022). These parameters collectively provide a robust framework for assessing soil health and nutrient dynamics in the studied ecosystem.

2.4 Data analysis

In this study, the experimental data were systematically analyzed and organized in Microsoft Excel 2021. The normality of the data distribution was evaluated via SPSS 25.0. Graphical representations of the soil pH, SOC, nitrogen (N), phosphorus (P), potassium (K), and enzyme activity data were generated with the ggplot2 package in R version 4.2.2. The soil micronutrient data were analyzed via one-way analysis of variance (ANOVA) using SPSS 25.0. Additionally, correlation analysis, random forest model (RFM) analysis and structural equation modeling (SEM) were performed in R, thereby employing the piecewiseSEM, corrplot, and pacman packages, respectively. In SEM analysis, a P value greater than 0.05 indicated that all path coefficients in the model were less than 1, with lower values of Fisher's exact test statistic, the Akaike information criterion (AIC), and the Bayesian information criterion (BIC) indicating a better model fit (Zhao et al., 2019). This comprehensive analytical approach ensured robust data interpretation and provided a solid foundation for understanding the relationships between soil properties and their influence on the studied ecosystem.

3.1 Effects of different levels of A. adenophora invasion on soil physicochemical properties

As shown in Fig. 2, significant changes (P < 0.05) were observed in the soil pH, TN, TK, and AP levels across the areas with varying degrees of A. adenophora invasion compared with those in noninvaded areas. Specifically, the soil pH increased with increasing invasion level (Fig. 2a), with increases of 1.34%, 3.19%, and 8.37% in lightly, moderately, and severely invaded areas, respectively, relative to those in noninvaded areas. The soil TN content significantly fluctuated (P < 0.05) with increasing invasion level, with a 35.38% increase in lightly invaded areas, a 10.73% decrease in moderately invaded areas, and a 9.59% increase in severely invaded areas (Fig. 2b). Conversely, the soil TK content increased with increasing invasion level, peaking (12.04 g/kg) in severely invaded areas. In contrast to the aforementioned parameters, the AP content significantly decreased (P < 0.05) with increasing invasion level, decreasing by 47.24%, 39.08%, and 40.76% in lightly, moderately, and severely invaded areas, respectively (Fig. 2g, P < 0.05). Notably, although not statistically significant, the SOC content increased with increasing invasion level.

3.2 Effects of different levels of A. adenophora invasion on soil micronutrient content and availability levels

The mean concentrations of soil trace elements under different invasion levels are provided in Table 2. Although the differences in micronutrient concentrations across invasion levels did not reach statistical significance (P > 0.05), certain trends were observed. Except boron (B), which exhibited the highest concentration in noninvaded areas, the remaining seven micronutrients demonstrated increasing trends following A. adenophora invasion, with increases ranging from 0.99% to 18.08%. Specifically, the maximum concentrations of Zn, Ca, Mg, and Al occurred in severely invaded areas, whereas Fe and Cu peaked in moderately invaded areas. The highest Mn concentration only occurred in lightly invaded areas among all the sampled areas.

Table 2
Effects of micronutrients on *A. adenophora* under different invasion levels.
Different levels of invasion	Mean ± SE
Different levels of invasion	Fe mg/kg	Mn mg/kg	Zn mg/kg	Cu mg/kg	B mg/kg	Ca mg/kg	Mg mg/kg	Al mg/kg
C	21.2 ± 0.6a	902.33 ± 119.08a	44.47 ± 0.95	27.88 ± 0.45a	86.55 ± 5.57a	1.82 ± 0.21a	2.6 ± 0.1a	64.37 ± 1.29a
L	20.98 ± 1.03a	1065.47 ± 163.62a	44.1 ± 1.01a	27.73 ± 1.04a	73.48 ± 4.99a	1.7 ± 0.22a	2.52 ± 0.08a	66.55 ± 2.29a
M	21.41 ± 0.51a	822.4 ± 106.57a	45.32 ± 0.87a	29.85 ± 1.01a	81.32 ± 4.39a	1.54 ± 0.11a	2.56 ± 0.1a	66.05 ± 3.96a
S	20.77 ± 1.09a	948.38 ± 128.17a	44.82 ± 0.98a	29 ± 1.31a	78.62 ± 6.18a	2.01 ± 0.16a	2.72 ± 0.11a	70.71 ± 3.5a

With respect to the availability of soil micronutrients (Table 3), significant differences (P < 0.05) were observed in available Mn, Zn, and Cu contents across the areas with different invasion levels, with an overall increasing trend. The concentrations of available Mn, Zn, and Cu in severely invaded areas were 45.48%, 98.52%, and 72.87% higher, respectively, than those in noninvaded areas. Moreover, although the differences in available Fe, Ca, and Mg concentrations did not reach statistical significance (P > 0.05), the values generally peaked in severely invaded areas. Conversely, compared with that in noninvaded areas, the available Al concentration decreased by 19.04%, 25.06%, and 18.56% with increasing invasion levels.

Table 3
Effects of different levels of *A. adenophora* invasion on available micronutrients.
Different levels of invasion	Mean ± SE
Different levels of invasion	available Fe mg/kg	available Mn mg/kg	available Zn mg/kg	available Cu mg/kg	available B mg/kg	Exchangeable Ca mg/kg	Exchangeable Mg mg/kg	available Al mg/kg
C	40.22 ± 5.05a	64.54 ± 5.18b	0.22 ± 0.02b	0.57 ± 0.03c	0.1 ± 0.03a	3.16 ± 0.18a	1.15 ± 0.09a	52.07 ± 5.63a
L	45.24 ± 2.89a	76.62 ± 3.99b	0.31 ± 0.08ab	0.7 ± 0.04bc	0.12 ± 0.03a	4.24 ± 0.75a	1.26 ± 0.22a	42.16 ± 4.95a
M	42.72 ± 8.41a	68.43 ± 7.91b	0.25 ± 0.05ab	0.78 ± 0.08b	0.13 ± 0.03a	4 ± 0.18a	1.13 ± 0.02a	39.02 ± 7.23a
S	44.71 ± 1.97a	93.89 ± 3.25a	0.44 ± 0.09a	0.98 ± 0.08a	0.1 ± 0.03a	4.8 ± 0.69a	1.37 ± 0.19a	42.41 ± 3.72a
Note: C, noninvaded; L, lightly invaded; M, moderately invaded; S, severely invaded.

3.3 Effects of different levels of A. adenophora invasion on soil enzymes

The invasion of A. adenophora significantly affected soil SSC and NR activity levels (P < 0.05), whereas the impacts on soil SUE, CAT, and ALP activity levels were relatively minor (P > 0.05). In severely invaded areas, soil sucrase activity reached its peak value (26.09 mg/kg), whereas moderately invaded areas exhibited the lowest activity (12.90 mg/kg). Compared with those in noninvaded areas, lightly invaded areas exhibited comparable soil sucrase activity levels (Fig. 3b). Compared with those in noninvaded areas, soil nitrate reductase activity levels increased by 4.85% and 0.76% in lightly and moderately invaded areas, respectively, but decreased by 4.67% in severely invaded areas (Fig. 3c). Additionally, soil CAT (Fig. 3d) and ALP (Fig. 3e) activity levels increased with increasing invasion level.

3.4 Determination of the primary factors driving coverage change under different levels of A. adenophora invasion

This study revealed the complex interactions among soil trace elements, enzyme activity, and nutrient dynamics through comprehensive correlation analysis of soil enzymatic activity and physicochemical properties (Fig. 4). The results revealed significant correlations (P < 0.05) among various soil trace elements. Notably, TK was significantly positively correlated with B, Mg, and available Fe (P < 0.05) but significantly negatively correlated with AK (P < 0.05). TP was significantly positively correlated with AP and TN (P < 0.05) but significantly negatively correlated with available Ca and available Mg (P < 0.05). Furthermore, with respect to activity, significant positive correlations (P < 0.05) were observed among four soil enzymes (SSC, SUE, NR, and ALP). Importantly, the soil pH was significantly positively correlated with the SOC, SSC, ALP, CAT, AK, available Cu, and available Mn levels (P < 0.05).

The RFM, which is a robust machine learning tool, was employed in this study to systematically identify and predict the key environmental drivers influencing the invasion and spread of A. adenophora. Our model results revealed significant variations in the driving factors influencing the invasion coverage of A. adenophora across the areas with different invasion levels (Fig. 5). Specifically, in noninvaded areas (Fig. 5a), available Mn, AK, available Zn, available B, and Zn were identified as the most significant factors influencing the invasion coverage of A. adenophora (P < 0.05). In lightly invaded areas (Fig. 5b), Al, available Al, available Fe, available Mg, and available Ca emerged as the primary drivers (P < 0.05). In moderately invaded areas (Fig. 5c), Cu, Mg, Al, B, available Zn, available Cu, available Ca, and available Mn significantly affected the invasion coverage of A. adenophora (P < 0.05). In severely invaded areas (Fig. 5d), Mg, B, Zn, Fe, available Cu, and available Al were identified as the key drivers influencing invasion coverage (P < 0.05).

3.5 What are the pathways or mechanisms that contribute to the increase in the invasion coverage of A. adenophora?

SEM analysis was employed to elucidate the significant and nonsignificant pathways through which soil properties influence the coverage of A. adenophora (A. adenophora) under varying invasion levels, providing critical insights into its invasion mechanisms. In this study, we observed a significant linear increase in the soil pH following A. adenophora invasion (P < 0.05), indicating that its inclusion was an independent variable in the model (Fig. 2a). The key soil factors identified through the RFM were selected as observed variables, while the aboveground coverage of A. adenophora served as the dependent variable (Table 1). The results revealed distinct response pathways of soil physicochemical properties for A. adenophora across the different invasion levels (Fig. 6). Specifically, in noninvaded areas, pH indirectly influenced A. adenophora coverage by regulating the availability of soil nutrients (R² = 0.7), with AK emerging as a critical driver (P < 0.05). In lightly invaded areas, soil nutrients directly and significantly affected A. adenophora coverage (R² = 0.69), with a path coefficient of 0.64 (P < 0.05). In moderately invaded areas, both pH and soil nutrient content indirectly promoted A. adenophora coverage by influencing the availability of soil nutrients (R² = 0.52). Notably, the effects of soil nutrients (Al) and available nutrients (available Ca and available Cu) were significantly greater than that of pH, with path coefficients of 0.38 (P < 0.05) and 0.96 (P < 0.001), respectively. In severely invaded areas, both available nutrients and soil nutrients significantly influenced A. adenophora coverage (R² = 0.91), with path coefficients of 0.63 (P < 0.001) and 0.46 (P < 0.01), respectively. Importantly, B, Fe, and available Al played particularly significant roles in influencing A. adenophora coverage in severely invaded areas, highlighting the critical role of soil properties at advanced invasion stages.

4.1 A. adenophora invasion increases the soil pH and alters the levels of soil macronutrients

The soil water content and pH significantly influence plant growth and development (Puissant et al., 2019; Guo et al., 2022). Invasive plants modify soil pH conditions through changes in soil physical properties, such as increased water uptake and root infiltration (Niu et al., 2007; Xiao et al., 2017; Puissant et al., 2019). For example, Zhang and Suseela (2021) reported that the soil pH was significantly lower (pH = 5.3) in fertilized and invaded areas than in noninvaded areas (pH = 5.8) and other invaded areas (pH = 6.1). Additionally, invasive species have been shown to regulate the soil pH and alter the nutrient status, with Xia et al. (2022) demonstrating that significant releases of soil cations in invaded areas led to an increase in the soil pH due to the consumption of hydrogen ions (Bojórquez-Quintal et al., 2017; Fan et al., 2022; Wang et al., 2019; Chen et al., 2022; Marchante et al., 2023). The habitats in our study, which are located in Pinus yunnanensis forests, are characterized by high soil acidification (Xiao et al., 2017; Wu et al., 2020). We investigated whether A. adenophora can leverage its characteristics to promote invasion by improving habitat conditions. Our findings indicated that invasion significantly altered the soil pH in invaded areas, with a notable difference between severely invaded areas (with pH values ranging from approximately 5.4–6.2) and noninvaded areas (with pH values ranging from approximately 4.8–5.3) (Jones et al., 2019). Furthermore, research from Kashmir Himalaya has indicated that the soil pH in invaded areas is significantly greater than that in noninvaded areas after invasion (Kumar et al., 2021; Ahmad Dar et al., 2023; Dar et al., 2023), confirming that A. adenophora can increase the soil pH.

In highly acidic and alkaline soils, invasive plants modify their physicochemical properties, affecting nutrient availability, which is crucial for rapid growth and development (Osunkoya and Perrett, 2011; Ren et al., 2021; Yang et al., 2013; Souza-Alonso et al., 2014). The growth of A. adenophora relies on N- and P-enriched soils, leading to significant reductions in soil TN and AP concentrations in invaded areas (Khatri et al., 2023; Zhang and Suseela, 2021). This trend is supported by the gradual increase in the SOC content observed with increasing invasion level in our study (Sun et al., 2019; McLeod et al., 2021), as shown in Fig. 2e. Additionally, studies have indicated that plant invasion alters soil enzyme activity levels, thus affecting nutrient effectiveness (Zhang et al., 2022). Changes in soil properties and plant diversity due to A. adenophora invasion have also been observed in Punakha, Bhutan, and in evergreen broad-leaved forests in southwestern Yunnan Province, China (Lhamo et al., 2023; Zhao et al., 2019; Zhang et al., 2023). Our findings revealed that the soil TN content is significantly greater in lightly invaded areas than in severely invaded areas, whereas the soil TK content shows the opposite pattern (Zhang and Suseela, 2021). This difference may stem from the distinct nutrient requirements of A. adenophora; notably, in lightly invaded areas, A. adenophora may demand more TK for rapid growth, whereas in severely invaded areas, it may need more TN to increase biomass and soil organic matter (Chen et al., 2022; Cotrufo et al., 2022).

4.2 Invasion of A. adenophora significantly affects soil available micronutrient contents

Soil micronutrients, which are essential for plant growth, are effectively used by invasive species such as A. adenophora for growth and development (Liu et al., 2023). The relationship between soil enzyme activity and micronutrient levels often results in synergistic or antagonistic interactions with plants, influencing micronutrient uptake (Niu et al., 2007; Kaur et al., 2012; Jones et al., 2019). In this study, we investigated the preferences of A. adenophora for specific micronutrients and revealed that all micronutrients except available Al occur at higher concentrations in invaded areas than in noninvaded areas, with Mn, Zn, and Cu exhibiting significant variability across the areas with different invasion levels (Pizzeghello et al., 2011; Wu et al., 2023).

Excessive or insufficient soil micronutrient levels can be lethal to plants (Osunkoya and Perrett, 2011; Marchante et al., 2023). Recent research has indicated that A. adenophora can absorb copper ions from aquatic environments, acting as an adsorbent (Fan et al., 2022). Additionally, A. adenophora requires substantial amounts of boron (B) for growth, and B deficiency can be fatal to native plants (Bursali et al., 2009; Chen et al., 2021). Our findings also revealed a decreasing trend in the soil B content with increasing invasion level, whereas the Al content increased (Jones et al., 2019).

Previous research has demonstrated that reduced Fe and available Al levels in soil can lead to P loss (Pizzeghello et al., 2011). Consistent with these findings, our study revealed lower AP, Fe, and Al levels in invaded areas than in uninvaded areas (Chapuis-Lardy et al., 2006; Lin et al., 2023), which conforms with findings of Wu et al. (2020). There is consensus that changes in soil micronutrient levels impact soil properties, a phenomenon also observed in areas invaded by Lantana camara L. (Osunkoya and Perrett, 2011; Datta et al., 2017). Our results demonstrated that A. adenophora affects soil micronutrient levels as invasion progresses, particularly those of Mn, Zn, Al, B, Fe, and Cu (Wang et al., 2015; Shen et al., 2019; Souza-Alonso et al., 2014; Jones et al., 2019; Lin et al., 2023). This adaptation enables A. adenophora to alter soil properties and manipulate nutrient cycling, thus suppressing the development of native plants (Yang et al., 2013; Xiao et al., 2017; Fan et al., 2022).

4.3 Correlations between soil enzyme activity and soil nutrient levels altered by A. adenophora invasion

Soil enzyme activity is significantly correlated with both the ambient temperature and soil pH (Esch et al., 2017; Kim et al., 2018). Puissant et al. (2019) reported that the optimal pH for enzyme activity did not always coincide with the environmental soil pH. It is widely acknowledged that invasive plants can modify soil habitats, thereby altering soil properties and nutrient cycling via soil enzyme activities (Shen et al., 2019; Hu et al., 2021; Khatri et al., 2023). In our research, a strong correlation was observed between the soil pH and three soil enzymes, excluding nitrate reductase and urease (Fig. 4). Invasions by Amaranthus palmeri and Phragmites australis have been shown to significantly impact soil enzyme activity levels (Zhang et al., 2022; Kim et al., 2018). Similarly, our findings indicated that A. adenophora invasion significantly increased the activity of soil sucrase, catalase, and alkaline phosphatase (Wang et al., 2015; Puissant et al., 2019). However, changes in soil enzyme activity can be attributed to various mechanisms (Kim et al., 2018).

Soil enzyme activity, which is influenced by microorganisms, root secretions, and the decomposition of organic material, plays crucial roles in shaping plant invasion dynamics (DeForest and Moorhead, 2020; Lhamo et al., 2023). In the A. adenophora community, variations in enzyme activities across different invasion levels are likely linked to root secretions and apoplastic materials (Wherry, 1920; Yang et al., 2013; Zhao et al., 2019). Our study demonstrated that soil urease activity decreased gradually with increasing invasion level, while alkaline phosphatase activity increased slowly (Fig. 3). These observations conform with the results of other studies, where invasions by Mimosa pudica and Falcataria moluccana led to significant increases in soil urease, catalase, and acid phosphatase activity levels (Wang et al., 2015; Esch et al., 2017; DeForest and Moorhead, 2020; Hu et al., 2021). Furthermore, A. adenophora invasion significantly increased the activities of soil sucrase, catalase, and alkaline phosphatase, contributing to a sharp decline in soil TN and AP contents (Sun et al., 2019; Wang et al., 2019), which agrees with findings for Mimosa pudica invasion (Wang et al., 2015). This suggests that optimizing the nutrient acquisition efficiency by regulating soil enzyme activity is a common strategy for successful invasion (Zhao et al., 2019; Zhang and Suseela, 2021; Zhang et al., 2022).

4.4 Soil pH and micronutrients are important factors for A. adenophora invasion in acid-poor areas

A. adenophora invasion poses significant ecological threats, including biodiversity loss (Yang et al., 2013; Nunes et al., 2022; Guo et al., 2023) and adverse impacts on agriculture, forestry, and livestock health (Datta et al., 2017; Cotrufo et al., 2022). In the study area, the low soil pH under the canopy of Pinus yunnanensis has been associated with the increase in soil pH following A. adenophora invasion (Wu et al., 2020; Zhang et al., 2022). In this study, we integrated RFM and SEM analysis methods to systematically analyze the driving mechanisms of the influence of soil physicochemical properties on the aboveground coverage of A. adenophora during invasion (Xiao et al., 2017; Jones et al., 2019; Puissant et al., 2019). The results revealed that the invasion strategy of A. adenophora exhibits distinct stage-specific characteristics, with its success relying on dynamic adaptation and the regulation of soil environmental factors across different invasion stages (Ren et al., 2021; SUN et al., 2021).

Previous studies have demonstrated that A. adenophora modulates the soil pH to suit its optimal acclimation range, thereby increasing the soil pH when it is less than 6 and decreasing it when it exceeds 7.5 (Kumar et al., 2021; Wu et al., 2020; Zhang and Suseela, 2021). This raises the question of whether stabilizing the soil pH could effectively control A. adenophora invasion (Niu et al., 2007; Shen et al., 2019; Xu et al., 2023). The RFM results revealed stage-specific differentiation of driving factors during A. adenophora invasion (Fig. 5) (Malik et al., 2018; Guo et al., 2023; Marchante et al., 2023). In noninvaded areas, available Mn, Zn, and B play dominant roles in shaping invasion coverage (p < 0.05), likely because of the rapid nutrient acquisition strategy of A. adenophora during early invasion (Zhang and Suseela, 2021; Guo et al., 2022; Marchante et al., 2023). At the light invasion stage, the increased significance of Al and available Fe (p < 0.05) suggests that A. adenophora mitigates aluminum toxicity by altering soil metal ion speciation while enhancing competitiveness through iron-mediated redox processes (Yang et al., 2013). At the moderate to severe invasion stages, the significant influence of Cu, Mg, and available Ca (p < 0.05) may be linked to the regulation of the soil cation exchange capacity (CEC) via root exudates to optimize the nutrient acquisition efficiency (Xiao et al., 2017). This dynamic shift in driving factors reflects the evolution of A. adenophora strategies from nutrient exploitation to habitat modification, which conforms closely with the positive feedback loop theory of invasive plants (Niu et al., 2007). This feedback mechanism may operate through the following pathways: (1) chelation, which reduces aluminum toxicity and facilitates boron-dependent cell wall synthesis (Chen et al., 2021), and (2) nutrient availability optimization through soil pH modification (Wu et al., 2020). These adaptive strategies enable A. adenophora to more efficiently absorb soil nutrients at severe invasion stages, thereby suppressing native plant growth and ultimately displacing them from their ecological niches (Marchante et al., 2023).

Invasive plants disrupt native plant growth by modifying soil enzyme activity levels to favor their own development (Niu et al., 2007). SEM analysis revealed the synergistic effects of the soil pH and nutrient pathways (Fig. 6). In noninvaded areas, pH indirectly influences coverage by regulating available nutrients (R² = 0.7), with the key role of AK (path coefficient = 0.64, p < 0.05) likely related to the efficient use of potassium ion channels by A. adenophora during early invasion (Jones et al., 2019). With increasing invasion level, the direct effect of pH decreases, while the path coefficients of soil nutrients (e.g., Al and available Cu) significantly increase (p < 0.001), indicating that A. adenophora actively modifies the soil environment by altering rhizosphere microbial communities (e.g., acid-producing bacteria abundance) (Puissant et al., 2019; Lin et al., 2023). Particularly at severe invasion stages, the significant influences of available Al and B (path coefficient = 0.63, p < 0.001) may be attributed to their roles in reducing aluminum toxicity through chelation and promoting boron-dependent cell wall synthesis (Chen et al., 2021). This mechanism is particularly advantageous in regions with frequent acid rainfall (pH < 5.5) (Wu et al., 2020).

By combining RFM and SEM analysis methods, we quantified, for the first time, the threshold effects of the nutrient competition-habitat modification dual-stage model during A. adenophora invasion (Malik et al., 2018; Puissant et al., 2019; Guo et al., 2023). The light invasion stage (R² = 0.69) is characterized primarily by direct nutrient competition, which can be mitigated through early intervention targeting available Fe and Al (Lin et al., 2023). In contrast, the severe invasion stage (R² = 0.91) requires targeted strategies to disrupt the biogeochemical cycles of trace elements such as Cu and B (Kumar et al., 2021). Notably, the active regulation of pH by A. adenophora (with postinvasion pH increases ranging from 0.3–0.9 units) may exacerbate the vicious cycle of soil acidification and nutrient loss (Dar et al., 2023), providing a critical target for invasion control in acidic soil regions. Although this study identified key driving factors and their pathways, the impacts of soil microbial functional groups and faunal disturbances on nutrient cycling remain to be incorporated into the model (Lhamo et al., 2023). Future research could aim to integrate metagenomics and stable isotope labeling techniques to elucidate the regulatory mechanisms of rhizosphere microbe‒plant interactions for the turnover of specific nutrients (e.g., available Cu) (Guo et al., 2023). Additionally, on the basis of the stage-specific thresholds established in this study, biochar- or chelator-driven targeted remediation technologies could be developed to assess the feasibility of inhibiting A. adenophora expansion by disrupting the Al‒Cu‒B cycles (Fan et al., 2022).

In this study, we systematically investigated the dynamic changes and driving mechanisms of soil environmental factors in the invasion process of A. adenophora by integrating soil physicochemical properties, enzyme activities, and advanced modeling approaches, including RFM and SEM analysis methods. The results demonstrated that A. adenophora invasion significantly altered soil pH, nutrient content, and enzyme activity levels, with the driving factors exhibiting distinct stage-specific characteristics. Specifically, the soil pH increased with increasing invasion level, with an 8.37% increase in severely invaded areas compared with that in noninvaded regions (P < 0.05). The soil TN and AP contents significantly fluctuated with invasion level, with the TN content increasing by 35.38% in lightly invaded areas and the AP content decreasing by 40.76% in severely invaded regions (P < 0.05). Additionally, soil TK and micronutrients (e.g., Zn, Cu, and Mn) reached peak levels in severely invaded areas. Correlation analysis underscored the pivotal role of pH in regulating soil nutrient availability and microbial activity levels. The RFM results revealed significant differences in key driving factors across invasion stages: available Mn, AK, and available Zn were dominant in noninvaded areas (P < 0.05), whereas Mg, B, and available Cu were the primary drivers in severely invaded regions (P < 0.05). This highlights a shift in A. adenophora strategies from nutrient competition to habitat modification. SEM analysis was employed to quantify the synergistic effects of the soil pH and nutrient pathways and revealed that the path coefficient of available nutrients for coverage in severely invaded areas reached 0.63 (P < 0.001), indicating that A. adenophora exacerbates invasion through plant‒soil feedback mechanisms.

In summary, A. adenophora invasion establishes favorable habitat conditions by altering soil pH, nutrient cycling, and enzyme activity levels, thereby suppressing the growth of native plants and ultimately displacing them from their ecological niches. This study provides a systematic basis for the formulation of stage-specific control strategies against A. adenophora invasion. Early intervention through the regulation of the contents of available Fe and Al is recommended at the light invasion stage, whereas targeted strategies to disrupt the biogeochemical cycles of Mg, B, and available Cu are essential for managing severe invasion.

Acknowledge

This research was funded by the financial support of Sponsored by Funded Projects: Scientific research projects of China Three Gorges (Construction) Group Corporation (JG-EP-030222001 and JG-EP-030222002); Western Light Project of the Chinese Academy of Sciences (2022XBZG_XBQNXZ_A_003), Sichuan Science and Technology Program (2025ZNSFSC1017).

CRediT author statement

Juan Wang & Jingying Lu & Yuehua Zhang & Xianyong Dong & Xiaogang Wu & Lumei Xiao & Kaiwen Pan & Lin Zhang: Sample-plot Investigation, Conceptualization, Methodology, Software, Data curation, Visualization, Writing- Original draft preparation, Writing- Reviewing and Editing, sample-plot Investigation, Supervision, Revise, Writing- Reviewing and Editing, Funding acquisition.

Declaration of interests

☒ 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.

☐ The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:

data availability statement

Data will be made available upon request

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The Soil pH and Micronutrients Drive Ageratina Adenophora Invasion in Areas with Acidic and Nutrient-Poor Soils

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