Dynamics of soil nutrients and biological activities along an infection chronosequence of pine wilt disease in subtropical Masson pine forests

Pine wilt disease (PWD) is a devastating forest disease that severely impacts pine trees, with widespread outbreaks leading to catastrophic damage in pine forests worldwide. Our study aims to investigate the dynamics of PWD infection on soil physicochemical properties and biological activities, as well as the interrelationships between them. Soil samples were collected from 0 to 10 cm and 10 to 20 cm depths in subtropical Pinus massoniana (Masson pine) forests with PWD infection years of 0 (non-infection), 6, 10, and 16 years. The physicochemical properties, microbial biomass, and enzymatic activities of these soil samples were measured. The results revealed that soil non-capillary porosity, clay, microbial biomass carbon and microbial biomass nitrogen decreased significantly in 6 years forests. Available potassium consistently decreased with longer invasion periods, while soil polyphenol oxidase, leucine amino peptidase, and available phosphorous peaked in 6 years forests and then declined over time. The soil physicochemical properties, biological activities all decreased as soil depth increased. Redundancy analysis and Mantel tests underscored the critical role of Total potassium, pH, Total phosphorous, and bulk density in shaping microbial activities. This study demonstrated that PWD infection significantly effect on soil physicochemical properties, microbial biomass, and enzymatic activities with the chronosequence progresses. These finding contribute to a deeper understanding of how invasive pathogens like PWD can reshape soil environments, with implications for forest conservation and restoration practices.

Introduction

Pine wilt disease (PWD) is a globally significant quarantine forest disease caused by the Bursaphelenchus xylophilus (pine wood nematode, PWN) that primarily affects pine trees (Yang et al., 2014). Originating in North America, PWD was first reported in Japan in the early 20th century. It has since become established in several countries, including China, Japan, South Korea, the United States, Portugal, and Mexico, causing widespread pine mortality as well as significant ecological and economic losses (Liu J. et al., 2023; Back et al., 2024). In Europe, PWD has been detected in Portugal, where it has led to significant pine mortality, raising concerns about the potential for further spread across the continent (Seidl et al., 2018; Calvão et al., 2019). In China, PWD was first found in the Nanjing city in 1982, then it has rapidly spread to many other regions, particularly in the southern provinces (Hao et al., 2021). The subtropical climate of these areas, characterized by warm temperatures and high humidity, creates an ideal environment for the proliferation of the PWN and its vector beetles (Tang et al., 2021). As a result, large-scale pine die-offs have occurred, severely affecting the landscape and local economies dependent on pine forests (Hao et al., 2022).

Soil is a critical component of forest ecosystems, serving as a reservoir of nutrients, organic matter, and microbial communities that support plant growth and maintain ecosystem balance (Binkley and Fisher, 2019). PWN is transmitted by insect vectors, which introduce the nematode into pine trees during feeding (de la Fuente and Beck, 2019; Liu Y. et al., 2023). An infected pine tree typically exhibits reduced or halted resin secretion alongside rapid needle dehydration and yellowing, impairing its photosynthetic capacity and potentially causing death within a few months (Tian et al., 2022). The loss of pine trees due to PWD not only reduces forest cover but also disrupts the ecological balance of affected areas (Binkley and Fisher, 2019). Moreover, the death of pine trees has cascading effects on other ecological processes, particularly those related to the soil environment, including soil properties and biological activities (Wu et al., 2023; Baek and Kim, 2023). Research has shown that PWD can cause significant alterations in the soil chemical composition, affecting not only nutrient availability but also soil pH and the balance of soil minerals (Chu et al., 2016). Gao et al. (2015) reported shifts in soil nutrient elements following pine mortality: due to decreased litter input and increased nutrient leaching, the levels of elements such as nitrogen and potassium declined with the duration of the PWD invasion. The decomposition of dead pine trees also influences the soil’s physical properties, including its structure and water-holding capacity. The loss of tree roots also can lead to increased soil erosion and compaction (Kim et al., 2010). These changes in physical and nutrient conditions can impact microbial communities essential for nutrient cycling, potentially altering both their diversity and function of the soil ecosystem (Jiao et al., 2023).

Soil biological activity plays a crucial role in organic matter metabolism and is closely linked to soil properties (Gispert et al., 2013; Zhang et al., 2018). It is generally recognized that soil microbial biomass and enzyme activity increase with the length of cultivation and serve as effective indicators for assessing soil quality (Lucas-Borja et al., 2016). In addition to changes in nutrient dynamics, the death of trees and the subsequent changes in soil conditions can disrupt these microbial communities, leading to shifts in their structure and function (Back et al., 2024; Mabuhay and Nakagoshi, 2012). Previous studies have indicated that PWD can lead to an initial boost in microbial activity, as decomposing wood and needles provide a source of organic carbon (Baek and Kim, 2023). However, as the decomposition process progresses and the availability of easily decomposable organic matter decreases, microbial activity may decline, leading to changes in the composition and function of the microbial communities (Qu et al., 2020; Guo et al., 2023). Zhang et al. (2021) reported a marked increase in soil microbial biomass carbon and nitrogen levels following the removal of dead trees affected by PWD. PWD infection also accelerates forest succession, leading to significant changes in soil microbial community composition and structure at different stages of succession (Qu et al., 2020).

Pinus massoniana (Masson pine) is a keystone species in subtropical forests, particularly in southern China (Chi et al., 2023). These forests are not only economically valuable, providing timber and non-timber forest products, but they also play crucial roles in maintaining regional ecological balance (Pan et al., 2021). They contribute to carbon sequestration, soil conservation, water regulation, and biodiversity preservation (Gao et al., 2015). The latest survey data shows that the planting area of Masson pine has exceeded 8 million hectares (National Forestry and Grassland Administration, 2020). Statistics indicate that PWD currently affects about 650,000 hectares annually, with the majority of the dead pine trees being Masson pines in China (Wang et al., 2022). Previous research has primarily focused on changes in soil physicochemical properties (Bashir et al., 2021; Siegert et al., 2024), and microbial activities (Shi et al., 2015a; Qu et al., 2022) by PWD infection. However, there remains a paucity of studies examining the temporal dynamics—and their interrelationships—of soil physicochemical properties, microbial biomass, and soil enzyme activities in PWD-infected Masson pine forests.

It is crucial to develop effective strategies for managing forests affected by PWD by understanding its impact on soil nutrient characteristics and biological activities (Qu et al., 2022). Previous research has provided valuable insights into the immediate effects of PWD on soil and forest ecosystems, but there is limited understanding of the interactions between soil nutrient changes and microbial activity within the context of pest disturbances and the long-term resilience and sustainability of forest ecosystem (Jeong et al., 2013; Holden and Treseder, 2013). Furthermore, the chronosequence of PWD infection—referring to the progression of infection over time—provides a opportunity to study the temporal dynamics of soil nutrient properties and biological activities (Gao et al., 2015), which allow researchers to infer the long-term effects of PWD by examining soils at different stages of infection (Anderson-Teixeira et al., 2021). The primary aims of this study sought to (i) characterize the changes in soil nutrient properties along a PWD infection chronosequence and across different soil layers in subtropical Masson pine forests, (ii) investigate the associated changes in soil biological activities—including microbial biomass and enzyme activities critical for nutrient cycling, and (iii) determine the response of microbial biomass and enzymatic activities to soil physicochemical properties and the relationships among the three along the chronosequence.

Materials and methods

Study region

Our research was conducted in Yichang City, Hubei Province, China (Table 1). This area has an eastern mid-subtropical monsoon climate, with a with a mean annual temperature of 16.9°C and a mean annual precipitation of 1215.6 mm, respectively. Before the PWD invasion, Masson pine was the dominant tree species in the region, widely distributed at elevations between 45 and 1500 m, playing a crucial role in ecological and environmental protection (Gao et al., 2015). Moreover, since the area is a key environmental protection zone, these Masson pines have not been subjected to any human-induced logging since their planting, and there are no records of significant natural disasters (such as fires or snowstorms). The PWD is currently the only recorded severe natural disaster affecting the Masson pine forests. Since 2006, PWD attacked the Masson pines in this area and has since spread rapidly (Gao et al., 2018).

TABLE 1

Table 1. General information on each site in the Masson pine forests.

Soil sampling

We selected four stands which had consistent stand age and initial planting density based on the PWD invasion data provided by the local forestry department. The four stands selected were Masson pine forests that had not been invaded by PWD (non-infection, 0 years) and had been invaded by PWD for 6, 10, and 16 years, respectively. Three plots (20 × 20 m) for each site were randomly established for the subsequent soil sampling. There were 12 plots (four PWD infection years × three replicate plots). Detail information for each period of Masson pine forest is shown in Table 1.

In each plot, 5 sampling points were selected along an S-shaped curve, with each point at least 1 meter away from the trees. Soil samples were taken from 0 to 10 cm and 10 to 20 cm depths after removing forest litter and herbaceous plants. Firstly we collected the soil by cutting ring (100 cm³) method for bulk density and non-capillary porosity analyses (Zhang et al., 2018). Soil samples were collected using a soil auger with a 5 cm inner diameter. Samples from the same plot and soil layer were thoroughly mixed and evenly divided into two portions: one portion was immediately stored at 4°C for the analysis of soil biological properties, while the other was reserved for chemical analysis.

Laboratory analysis

Soil non-capillary porosity (NCP) and bulk density (BD) were determined within the cutting ring in the laboratory. Soil pH was measured in soil-water (1:2.5 w/v) suspension using a pH meter (PHS–25, REX, China) (Zhang et al., 2018). Clay was measured by the hydrometer method. The soil organic carbon (SOC), total N (TN) and available N (AN) were measured using an elemental analyzer (Euro EA, Germany). The determination of total P (TP) and available P (AP) was conducted with a UV-Visible Spectrophotometer (UV-2550, Japan) using ammonium molybdate. Total K (TK) was measured using the NaOH fusion–molybdenum antimony colorimetric method (Chen et al., 2022). Available K (AK) content was analyzed by plasma emission spectroscopy following digestion with a 1 mol⋅L⁻¹ NH4OAc solution (IRIS Intrepid II XSP, USA).

The chloroform fumigation-extraction method was used to estimate the microbial biomass (C, N, and P) (Bao, 2000). Soil enzyme activities were analyzed by Saiya-Cork et al. (2002) using a microtiter plate fluorescence assay for the determination of four hydrolases and two oxidoreductases including β-glucosidase (BG), acid phosphatase (ACP), N-acetyl-glucosidase (NAG), leucine amino peptidase (LAP), polyphenol oxidase (POX) and peroxidase (PER).

Statistical analyses

A one-way analysis of variance (ANOVA) were used to assess the differences in stand density and DBH between stands of infection years, followed by post hoc multiple comparisons using the Tukey-HSD method. A linear mixed-effects model (LMM) was used to analyze differences in soil physicochemical properties, microbial biomass, and enzyme activities, with the duration of PWD infection specified as a fixed effect and replicate plots within each stand treated as a random effect.

Data analysis was performed using SPSS 26.0 and JMP 17. All plots were performed in Origin 2024 Mantel test analysis between soil physicochemical properties and microbial activity was conducted using the “ggcor” R package, and correlation heatmaps were generated using ChiPlot (accessed on August 21, 2022)¹. Redundancy analysis (RDA) was conducted using CANOCO 5.0 to assess the relationships among soil physicochemical properties, microbial biomass, and biological activities.

Results

Soil physical and chemical properties

The physicochemical properties in different soil depth of the Masson forests showed significant changes with increasing PWD infection years (Table 2). NCP in 10–20 cm was significantly reduced in 6-year infection forests of PWD, and gradually recovered with increasing years of invasion. Soil clay in 0–10 and 10–20 cm depth in infected forests were significantly decreased. Soil pH showed an increasing, then decreasing, then increasing trend with the number of years of PWD infection in 0–10 and 10–20 cm depth. The SOC in the 10–20 cm depth increased in 10 years infection forests. TP and AP were both significantly increased in 6 years forests of PWD invasion, and then decreased with increasing years of invasion. AK showed a decreasing trend in 0–10 and 10–20 cm soil depth with increasing years of PWD invasion. Soil nutrient elements decreased with increasing soil depth.

TABLE 2

Table 2. Soil physiochemical properties between different PWD infection years.

Soil microbial biomass and enzymatic activities

The microbial biomass and enzyme activity in different soil depth of the Masson forests showed significant changes with the increase in PWD infection years (Figure 1). Compared to non-infection stands, there was a significant increase in BG activities in 10–20 cm soil depth of the 16-year infection forests. PWD infection significantly increased LAP activities in 0–10 cm soil depth. At the same time, during the initial stages of PWD invasion, the POX activities also significantly increased, reaching its peak in 6 years infection forests.

FIGURE 1

Figure 1. Soil enzymatic activities (A–F) and microbial biomass (G–I) between different PWD infection years. MBP, microbial biomass P; MBC, microbial biomass C; MBN, microbial biomass N; BG, β-glucosidase activities; ACP, acid phosphatase activities; NAG, N-acetyl-glucosidase activities; LAP, leucine amino peptidase activities; POX, polyphenol oxidase activities; PER, peroxidase activities. Different lowercase letters indicate significant differences between stands with varying durations of PWD infection at the same soil depth (p < 0.05).

In 10–20 cm soil depth, MBC and MBN showed a trend of initially decreasing and then increasing with increasing years of PWD invasion, and the lowest values were observed after 10 years infection forests.

Relationships between soil physicochemical properties and biological activities

Mantel tests and RDA analysis were used to examine the relationship between the soil biological variables and the physicochemical variables (Figures 2, 3 and Supplementary Table 1). TK was significantly positively correlated with enzyme activity in 0–10 cm soil depth (Figure 2A). SOC and BD exhibited a significant positive correlation with microbial biomass (Figure 2B) in 10–20 cm soil depth. Mantel tests further revealed a highly significant negative correlation between TP and clay, and a highly significant positive correlation between TP and AP, AN and TN (Figures 2A, B).

FIGURE 2

Figure 2. Correlations among the soil biological activities and physical-chemical properties in 0–10 cm (A) and 10–20 cm (B) depth. Significance levels of each predictor are *p < 0.05, **p < 0.01, ***p < 0.001.

FIGURE 3

Figure 3. Relationships between soil biological activities and physicochemical properties at soil depths of 0–10 cm (A) and 10–20 cm (B) were identified by RDA.

The results of RDA showed that the first two axes of the plot explained 42.97 and 25.09% of the variation in soil biological activities (soil microbial biomass and enzyme activities) in 0–10 cm soil depth (Figure 3A), and 37.25 and 20.86% in 10–20 cm soil depth (Figure 3B). In particular, the TK and pH were important soil factors affecting soil biological activities in 0–10 cm soil depth. BD and AP important soil factors affecting soil biological activities in 10–20 cm soil depth.

Discussion

Effects of PWD infection on soil physicochemical properties

The reduction in NCP and clay during the early stages of PWD infection, particularly noticeable in 6 years infected forests, indicates significant soil structure disruption (Table 2). Coarser soils may experience increased erosion risks and reduced ability to retain organic matter and nutrients, influencing overall soil fertility and ecosystem stability. This initial compaction is likely due to the loss of plant biomass, resulting in reduced soil aeration and water infiltration capacity (Gao et al., 2015). Furthermore, the decrease in tree canopy cover caused by widespread pine mortality enhances understory light availability and increases water evaporation, contributing further to soil compaction (Sakamoto et al., 2003; Fukasawa, 2016). However, the gradual recovery of porosity over time indicates a resilience of soil structure, potentially due to the re-establishment of plant or microbial activity that helps to re-aggregate soil particles (Liu J. et al., 2023; Guo et al., 2023).

We observed that soil nutrients exhibited a complex interaction between soil chemistry and disease progression (Table 2). The early increase in TP and AP in PWD-infected soils indicates an initial phase of nutrient release, possibly due to the breakdown of organic matter and root tissues. The peak phosphorus levels in the 6-year infection forests emphasize the rapid nutrient cycling during the early infection stages, which could temporarily enhance soil fertility (Hok et al., 2015). Conversely, the decreasing trend in soil AK with prolonged PWD infection underscores ongoing nutrient depletion (Table 2). These changes may be due to the increased nutrient consumption resulting from the recovery of vegetation biomass as the duration of PWD infection progresses (Fukasawa, 2016). Previous studies have suggested that soil nutrients are generally higher in non-infection stands compared to infected ones (Kim et al., 2011; Mabuhay and Nakagoshi, 2012). Differences in research results may be due to variations in soil properties arising from changes in observation time, forest conditions, and vegetation structure (Ge et al., 2014; Gao et al., 2018). These variations might be due to changes in soil physical properties, like BD, resulting from PWD infection, which influence microbial community composition and activity. Consequently, this can impact the availability of essential nutrients for plants, ultimately affecting nutrient cycling and ecosystem functions within the forest (Cobb et al., 2016). Notably, the absence of significant changes in soil BD, TN, TK, and AN across different years of PWD infection suggests that these properties are less sensitive to PWD impacts or may reflect a balance between nutrient inputs and losses. This stability might indicate a resilient aspect of soil properties that can buffer against the disturbances caused by PWD, maintaining certain critical soil functions, or that their responses are more delayed and require longer observation periods to manifest (Siegert et al., 2024; Anderson-Teixeira et al., 2021).

Effects of PWD infection on soil microbial biomass and enzymatic activities

The observed significant increases in LAP and POX activities during the early stages of PWD infection, with peaks observed at 6 years (Figures 1D, E), highlight notable shifts in microbial enzymatic profiles. These findings suggest that the initial stages of PWD invasion introduce substantial amounts of dying and decaying tree material into the soil (Fujihara, 1996; Fukasawa, 2018). This influx likely stimulates microbial activity related to lignin and nitrogen degradation, as microbes increase the production of LAP and POX to process the newly available substrates (Wan et al., 2022; Xu et al., 2020). Conversely, the long-term effects of PWD infection are reflected in the changes observed in BG and NAG activities (Figures 1A, C). The increased activities of these enzymes indicate that long-term PWD infection likely alters the composition and input of organic matter, prompting microbial communities to enhance BG and NAG activities to meet their carbon and nitrogen needs. This will benefit the restoration of the soil ecosystem in affected forests, as the increased enzyme activities help promote the decomposition of organic matter and the cycling of nutrients, thereby improving soil health and ecological function (Chen et al., 2024).

Our observations also revealed that changes in microbial biomass did not consistently correlate with changes in enzyme activity levels (Figures 1G–I). The invasion of PWD involves not only biotic disturbances but also abiotic disturbances (Fukasawa, 2016). Firstly, the invasion of PWD leads to tree mortality, which alters the underground soil environment and impacts soil ecosystem functions (Shi et al., 2015b). Secondly, abiotic disturbances can also exert significant influence during biotic disturbances (Holden and Treseder, 2013; Wen et al., 2022). For example, human activities such as felling diseased trees can result in severe soil compaction (Veldkamp et al., 2020). Soil compaction alters soil porosity, potentially impairing gas exchange, reducing drainage, and inhibiting soil microbial growth (Nazari et al., 2021). The burning of infected wood can damage the soil by heating and scorching the surface layer (Whitman et al., 2019). The direct impact of abiotic disturbances on soil properties can partly explain the alterations in soil characteristics observed after such events (Fichtner et al., 2014). However, biotic disturbances generally do not cause direct physical alterations to the soil but can lead to significant indirect effects on soil properties (Zhang et al., 2024). We hypothesize that during the initial stages of PWD invasion, alterations in soil physicochemical properties—including pH, SOC, and clay — along with fluctuating pH levels, created a stressful environment for microbial communities. This stress may have influenced microbial metabolic processes and enzyme stability. Although soil conditions appeared to improve subsequently, leading to a more favorable environment for microbial growth and activity, the initial decline in biological activities may have resulted from a delayed microbial response to these environmental changes (Norris et al., 2023).

Relationship between physicochemical properties and biological activities

The results from Mantel test and RDA analysis revealed a significant positive correlation between soil physicochemical properties and biological activity (Figures 2, 3). These findings emphasize that maintaining adequate levels of these soil properties could be crucial for sustaining soil function in PWD-affected forests. For example, Potassium is essential for microbial metabolism and enzyme production, and its availability directly influences enzyme activities involved in nutrient cycling (Hou et al., 2018). Increased soil nutrient content levels can enhance microbial growth and enzymatic activity, thereby supporting the soil’s ability to process organic matter and potentially suppress pathogen populations through competitive interactions (Guo et al., 2023; Yan et al., 2024). High BD can restrict root growth, reduce pore space for microbial activities, and limit nutrient availability (Gérard, 2016), which can exacerbate the effects of PWD infection. BD was positively correlated with microbial activities in 10–20 cm depth (Figure 2B), suggesting that despite increased compaction, microbial biomass and activity can persist if other conditions are favorable. This resilience indicates that deeper soil layers may support substantial microbial communities, which can contribute to nutrient cycling and ecosystem functioning even under stress conditions induced by PWD infection (Liu Y. et al., 2023).

Previous studies have suggested that pH is a critical factor influencing soil biological activities (Mabuhay and Nakagoshi, 2012). Conifer species, through their mycorrhizal associations, can release organic acids and absorb basic cations, contributing to soil acidification (Rigueiro Rodríguez et al., 2012). The decline in mycorrhizal activity under the influence of PWD may have contributed to a marked increase in the pH of the affected soil (Ma et al., 2020). Fan et al. (2023) found that adjusting soil pH significantly alleviates the incidence and severity of PWD. In the context of PWD infection, pH fluctuations can influence microbial populations differently, potentially altering enzyme activities and overall soil health (Figure 2 and Table 2). A favorable pH range can enhance enzyme activities and microbial processes, contributing to a more resilient soil ecosystem (Chen et al., 2022). In subtropical Masson pine forests, managing soil pH within an optimal range can enhance microbial functions and improve the soil’s resilience to PWD infection (Fan et al., 2023).

The observed relationships between soil properties and biological activities have significant implications for forest management and disease control strategies in subtropical Masson pine forests (Holden and Treseder, 2013; Norris et al., 2023; Fan et al., 2023; Zhang et al., 2024). In the topsoil, enhancing organic matter inputs, optimizing phosphorus availability, and managing soil pH can bolster microbial activity and enzyme functions, improving the soil’s ability to cope with PWD infection (Zhang et al., 2018). Practices such as compost application, pH adjustment, and balanced fertilization can support microbial health and potentially suppress pathogen populations through competitive and antagonistic mechanisms (De Corato, 2020). For deeper soil layers, strategies to manage phosphorus levels and alleviate soil compaction are crucial. Implementing practices to reduce BD, such as minimizing understory vegetation disturbance or enhancing biological control, can improve soil structure and microbial habitat, thereby enhancing resistance to PWD infection (Yang et al., 2014; Back et al., 2024).

Conclusion

Our results demonstrated that the duration of PWD infection significantly influence the soil physicochemical properties, microbial biomass, and enzymatic activities. These changes reflect the adaptive response of the microbial community to changes in soil conditions after PWD infection. The strong correlations between physicochemical properties and microbial activities emphasize the interdependence of soil properties and biological processes under PWD stress. In summary, our results reflect the impact of prolonged PWD infection on soil physicochemical properties and microbial activity, as well as their potential interrelationships. They enhance our understanding of soil conditions and processes across different soil depths under PWD infection, which is crucial for the restoration of Masson pine forest ecosystems.

Data availability statement

The original contributions presented in this study are included in this article/Supplementary material, further inquiries can be directed to the corresponding authors.

Author contributions

XS: Investigation, Writing – original draft. ZJ: Writing – review and editing. KW: Writing – review and editing. XW: Funding acquisition, Project administration, Writing – review and editing. WX: Methodology, Writing – review and editing, Formal Analysis, Supervision.

Funding

The author(s) declare that financial support was received for the research and/or publication of this article. This work was supported by the Fundamental Research Funds of CAF (CAFYBB2021ZG001) and National Key R&D Program of China (2021YFD1400900).

Acknowledgments

We thank the staff who provided assistance in sampling and investigations and the Hubei Zigui Three Gorges Reservoir National Forest Ecosystem Observation and Research Station that provided support in investigations, and samples process.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Generative AI statement

The authors declare that no Generative AI was used in the creation of this manuscript.

Publisher’s note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Supplementary material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/ffgc.2025.1544221/full#supplementary-material

Footnotes

1. ^https://www.chiplot.online/

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