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Article

Eleven-Year Canopy Nitrogen Addition Enhances the Uptake of Phosphorus by Plants and Accelerates Its Depletion in Soil

by
Xiaoli Gao
1,2,3,
Yinmei Gao
4,
Xiaowei Li
3,5,
Chenlu Zhang
3,5,*,
Quanxin Zeng
6,
Xiaochun Yuan
6,7,
Yuehmin Chen
6,*,
Yuanchun Yu
2 and
Shenglei Fu
3,5
1
College of Tourism, Xinyang Normal University, Xinyang 464000, China
2
College of Ecology and Environment, Nanjing Forestry University, Nanjing 210037, China
3
Xinyang Academy of Ecological Research, Xinyang 464000, China
4
Department of Geology and Mining Engineering, Henan Geology Mineral College, Zhengzhou 451464, China
5
Key Laboratory of Geospatial Technology for the Middle and Lower Yellow River Regions, Ministry of Education, College of Geography and Environmental Science, Henan University, Kaifeng 475004, China
6
School of Geographical Sciences, Fujian Normal University, Fuzhou 350007, China
7
College of Tourism, Wuyi University, Wuyishan 354300, China
*
Authors to whom correspondence should be addressed.
Forests 2024, 15(3), 416; https://doi.org/10.3390/f15030416
Submission received: 29 December 2023 / Revised: 12 February 2024 / Accepted: 19 February 2024 / Published: 22 February 2024
(This article belongs to the Special Issue Soil Organic Carbon and Nutrient Cycling in the Forest Ecosystems)
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Abstract

:
Soil phosphorus (P) is a critical factor that limits plant productivity. Enhanced nitrogen (N) deposition has the potential to modify P transformation and availability, thereby potentially affecting the long-term productivity of forests. Here, we conducted an 11-year-long field experiment to simulate N deposition by adding N to the forest canopy in a N-limited northern subtropical forest in central China and assessed the changes in soil organic P mineralization, P fractions, microbial biomass P content, phosphatase activity, and plant P content under N deposition. Our objective was to establish a theoretical framework for addressing the P supply and sustaining plant productivity in soils with low P availability, particularly in a changing global setting. The results demonstrated a substantial reduction in the levels of total, organic, and available P owing to the canopy addition of N. Furthermore, there was a marked decrease in the proportion of organic P in the total P pool. However, no substantial changes were observed in the soil inorganic P content or the proportion of inorganic P within the total P across different treatments. Canopy N addition significantly enhanced the microbial biomass P content, phosphatase activity, and organic P mineralization rate, suggesting that in soils with limited P availability, the primary source of P was derived from the mineralization of organic P. Canopy N addition substantially increased the P content in leaves and fine roots while concurrently causing a considerable decrease in the N:P ratio. This indicates that N deposition increases P demand in plants. Correlation analysis revealed a significant negative association among the total, organic, and available P levels in the soil and plant P concentrations (p < 0.05). This suggests that the primary cause of the reduced fractions of P was plant uptake following canopy N addition. Various studies have demonstrated that N deposition induces an augmented P demand in plants and expedites the utilization of available P. A substantial reduction in potentially accessible soil P caused by N deposition is likely to exacerbate regional P depletion, thereby exerting adverse impacts on forest ecosystem productivity.

1. Introduction

Soil phosphorus (P) plays a crucial role in determining the structural evolution and function of forest ecosystems because it is an essential nutrient required for plant growth [1,2,3]. The availability of soil P is influenced by factors such as soil mineral composition, pH, moisture content, temperature variation, vegetation type, land management practices, and human activities [4,5,6]. Over the past century, human activities, such as intensive agricultural practices, rapid industrial and urban development, and increased fuel consumption in transportation and energy production, have resulted in excessive inputs of reactive nitrogen (N), which greatly exceed ecosystem N requirements [7,8,9]. Consequently, a significant increase has been noted in anthropogenic emissions of reactive N, which has had a substantial impact on the P cycle and associated processes within forest ecosystems, leading to modifications in soil P fractions and availability [10,11]. Consequently, this topic has emerged as a focal point of research.
Previous investigations of terrestrial ecosystems have demonstrated that N deposition can enhance the net primary productivity of plants in most N-limited ecosystems [12,13]. However, excessive N supply may result in reduced biodiversity within forest ecosystems, soil acidification, and the loss of soil P [14,15]. The application of N enhances the P demand of plants and microorganisms, thereby intensifying their competition for soil P and ultimately limiting P in ecosystems [15,16,17,18]. The findings can be summarized by highlighting three primary domains: first, N deposition enhances the availability of N in the soil, further aggravating the imbalance between N and P nutrients [19,20,21]; second, N deposition stimulates plant growth, thereby increasing their demand for P. Consequently, the balance between absorbed N and available P supply in soil may become challenging to maintain, resulting in an elevated N:P ratio within the leaves [22,23,24,25]; and third, N deposition can affect the sorption and desorption processes of P in both the solid and liquid phases of the soil [26,27]. For instance, N deposition can lead to soil acidification, which in turn stimulates the fixation of soluble P by activated aluminum (Al) and iron (Fe) hydrous oxides [28,29,30,31], thereby reducing the availability of P in the soil. The alternative hypothesis proposes that N deposition does not exacerbate P limitations in forest ecosystems. For instance, Yu et al. [32] discovered that after 18 years of N addition, an investigation of N-saturated South Asian tropical forests did not reveal a discernible increase in either P demand by plants or reduction in P limitations on plant growth. Chen et al. [33] conducted a meta-analysis on the findings of 140 global studies and discovered that in cases where N application duration is short (≤5 years), the limitation of P caused by N deposition in terrestrial ecosystems can be alleviated through an increase in soil phosphatase activity, thereby ensuring an adequate supply of P to sustain plant growth. Furthermore, Deng et al. [34] conducted a global meta-analysis of 192 published studies and revealed that N deposition can fulfill the P demand to promote accelerated plant growth in P-deficient ecosystems. The increased demand for P by plants is primarily achieved through the enhancement of internal biochemical processes within ecosystems, such as plant P resorption, soil P mineralization, and P dissolution, rather than by relying on more energy-intensive pathways, such as the enhancement of fine roots and mycorrhizal fungal abundance. These findings suggest that the effect of N deposition on soil P transformation and availability is complex and influenced by multiple factors [25,32,35]. Currently, as there is no consensus or comprehensive understanding, further investigation is required.
Notably, the aforementioned study applied a direct spray of N solution onto the forest floor to simulate the increased deposition of atmospheric N in forest ecosystems without considering a series of interception processes, such as N absorption, adsorption, and transformation by the tree canopy [36]. In reality, a large proportion of N is initially absorbed by leaves and subsequently stored in branches and stems [37]; thus, ignoring the forest canopy could introduce several uncertainties in the findings of this study [38,39,40,41]. Therefore, in 2012, we constructed the world’s most advanced experimental platform for simulating natural atmospheric N deposition by adding N to the forest canopy at the Jigongshan National Nature Reserve in Xinyang City, Henan Province, Central China [36]. This platform enables a more precise simulation of atmospheric N deposition processes. The northern subtropical forest ecosystem (adjacent to the warm temperate climate zone) was chosen as the research site for this study because of the unique convergence of plants from both the northern and southern regions, rendering the forest ecosystem’s structure and function highly responsive to environmental changes [36,42,43]. In this mixed zone between the northern subtropical and warm temperate regions, southern plant species, such as Pinus massoniana, Castanea mollissima, Pteroceltis tatarinowii, and Lindera glauca, cohabit with northern plant species, such as Quercus variabilis, Quercus acutissima, and Quercus aliena. Consequently, it serves as a natural laboratory with excellent representativeness and potential for investigating the response and feedback mechanisms of nutrient availability to global change [36]. Understanding the P transformation process and plant P demand in northern subtropical forest soils under the backdrop of long-term N deposition is important for evaluating the impact of N deposition on forest ecosystem structure and function. Furthermore, it plays a pivotal role in using the pertinent Earth System P Cycle Models to guide forestry management and formulate environmental protection policies [32].
In this study, a long-term (11 years) manipulative experiment was conducted in a N and P-limited northern subtropical forest in central China. We aimed to evaluate the impact of a novel and realistic manipulation of canopy addition of N at three different rates (0, 25, and 50 kg N ha−1 yr−1) on soil organic P mineralization, P fractions, microbial biomass P (MBP), phosphatase activity (AcP), and plant P content in a subtropical forest ecosystem. Our hypotheses were as follows: (1) Canopy N addition over an 11-year period is expected to decrease available P in soil due to the enhanced uptake of available P by plants; (2) a long-term 11-year canopy N addition is expected to cause a decline in organic P pools because its mineralization is a primary process that provides available P to plants in acidic soils; and (3) the 11-year canopy N addition resulted in a decrease in both organic and available P pools, ultimately leading to soil P depletion. The findings of our study are expected to challenge the conclusions drawn from previous forest studies that utilized the conventional approach of simulating N deposition effects.

2. Materials and Methods

2.1. Site Description

The Jigongshan National Nature Reserve (114°05′ E, 31°46′ N) is located 38 km south of Xinyang City in Henan Province, China, covering an expansive area of 2917 hectares (Figure 1). The reserve is located on the border of the northern subtropical zone and exhibits climatic characteristics similar to those of warm temperate zones [36]. The soil type is cambisol, characterized by a pH range of 4–5 [38,39]. The annual average temperature stands at 15.3 °C, with July recording the highest monthly average temperature of 27.5 °C and January marking the lowest temperature of 1.9 °C. The annual precipitation is 1102 mm, with a concentration of 80% occurring between April and October. The ambient N deposition in rainfall is 19.7 ± 0.8 kg N ha−1 yr−1, with the NH4+-N content slightly exceeding that of NO3−-N. The forest is 60 years old, and the canopy tree species are dominated by Quercus variabilis, Quercus acutissima, and Liquidambar formosana. The slope direction (southwest) and slope (15–20°) of all plots were basically the same [36].

2.2. Experimental Design

The specific research work was conducted using the internationally renowned field control experimental platform for canopy N addition, which had been established and operational since 2013, garnering widespread acclaim [36]. Canopy N addition was achieved by installing spraying systems on the top of towers. These towers were constructed in the center of canopy N addition treatment plots at a height of 35 m (5–8 m above the forest canopy) to support PVC pipelines with an inner diameter of 10 cm (Figure 1) that were used to transfer the N solution [23,24,36,38,39]. A completely randomized block design was used for the experiment. Four blocks were established, with each block randomly assigned to three circular plots (30 m × 30 m) corresponding to three treatments. A total of 12 plots were constructed. Each plot was surrounded by a >20 m buffer zone. Considering that the background rate of atmospheric N deposition in the study area ranges from 20 to 50 kg N ha−1 yr−1 [36], three N addition gradients were established: control (0 kg N ha−1 yr−1), canopy addition of low N (25 kg N ha−1 yr−1), and canopy addition of high N (50 kg N ha−1 yr−1). The N solution was applied on a monthly basis throughout the growing season, spanning from April to October (a total of seven applications per year). Pristine mountain stream water served as the solvent for NH4NO3 (99.9%), which was used as the N source. Under calm weather conditions with no wind or rain, or a morning or evening wind speed below 1 m/s, the N solution was uniformly sprayed onto the upper portion of the tree canopy [23,24,36,38,39].

2.3. Sample Collection and Processing

Soil samples (0–10 cm) were collected in July, 2023. Five soil cores were randomly obtained from each plot and pooled to obtain composite samples, which were immediately transported to the laboratory. After removing gravel, debris, and other foreign materials, the fine roots of the entire plant were collected for analysis of biomass as well as N and P contents. Soil samples were sieved through a 2 mm mesh and then divided into two equal portions, with one portion of fresh soil being stored at 4 °C in a refrigerator for the determination of soil microbial biomass P (MBP) and phosphatase activities (AcP). Another portion of the soil sample was air-dried and used to determine the fundamental physical and chemical properties of the soil, as well as the different forms of P.
The leaves of Q. acutissima, Q. variabilis, and L. formosana were sampled in July 2023 for analysis of N and P contents. Two trees of comparable height were selected from each species within each plot. Subsequently, three fresh branches were cut from each of the six trees approximately 20 m above the ground and exposed to the sun. Leaves were detached from the twigs and subsequently combined to form a composite sample comprising all three tree species [23,24].

2.4. Measuring In Situ Organic P Mineralization in the Topsoil

An in situ culture method was employed for the investigation of field-based organic P mineralization [44]. First, three points were randomly selected from each plot to remove the litter from the soil surface. Subsequently, three PVC tubes with an inner diameter of 4 cm and a height of 15 cm were inserted perpendicularly into the ground (10 cm below and 5 cm above ground level). The tube walls were perforated with 1 mm holes to prevent soil mineralization in an anaerobic environment. The tube containing the undisturbed soil column was carefully removed, with the top sealed using a breathable and impermeable plastic film and the bottom sealed with absorbent cotton and gauze. Once both ends were securely sealed, the tube was repositioned to its original location, restoring the soil surface to its initial state. Simultaneously, the top 0–10 cm layer of soil was collected 10 cm away from the PVC tube, and the initial organic P content was determined. The tubes were buried on 15 July 2023 and the soil within the tubes was removed on 15 August 2023. Incubated soil from the three tubes was bulked to form one composite sample, sieved through a 2 mm mesh, and subsequently air-dried to determine the organic P content. The organic P mineralization rate refers to the change in soil organic P concentration over a one-month period.

2.5. Soil and Plant Analysis

The soil moisture content was determined using the conventional oven-drying method, wherein 10 g of fresh soil was dried at 105 °C for 24 h. Soil pH was determined using a pH meter, which relied on a 1:2.5 (w/v) soil-to-water solution. Soil organic carbon (SOC) was quantified via dichromate oxidation, while soil total nitrogen (TN) was determined via ultraviolet spectrophotometry following Kjeldahl digestion [45,46,47]. Soil ammonium (NH4+) and nitrate (NO3−) were extracted using a 2 M KCl solution, followed by quantification using flow injection analysis in an autoanalyzer (FIA, Lachat Instruments, Milwaukee, WI, USA). Soil available nitrogen (AN) was determined as the combined concentration of NH4+ and NO3−. Total soil P was determined colorimetrically following the digestion of air-dried soil (<0.15 mm) in a mixture of HClO4 and H2SO4 [46,47]. Inorganic P was extracted by shaking 1 g of air-dried sample (<2 mm) for 16 h in 50 mL of 0.5 M H2SO4, followed by colorimetric quantification of phosphate ions in the resulting filtrates [46,48]. Soil organic P was defined as the residual P after subtracting the inorganic P from the total P. The Bray-1 method, also known as the 0.025 M HCl + 0.03 M NH4F method, was used to determine the available P in the soil [46]. The chloroform fumigation–0.03 M NH4F + 0.025 M HCl–extraction method was employed to quantify soil microbial biomass P (MBP) [49,50]. The activity of acid phosphatases (AcP) was determined using the p–nitrophenyl phosphate method [44,46,47]. The P content in the leaf and fine root samples was quantified using the molybdate blue colorimetric method following digestion in H2SO4–H2O2. The N content of the leaf and fine root samples was determined using a high-capacity element analyzer (vario MACRO cube, Elementar, Hanau, Germany). Soil cation exchange capacity (CEC) was determined using a continuous FIA after ammonium acetate extraction [51]. Soil exchangeable base cations were quantified using the ammonium acetate extraction method, and base saturation (BS) was calculated as the percentage of total exchangeable base cations to CEC [10,51]. The determination of soil exchangeable cations Al and Fe was conducted according to the methods outlined by Hendershot et al. [52].

2.6. Data Analysis

Statistical analysis of the data was performed using SPSS software (version 22.0; SPSS, Inc., Chicago, IL, USA). Prior to the analysis, all data underwent normality testing. The effects of N addition on soil characteristics, soil microorganisms, and N and P contents in plant samples were examined using one-way ANOVA and the LSD multiple comparison method (p < 0.05). Pearson correlation analysis was employed to examine the interrelationships among relevant indicators, whereas Origin 2018 and ArcGIS10.8 software were used for data visualization.

3. Results

3.1. Basic Soil Properties, Leaves, and Fine Roots

The pH, CEC, and BS of the 0–10 cm soil layer were substantially diminished as a result of canopy N addition. Canopy N addition significantly increased the SOC, total N, available N, soil exchangeable Fe and Al, and the stoichiometric ratios of C, N, and P. Canopy N addition did not result in a significant change in the content of inorganic P, but it significantly decreased the levels of total, organic, and available P (Table 1). Canopy N addition significantly enhanced leaf N and P contents, while concurrently reducing leaf N:P (Table 2). Moreover, it led to a significant increase in both the P content and biomass of the fine roots, whereas the N content and N:P ratio of the fine roots exhibited opposite trends (Table 3).

3.2. Soil Phosphorus Fractions and Stocks

Canopy N addition significantly increased MBP content but did not have any marked effects on inorganic P content or the ratio of inorganic P to Total P (Figure 2c,e and Figure 3b). Generally, the levels of Total P, organic P, and available P, as well as the proportion of organic P to Total P, all exhibited a decreasing trend with increasing N addition rates, reaching significant differences under the 50 kg N ha−1 yr−1 addition rate (Figure 2a,b,d and Figure 3a).
The stocks of total P, organic P, and available P in the 0–10 cm soil layer decreased significantly with increasing N addition rates (Figure 4a–c). Specifically, under a 25 kg N ha−1 yr−1 addition rate, the total P stock decreased by 8.75%, whereas under a 50 kg N ha−1 yr−1 addition rate, it decreased by 20.38%.

3.3. Soil Acid Phosphatase (AcP) Activity and Organic P Mineralization

AcP activity and the rate of organic P mineralization increased with the rate of canopy N addition (Figure 5a,b). Notably, under a 50 kg N ha−1 yr−1 addition rate, the AcP activity and organic P mineralization rate substantially increased by 23.2% and 45.7%, respectively.

3.4. Correlation Analysis among Factors

Pearson’s correlation analysis revealed a negative correlation between leaf P and total, organic, and available P contents (Figure 6d,f,h). Moreover, a significant negative correlation was observed between fine root P, soil total P, and organic P (Figure 6e,i). However, a significant non-linear negative correlation was observed between fine root P and available P (Figure 6g).

4. Discussion

4.1. Effects of Canopy N Addition on Leaves and Fine Root Nutrients

Nitrogen (N) and phosphorus (P) are essential constituents of various proteins and genetic material in organisms [53,54]. N and P play crucial regulatory roles in plant growth and physiological metabolism [32,44,55]. Specifically, the synergistic interaction between N and P strongly influenced individual plant functions and the overall ecosystem [3,20]. The present study revealed a marginal increase in leaf N and P contents due to canopy N addition, whereas the N:P ratio of the leaves exhibited a significant decrease. This study employed canopy N addition to simulate atmospheric N deposition, distinguishing it from previous studies on this topic. Within forest ecosystems, most settled reactive N initially traverses the forest canopy, where it can be assimilated by foliage or fixed by tree canopy biota prior to its eventual arrival at the forest floor [56,57,58]. The results of a 15N tracer study revealed that most of the intercepted N was initially absorbed by the leaves and subsequently stored within the plants. Furthermore, the N addition treatment was observed to significantly augment the vegetation N pool by 120%–412% in comparison to the control group [41]. The forest ecosystem in this region, which has experienced prolonged N-limitation during plant growth, can benefit from increased leaf N content by promoting plant growth, enhancing aboveground biomass, and improving forest productivity [59,60]. Plant growth necessitates the maintenance of a specific N:P ratio; therefore, N deposition can augment the demand for P in plants and subsequently increase the leaf P content. The stoichiometric ratio of plant leaves varies with season and tree species [61]. However, when the N:P ratio falls below 14, it indicates N limitation; when it exceeds 16, it suggests P limitation; when it lies between these two values, it implies co-limitation by both N and P [62,63]. In this study, the leaf N:P range was found to be 18.03–19.67, indicating that plant growth in this area is still limited by P. The canopy N addition resulted in a significant reduction in the leaf N:P ratio, potentially owing to the promotion of plant uptake of P from the soil, particularly in forest ecosystems with limited P availability. Plants are more deficient in P than in N during growth, and P content increases at a faster rate than N content.
Some studies have indicated that plants may enhance the uptake of soil P under conditions of limited P availability by modifying root characteristics owing to the low fluidity and solubility of soil P [35,64,65]. For instance, Lin et al. [66] reported that N application could augment the plant capacity for P absorption by increasing root biomass, which aligns with our own research findings (Table 3). The following factors can account for these observations: First, the presence of high N levels typically induces oxidative or respiratory stress in fine root tissue, resulting in a negative correlation between fine root biomass and fine root N content [67,68,69]. In our study, the canopy N addition led to a reduction in the N content of fine roots, with a moderate decrease in N concentration within the fine root tissue, proving more advantageous for both fine root growth and P absorption. Second, the addition of N to the canopy can enhance the allocation of leaf photosynthetic products to fine roots [70,71], thereby promoting root C investment (e.g., increasing root biomass) and improving plant P uptake efficiency. Third, the canopy N addition, as compared to traditional understory N addition, may potentially retard the dissolution of exchangeable Fe/Al in soil [23,24]. Consequently, the reduction in Fe/Al ions facilitates P uptake by plants [68,72,73], leading to an increase in P content within leaves and fine roots while simultaneously reducing the N:P ratio of plants.

4.2. Effects of Canopy N Addition on Soil P Fractions and Stocks

The biogeochemical cycle of P in natural ecosystems differs from that of C and N, as the latter primarily originate from atmospheric sources through processes such as photosynthesis by plants, biological fixation, and abiotic deposition [44]. Throughout the process of ecosystem succession, P undergoes depletion due to factors such as the removal of plant biomass, leaching, and erosion [32,44,74]. In this study, canopy N addition had a significant impact on both soil total P and its individual fractions (Figure 1). Specifically, the canopy addition of high-N (50 kg ha−1 yr−1) resulted in a notable decrease in soil total P content by 4.68% and a substantial reduction in total P stock by 20.38% (Figure 4). These findings suggest that canopy N addition for 11 years altered the balance between P input and output within the soil system. The input of P into the soil is primarily determined by the atmospheric deposition of P and the return of aboveground litter in forest ecosystems [75,76,77]. In contrast to the N cycle, the P cycle lacks a gaseous form [44,78]. Therefore, the input of external P into forest ecosystems primarily relies on mineral dust deposition, which is significantly lower than N deposition [63,75,78] (the ratio of reactive N and P inputs via atmospheric deposition ranges from 44:1 to 47:1). This indicated that atmospheric P deposition was negligible. The findings of relevant studies suggest that in P-deficient ecosystems, the primary mechanism for meeting the demand for P required for plant growth is by enhancing biological and geochemical processes within the ecosystem, such as plant P resorption and soil organic P mineralization [32,79]. This approach has proven to be more effective than modifying the P flux, such as litter P mineralization, or promoting energy-intensive pathways, such as increasing the abundance of mycorrhizal fungi [53,80,81]. The study conducted by Peng et al. [82] investigated four forest ecosystems spanning the cold temperate, warm temperate, subtropical, and tropical zones and analyzed the leaves of 47 tree species. These findings revealed that plants employ internal nutrient retention as a strategy to optimize their nutrient supply. Approximately 98% of the P required for plant growth in forest ecosystems is derived from two processes: P resorption prior to leaf litter formation [17,18] and organic P mineralization [15,65]. Consequently, we propose that, owing to the influence of plant P resorption, the P returned via the decomposition of leaf litter is insufficient to disrupt the net balance of the soil P cycle. The addition of N has been extensively studied and has been consistently shown to enhance plant photosynthesis, augment net primary productivity, and stimulate P demand in plants [32,83,84]. In the present study, soil P mineralization exhibited a corresponding increase with the addition of N to the canopy. In general, a higher net mineralization rate of P is typically associated with an increased availability of P in the soil [85]. However, contrary to expectations, this study revealed a significant decrease in the availability of P. Furthermore, correlation analysis demonstrated a substantial negative relationship between the availability of P in the soil and the contents of leaf and root P (Figure 6), which supports the hypothesis (I) that canopy N addition leads to reduced soil available P owing to enhanced plant uptake. In conclusion, the soil system obtained a limited amount of P from plant litter, whereas the atmospheric P input remained relatively low. Therefore, the excessive accumulation of P in plant biomass may lead to soil P depletion (Figure 4). Naturally, the potential impact of leaching and runoff cannot be disregarded because of the 15–20° slope of our sample plot and the high precipitation levels in the area [86].
In this study, the canopy N addition did not significantly affect the inorganic P content or its proportion to total P, whereas a significant decrease in organic P content, its proportion to total P, and organic P stock was noted (Figure 2, Figure 3 and Figure 4). The findings presented here are consistent with those reported by Fan et al. [15], suggesting that the deposition of N does not disrupt the equilibrium between dissolution and fixation of inorganic P in soil. Although soil acidification enhances the dissolution of inorganic P, as soil pH decreases, there is an increasing binding of soil available P with Al or Fe oxides. The decrease in available P content in the soil further stimulates mineral dissolution, such as apatite, leading to increased P release. The outcome is a harmonious equilibrium between the release and immobilization of P. We believe this could be a significant factor contributing to the unchanged levels of inorganic P content in the soil [32]. The availability of soil P primarily relies on organic P mineralization when P released from soil through inorganic P dissolution and desorption is insufficient [87,88,89,90]. These results corroborate hypothesis (II) that canopy N addition induces a reduction in organic P, as the mineralization of organic P is the main pathway by which plants acquire P from acidic soils. A study conducted by Yu et al. [32] in a South Asian tropical forest revealed that, owing to the strong fixation of inorganic P in highly weathered acidic soils, soil organic P mineralization plays a pivotal role in maintaining an adequate supply of available P during N deposition. A study conducted by Fan et al. [10] in a subtropical Castanopsis carlesii natural forest demonstrated the pivotal role of moderately labile organic P in maintaining soil P availability. The study conducted by Heuck et al. [91] revealed a significant decrease in the content of moderately labile organic P in both temperate broadleaf and coniferous forests as a result of N application. Consequently, the mineralization of organic P may serve as the fundamental basis for maintaining soil P availability and play a pivotal role, particularly when the availability of inorganic P in the soil is limited [92].

4.3. Effects of Canopy N Addition on Soil Organic P Mineralization

The process of soil organic P mineralization is primarily governed by the activity of soil enzymes, the presence and function of soil microorganisms, and the physical and chemical properties inherent to the soil [44,93,94]. The rate of organic P mineralization generally exhibits a positive correlation with AcP, MBP, and root biomass in the soil [44]. A greater root biomass generally corresponds to enhanced root activity (e.g., increased secretion of enzymes and exudates) and heightened microbial activity in the rhizosphere [95,96]. Microbes serve as sources and sinks of P in the soil and are directly involved in P mineralization [97,98]. In addition to mycorrhiza and roots, soil microbes also engage in the synthesis of phosphatases and phytases [99]. The results of this study show that adding N to the canopy substantially increases the fine root biomass (Table 3), AcP, and MBP content in soil, thereby facilitating the mineralization of organic P to meet plant P requirements (Figure 2 and Figure 5). Consequently, prolonged N addition may deplete substantial amounts of organic and available P in the soil (Figure 4), potentially compromising the sustainable provision of high-quality soil P within the region. The findings align with hypothesis (III).
Soil phosphatase plays a pivotal role in driving the mineralization of soil P [100]. Phosphatases are N-rich molecules [101,102] and canopy N addition enhances the availability of soil N, thereby promoting soil phosphatase synthesis. The study conducted by Marklein and Houlton [19] revealed that an augmentation in soil N availability could elicit a heightened allocation of energy and resources for the synthesis of phosphatase enzymes by plant roots and microbes. In this study, the canopy N addition significantly augmented the soil available N content (Table 1) while also inducing a substantial increase in soil AcP activity (Figure 5). These findings are consistent with those of previous studies [10,15,33], which suggest that the elevation of AcP activity resulting from N addition contributes to organic P mineralization. Soil MBP serves as a crucial reservoir of soil P [44], actively participating in the biogeochemical cycling of this element and supplying it to plants. In scenarios where soil P becomes a limiting factor for plant growth, soil microbes can fulfill the P requirements of plants by expediting P cycling and reducing P immobilization by microorganisms themselves [91,102]. The present study revealed a substantial increase in soil MBP content attributable to canopy N addition, implying that heightened soil MBP resulting from N deposition stimulates soil organic P mineralization. Comparable findings have been documented for other P-deficient subtropical forest soils, suggesting a potential strategy employed by natural ecosystems to counteract P deficiency. In conclusion, canopy N addition directly enhances soil microbial biomass (e.g., MBP) and acid phosphatase activity, indirectly stimulating organic P mineralization in the soil. Consequently, the soluble P content in soil is increased, and the risk of P loss is elevated, which may be a notable factor contributing to soil P depletion.

5. Conclusions

The simulation of atmospheric N deposition based on canopy manipulation can provide a more accurate representation of the natural N deposition process in the atmosphere, thereby objectively elucidating the potential impact of N deposition on the P cycle of the northern subtropical forest ecosystem. The findings of our research indicate that the augmentation of N deposition enhances the mineralization of organic P through the stimulation of phosphatase and microbial activities in the soil, thereby enhancing P availability, fulfilling plant requirements, and mitigating P limitation (Hypothesis II). Meanwhile, the increase in N deposition remarkably enhanced the P demand of the plants (Hypothesis I); however, no significant increase was observed in the P content of the litter. Consequently, the limited return of P to the soil from the litter further intensifies soil P consumption (Hypothesis III). In the long term, the substantial reduction in potentially available soil P resulting from N deposition may exacerbate P limitation in the region, thereby negatively affecting forest ecosystem productivity (Figure 7).

Author Contributions

Conceptualization, Methodology, Formal analysis, Investigation, Writing–original draft, Visualization, Funding acquisition, X.G.; Conceptualization, Investigation, Validation, Formal analysis, Data curation, Visualization, Resources, Y.G.; Project administration, X.L.; Project administration, Funding acquisition, C.Z.; Visualization, Q.Z.; Visualization, X.Y.; Writing–review and editing, Funding acquisition, Y.C.; Resources, Y.Y.; Supervision, Project administration, S.F. All authors have read and agreed to the published version of the manuscript.

Funding

This research was financially supported by grants from the Key Research Program Foundation of Higher Education of Henan Province (No. 24A180027 and No. 24B420003), the China Postdoctoral Science Foundation (No. 2023M741727), the Xinyang Academy of Ecological Research Open Foundation (No. 2023XYQN14), the Postdoctoral Research Foundation of Henan Province (No. 202103058), the Science &Technology Development Program of Henan Province (No.222102320082), and the National Natural Science Foundation of China (No.32371846).

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data is not publicly available due to privacy restrictions.

Acknowledgments

We thank the Henan Dabieshan National Field Observation and Research Station of the Forest Ecosystem. The authors also thank Chuang Wang, Shengqi Tang, and Yulong Bai for their assistance in the field.

Conflicts of Interest

The author hereby declares that there is no conflict of interest.

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Forests 15 00416 g001
Figure 1. Geographical location of the experimental site. The lower right corner shows a canopy addition of N (Photograph sourced from the official website of the Henan Dabieshan National Field Observation and Research Station of Forest Ecosystem).
Figure 1. Geographical location of the experimental site. The lower right corner shows a canopy addition of N (Photograph sourced from the official website of the Henan Dabieshan National Field Observation and Research Station of Forest Ecosystem).
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Figure 2. Variations in five soil P fraction contents (total P (a), organic P (b), inorganic P (c), available P (d), and microbial biomass P (MBP) (e) at 0–10 cm depth) after 11-year canopy addition of N in a typical N-limited northern subtropical forest in central China. Values are presented as means ± standard errors (n = 4). Different lowercase letters above the bars indicate statistically significant differences among the N-addition treatments (LSD test, p < 0.05). N treatments were implemented from 2013 to 2023, encompassing a control (0 kg N ha−1 yr−1), as well as the canopy addition of N at a rate of 25 kg ha−1 yr−1 or 50 kg ha−1 yr−1.
Figure 2. Variations in five soil P fraction contents (total P (a), organic P (b), inorganic P (c), available P (d), and microbial biomass P (MBP) (e) at 0–10 cm depth) after 11-year canopy addition of N in a typical N-limited northern subtropical forest in central China. Values are presented as means ± standard errors (n = 4). Different lowercase letters above the bars indicate statistically significant differences among the N-addition treatments (LSD test, p < 0.05). N treatments were implemented from 2013 to 2023, encompassing a control (0 kg N ha−1 yr−1), as well as the canopy addition of N at a rate of 25 kg ha−1 yr−1 or 50 kg ha−1 yr−1.
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Figure 3. Percentages of organic P (a) and inorganic P (b) in total P after 11-year canopy addition of N in a typical N-limited northern subtropical forest in central China. Values are presented as means ± standard errors (n = 4). Different lowercase letters above the bars indicate statistically significant differences among the N-addition treatments (LSD test, p < 0.05). N treatments were implemented from 2013 to 2023, encompassing a control (0 kg N ha−1 yr−1), as well as the canopy addition of N at a rate of 25 kg ha−1 yr−1 or 50 kg ha−1 yr−1.
Figure 3. Percentages of organic P (a) and inorganic P (b) in total P after 11-year canopy addition of N in a typical N-limited northern subtropical forest in central China. Values are presented as means ± standard errors (n = 4). Different lowercase letters above the bars indicate statistically significant differences among the N-addition treatments (LSD test, p < 0.05). N treatments were implemented from 2013 to 2023, encompassing a control (0 kg N ha−1 yr−1), as well as the canopy addition of N at a rate of 25 kg ha−1 yr−1 or 50 kg ha−1 yr−1.
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Figure 4. Soil total (a), organic (b), and available (c) P stocks at 0–10 cm depth after 11-year canopy addition of N in a typical N-limited northern subtropical forest in central China. Values are presented as means ± standard errors (n = 4). Different lowercase letters above the bars indicate statistically significant differences among the N-addition treatments (LSD test, p < 0.05). N treatments were implemented from 2013 to 2023, encompassing a control (0 kg N ha−1 yr−1), as well as the canopy addition of N at a rate of 25 kg ha−1 yr−1 or 50 kg ha−1 yr−1.
Figure 4. Soil total (a), organic (b), and available (c) P stocks at 0–10 cm depth after 11-year canopy addition of N in a typical N-limited northern subtropical forest in central China. Values are presented as means ± standard errors (n = 4). Different lowercase letters above the bars indicate statistically significant differences among the N-addition treatments (LSD test, p < 0.05). N treatments were implemented from 2013 to 2023, encompassing a control (0 kg N ha−1 yr−1), as well as the canopy addition of N at a rate of 25 kg ha−1 yr−1 or 50 kg ha−1 yr−1.
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Figure 5. Acid phosphatase activity (AcP) (a) and net organic P mineralization rate (b) at 0–10 cm soil depth in a typical N-limited northern subtropical forest in central China after 11-year canopy addition of N. Values are presented as means ± standard errors (n = 4). Different lowercase letters above the bars indicate statistically significant differences among the N-addition treatments (LSD test, p < 0.05). N treatments were implemented from 2013 to 2023, encompassing a control (0 kg N ha−1 yr−1), as well as the canopy addition of N at a rate of 25 kg ha−1 yr−1 or 50 kg ha−1 yr−1.
Figure 5. Acid phosphatase activity (AcP) (a) and net organic P mineralization rate (b) at 0–10 cm soil depth in a typical N-limited northern subtropical forest in central China after 11-year canopy addition of N. Values are presented as means ± standard errors (n = 4). Different lowercase letters above the bars indicate statistically significant differences among the N-addition treatments (LSD test, p < 0.05). N treatments were implemented from 2013 to 2023, encompassing a control (0 kg N ha−1 yr−1), as well as the canopy addition of N at a rate of 25 kg ha−1 yr−1 or 50 kg ha−1 yr−1.
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Figure 6. Relationships between organic P and total, available, microbial biomass, leaf, and fine-root P (a–e); between available P and leaf, fine-root P (f,g); between total P and leaf, fine-root P (h,i) in a typical N-limited northern subtropical forest in central China. All the correlation coefficients are statistically significant differences (p < 0.05).
Figure 6. Relationships between organic P and total, available, microbial biomass, leaf, and fine-root P (a–e); between available P and leaf, fine-root P (f,g); between total P and leaf, fine-root P (h,i) in a typical N-limited northern subtropical forest in central China. All the correlation coefficients are statistically significant differences (p < 0.05).
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Figure 7. The impact of an 11-year canopy addition of N on P fractions and transformations. A potential pathway to sustain increased P demand under N deposition in a typical N-limited northern subtropical forest in central China is depicted. The size of the circle corresponds to the P fraction content. The up-and down-pointing arrows indicate an increasing and decreasing trend, respectively. The red horizontal line indicates no alteration. The arrow width indicates the magnitude of the impact. AP, available P; MBP, microbial biomass P; L-OP, labile organic P; ML-OP, moderately labile organic P; Fe/P/Al, Fe/Al bound inorganic P. (1) The increased plant P content with rapid plant growth under N deposition is supported by the enhanced plant P uptake; (2) Soil P supply was dominated by organic P mineralization under N deposition, as reflected by an increase in soil acid phosphatase activity and the co-occurrence of decreases in organic P; (3) The unchanged inorganic P at the 0–10 cm soil depth indicates P release from Fe/Al-bound inorganic P was not an important P source for plant uptake.
Figure 7. The impact of an 11-year canopy addition of N on P fractions and transformations. A potential pathway to sustain increased P demand under N deposition in a typical N-limited northern subtropical forest in central China is depicted. The size of the circle corresponds to the P fraction content. The up-and down-pointing arrows indicate an increasing and decreasing trend, respectively. The red horizontal line indicates no alteration. The arrow width indicates the magnitude of the impact. AP, available P; MBP, microbial biomass P; L-OP, labile organic P; ML-OP, moderately labile organic P; Fe/P/Al, Fe/Al bound inorganic P. (1) The increased plant P content with rapid plant growth under N deposition is supported by the enhanced plant P uptake; (2) Soil P supply was dominated by organic P mineralization under N deposition, as reflected by an increase in soil acid phosphatase activity and the co-occurrence of decreases in organic P; (3) The unchanged inorganic P at the 0–10 cm soil depth indicates P release from Fe/Al-bound inorganic P was not an important P source for plant uptake.
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Table 1. Effects of 11-year canopy addition of N on basic soil physicochemical properties in a typical N-limited northern subtropical forest in central China.
Table 1. Effects of 11-year canopy addition of N on basic soil physicochemical properties in a typical N-limited northern subtropical forest in central China.
Soil PropertiesCanopy N Addition Rate (kg N ha−1 yr−1)
02550p
pH4.23 ± 0.05 a4.14 ± 0.02 a4.05 ± 0.02 b0.009
Soil moisture (%)17.75 ± 1.17 a18.13 ± 0.79 a19.19 ± 1.04 a0.599
SOC (g kg−1)22.33 ± 1.14 c29.16 ± 0.95 b36.6 ± 2.35 a0.001
Total N (g kg−1)2.18 ± 0.12 b2.34 ± 0.03 ab2.40 ± 0.06 a0.182
Available N (mg kg−1)27.66 ± 0.82 b28.79 ± 0.51 b31.66 ± 0.49 a0.004
Total P (g kg−1)545.16 ± 8.81 a541.65 ± 10.02 ab520.78 ± 6.86 b0.157
Organic P (g kg−1)167.46 ± 5.03 a151.97 ± 5.02 b143.39 ± 3.64 b0.015
Inorganic P (g kg−1)377.71 ± 6.24 a389.68 ± 7.91 a377.39 ± 4.39 a0.340
Available P (g kg−1)12.21 ± 0.91 a9.08 ± 0.90 b6.63 ± 0.53 c0.003
C/N10.30 ± 0.68 b12.48 ± 0.55 b15.31 ± 1.24 a0.010
C/P40.98 ± 2.15 c53.9 ± 2.13 b70.48 ± 5.31 a0.001
N/P4.01 ± 0.23 b4.32 ± 0.11 ab4.61 ± 0.06 a0.053
Fe (×10−3 cmol(+) kg−1)2.46 ± 0.09 b3.06 ± 0.09 ab3.24 ± 0.11 a0.001
Al (cmol(+) kg−1)2.39 ± 0.15 b3.14 ± 0.08 a3.50 ± 0.14 a0.001
CEC (mmol(+) kg−1)77.35 ± 0.95 a73.29 ± 2.15 b70.69 ± 0.6 b0.025
BS (%)61.65 ± 1.6 a60.94 ± 0.49 ab58.49 ± 0.7 b0.136
Values are presented as means ± standard errors (n = 4). Means in a row followed by different letters exhibit significant differences (p < 0.05), as determined by the LSD test. N treatments were implemented from 2013 to 2023, encompassing a control (0 kg N ha−1 yr−1) as well as the canopy addition of N at a rate of 25 kg ha−1 yr−1 or 50 kg ha−1 yr−1. CEC, cation exchange capacity; BS, base saturation. Available N is the sum of the concentrations of NH4+ and NO3−.
Table 2. Effects of 11-year canopy addition of N on leaf N and P content, as well as the leaf N:P ratio in a typical N-limited northern subtropical forest in central China.
Table 2. Effects of 11-year canopy addition of N on leaf N and P content, as well as the leaf N:P ratio in a typical N-limited northern subtropical forest in central China.
Plant OrganCanopy N Addition RateN (g kg−1)P (g kg−1)N/P
Leaf0 (kg N ha−1 yr−1)22.01 ± 0.69 b1.12 ± 0.05 c19.67 ± 0.83 a
25 (kg N ha−1 yr−1)22.72 ± 0.86 ab1.24 ± 0.02 b18.33 ± 0.70 ab
50 (kg N ha−1 yr−1)24.73 ± 0.81 a1.37 ± 0.03 a18.03 ± 0.57 b
Values are presented as means ± standard errors (n = 4). Means in a row followed by different letters exhibit significant differences (p < 0.05), as determined by the LSD test. N treatments were implemented from 2013 to 2023, encompassing a control (0 kg N ha−1 yr−1) as well as the canopy addition of N at a rate of 25 kg ha−1 yr−1 or 50 kg ha−1 yr−1.
Table 3. Effects of 11-year canopy addition of N on fine-root N content, P content, N:P ratio, and standing biomass in a typical N-limited northern subtropical forest in central China.
Table 3. Effects of 11-year canopy addition of N on fine-root N content, P content, N:P ratio, and standing biomass in a typical N-limited northern subtropical forest in central China.
Plant OrganCanopy N Addition RateN (g kg−1)P (g kg−1)N/PBiomass (g m−2)
Fine-root0 (kg N ha−1 yr−1)12.88 ± 0.64 a0.70 ± 0.08 b19.33 ± 2.68 a184.80 ± 1.78 c
25 (kg N ha−1 yr−1)11.53 ± 0.30 ab0.71 ± 0.04 b16.43 ± 0.78 a198.29 ± 1.50 b
25 (kg N ha−1 yr−1)10.21 ± 0.59 b1.08 ± 0.08 a9.54 ± 0.33 b226.82 ± 2.35 a
Values are presented as means ± standard errors (n = 4). Means in a row followed by different letters exhibit significant differences (p < 0.05), as determined by the LSD test. N treatments were implemented from 2013 to 2023, encompassing a control (0 kg N ha−1 yr−1), as well as the canopy addition of N at a rate of 25 kg ha−1 yr−1 or 50 kg ha−1 yr−1.
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Gao, X.; Gao, Y.; Li, X.; Zhang, C.; Zeng, Q.; Yuan, X.; Chen, Y.; Yu, Y.; Fu, S. Eleven-Year Canopy Nitrogen Addition Enhances the Uptake of Phosphorus by Plants and Accelerates Its Depletion in Soil. Forests 2024, 15, 416. https://doi.org/10.3390/f15030416

AMA Style

Gao X, Gao Y, Li X, Zhang C, Zeng Q, Yuan X, Chen Y, Yu Y, Fu S. Eleven-Year Canopy Nitrogen Addition Enhances the Uptake of Phosphorus by Plants and Accelerates Its Depletion in Soil. Forests. 2024; 15(3):416. https://doi.org/10.3390/f15030416

Chicago/Turabian Style

Gao, Xiaoli, Yinmei Gao, Xiaowei Li, Chenlu Zhang, Quanxin Zeng, Xiaochun Yuan, Yuehmin Chen, Yuanchun Yu, and Shenglei Fu. 2024. "Eleven-Year Canopy Nitrogen Addition Enhances the Uptake of Phosphorus by Plants and Accelerates Its Depletion in Soil" Forests 15, no. 3: 416. https://doi.org/10.3390/f15030416

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