INTRODUCTION

Phosphorus (P) is an element that is essential for plant growth and development [11]. The P required by plants is obtained mainly from the soil P pool [24]. Soil organic P is an important component of soil P, generally accounting for 20–80% of the total soil P, and can reach up to 95% [7, 21–23, 26, 30]. With the development of organic agriculture and ecological agriculture, more attention is being paid to soil organic P in soil science and plant nutrition. Compared with inorganic P levels in soil, the levels of organic P could shift easily [26]. Some organic P compounds entering the rhizosphere of crops can be absorbed directly by plants [21, 27]. Most organic P can be mineralized gradually into inorganic P, particularly microorganism P, which is mineralized easily, and, therefore, is a vital source of soil available P [15, 28]. Consequently, the forms and shifts in soil organic P influence soil P supply capacity in a soil and plant P nutrition [3, 4]. Studying soil organic P dynamics enhances our understanding of the P cycle in soil-plant systems [3, 9, 15].

Soil aggregates represent soil mass, soil blocks, or soil aggregates with different sizes, shapes, and properties, which are the basic units of soil structure. Different aggregate sizes interact with soil P or fertilizer P differently, in turn, influencing the establishment of soil available P pools and soil P availability to plants, and are directly linked to the potential soil nutrient supply [1, 8, 18]. The results [6] of a 14-year field experiment carried out on yellow-brown soil revealed that the order of the concentrations of organic P in different soil aggregate fractions was 0–0.002 mm > 0.002–0.01 mm > 0.05–0.1 mm > 0.01–0.05 mm. According to Cha et al. [5], labile organic P was distributed mainly in the <0.01 mm and 0.05–0.25 mm aggregate size fractions, and moderately labile organic P, moderately stable organic P, and highly stable organic P were distributed mainly in the <0.01 mm aggregate fraction. Wen et al., [25] observed that in large aggregates (>2 mm), the concentrations of moderately stable and highly stable organic P were higher, and in >2 mm or <0.5 mm aggregates, the concentrations of labile and moderately labile organic P were higher. However, the findings of Wu et al. [29] are slightly inconsistent with the results of other studies. The labile organic P and moderately labile organic P are distributed mainly in small-sized aggregates, and moderately stable organic P is mainly distributed the 2–5 mm and the <0.5 mm aggregate size fractions. The concentrations of highly stable organic P with high stability are the highest in the >2 mm fractions, there are more stable organic P concentrations in large aggregates and more effective organic P in small aggregates. However, the distribution characteristics of various forms of organic P in brown desert soil aggregates in soil under 10–14 years of cultivation in the south of Xinjiang revealed that they decrease with an increase in aggregate size fractions, and the diameters of most aggregates are mostly less than 0.1 mm [14]. Based on the results, different aggregate fractions have different capacities to retain organic P, and the distributions of organic P in different aggregate fractions are not similar due to differences in soil type, climate, and other conditions, which require further investigations.

Although the total area of the apple-pear orchard in the present study is relatively small, it offers a unique land use model for studying agricultural ecosystems in the cold regions of North China. The distribution, mineralization, and transformation processes of soil organic P in the Yanbian apple-pear orchard are different from those in other orchards considering the specific climatic conditions and pear varieties. Therefore, a study on the distribution characteristics of soil organic P in different soil fractions would provide insights on P cycles in northern orchards in China and provide a valuable reference for soil management in apple-pear orchards.

OBJECTS AND METHODS

Sampling points were located in apple-pear orchard, Hualong fruit farm, Longjing City, Yanbian Prefecture (N: 41°59–44°30, E: 127°27–131°18), in the Xitian Plain, at an altitude of approximately 280 m. The soil type is Haplic Luvisols. Clean tillage is adopted between rows of orchards, with no irrigation, in addition to good management practices. Urea, diammonium phosphate, and potassium sulfate are the major fertilizers applied in the orchard, and an N : P2O5 : K2O ratio of 1 : 0.5 : 0.04 was applied.

Soil samples were collected in the orchard from April 29 to May 2 in spring, July 28 to July 29 in summer, and October 15 to October 17 in autumn in 2015. 11, 25, 40, and 63 year-old apple-pear trees with good growth were selected randomly, and sampling points were set 1 m from the trunk while avoiding fertilization points. There were five sampling points in the fruit-tree area for each planting year group based on the five-spot-sampling method, yielding 25 sampling points. In spring, summer, and autumn, three undisturbed soil samples were collected from the 0–20 cm, 20–40 cm, and 40–60 cm soil layers in each sampling point, yielding 225 soil samples.

According to the method of Shavinov [10], the collected soil mass was broken into smaller pieces with 10–12 mm diameter along its natural structural fracture, and then air dried, and then soil aggregates of different fractions were determined by dry sieving. Soil (100–200 g) was obtained and put in a sieve with a diameter of 20 cm and sieved sequentially using 10 mm, 7 mm, 5 mm, 3 mm, 2 mm, 1 mm, 0.5 mm and 0.25 mm screens (with covers at the tops and at the bottoms). We divided the tested soil into aggregate fractions based on the following aggregate diameters: >10, 7–10, 5–7, 3–5, 2–3, 1–2, 0.5–1, 0.25–0.5 and <0.25 mm. In addition, we determined the mass of air-dried soil in each aggregate fraction, and calculated the percentage concentrations of soil aggregates in each soil fraction. The improved Bowman-Cole method was used for the determination of organic P components in aggregates [2, 31]. The improved Bowman-Cole method consisted of the following steps: (1) to the soil pretreated with chloroform, 0.5 mol L–1 of NaHCO3 were added with ultrasonic treatment for 10 minutes followed by oscillation for 30 minutes to extract the labile organic P into the supernatant; (2) to the soil left after the initial extraction, 0.1 mol L–1 of NaOH was added with ultrasound for 10 minutes followed by oscillating for 4 hours to leach the stable and the moderately labile organic P fractions into the alkali solution; (3) to the above alkali supernatant, acid was added to adjust the pH to 3.00 to precipitate the highly stable organic P and allow the moderately stable fraction remain in the solution and finally; (4) to the soil, 1 mol L–1 of H2SO4 was added with a constant oscillation for 3 hours to extract the moderately labile organic P. Compared with the original method, the current test method appeared to have optimized the conditions with improved efficiency.

IBM SPSS Statistics 20.0 (IBM, Armonk, NY, USA) and MS Excel 2016 (Microsoft Corp., Redmond, WA, USA) were used for calculations and statistical analyses. Multiple comparisons were performed using Duncan’s new multiple range test (α = 0.05). The data in the table are presented as estimated marginal means.

RESULTS AND DISCUSSION

The concentrations of labile organic P in the 0–20, 20–40, and 40–60 cm layers of plants with different planting years in spring, summer, and autumn have been plotted as column charts based on the different aggregate fractions (Figs. S1–S3). Analysis of variance (ANOVA) results of the labile organic P data revealed that the effects of four factors, including planting year, soil layer, season, and aggregate fraction, in addition to the effects of their interactions on P were best significant (P < 0.01). See Tables 1–4 for further multiple comparison results for each factor.

Table 1.   Distribution of organic phosphorus (mg kg–1) in soil aggregates under orchards with different planting years
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Table 2.   Distribution of organic phosphorus (mg kg–1) in soil aggregates under different soil layers
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Table 3.   Distribution of organic phosphorus (mg kg–1) in soil aggregates under different seasons
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Table 4.   Distribution of organic phosphorus (mg kg–1) in soil aggregates of different fraction
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Labile organic P increased and the decreased in soil aggregates with an increase in planting year (Table 1). In addition, the concentrations of labile organic P were the highest in the 25 and 40-year-old plants, at 10.3 mg kg–1 and 10.2 mg kg–1, respectively, and there were no significant differences between them (P = 0.26), while the concentrations in the two planting years were significantly higher (P < 0.05) than in the 63 and 11-year-old orchards. The concentrations of labile organic P were the lowest in the 11-year-old orchards (8.4 mg kg–1), which were significantly lower (P < 0.05) than in the other orchards. The concentrations of labile organic P in soil aggregates decreased linearly with an increase in soil depth (Table 2), and were 32.1% and 54.1% lower than in the concentrations in the surface layer, with significant differences among different layers (P < 0.05). In addition, the concentrations of labile organic P in soil aggregates in spring were the highest, and decreased slightly in summer (Table 3). There were no significant differences in the concentrations between spring and summer (P = 0.35). In autumn, the concentrations of active organic P decreased to 9.3 mg kg–1, and there were significant differences between the concentrations in spring and in summer (P < 0.05). The concentrations of labile organic P in the <0.25 mm fraction were the highest, reaching 11.6 mg kg–1 (Table 4), and the difference with other fractions was significant (P < 0.05). The second highest concentrations were observed in the 0.25–0.5 mm fraction. The above results show that the labile organic P is enriched relatively easily in small aggregates.

The concentrations of moderately labile organic P in the 0–20 cm, 20–40 cm and 40–60 cm layers in different planting years in spring, summer, and autumn have been plotted as a column chart based on the different aggregate fractions (Figs. S4–S6). The ANOVA results of moderately labile organic P data revealed that the effects of four factors (planting year, soil layer, season, and aggregate fraction) and their interactions were best significant (P < 0.01). Further multiple comparison results for each factor are listed in Tables 1–4.

The concentrations of moderately labile organic P in soil aggregates increased and then decreased with an increased in planting years (Table 1). In 11 years, the concentrations of moderately labile organic P in orchard aggregates were the lowest, at 40.5 mg kg–1, while they were the highest at 25 years, at 106.8 mg kg–1. In addition, the differences in concentrations of moderately labile P were significant among the four orchards (P < 0.05). The concentrations of moderately labile organic P in soil aggregates decreased linearly with an increase in soil depth (Table 2), which was 45.9% and 73.0% lower than the concentrations in the surface layer, with significant differences among different soil layers (P < 0.05). The concentrations of moderately labile organic P in soil aggregates were the lowest in spring (Table 3), at 64.7 mg kg–1, and the highest in summer, at 84.2 mg kg–1. There were significant differences in concentrations of moderately labile P among the three seasons (P < 0.05). The concentrations of moderately labile organic P in the <0.25 mm fraction were the highest (Table 4), reaching 102.4 mg kg–1, followed by the 0.25–0.5 mm fraction, at 89.9 mg kg–1. In addition, there were significant differences between the two fractions, and among all other fractions (P < 0.05). According to the results, moderately labile organic P was enriched relatively easily in small aggregates.

The concentrations of moderately stable organic P in the 0–20 cm, 20–40 cm, and 40–60 cm layers for different planting years in spring, summer, and autumn have been plotted as column charts based on the aggregates of different fractions (Figs. S7–S9). The results of the ANOVA carried out on the moderately stable organic P data showed that the four factors (planting year, soil layer, season, and aggregate fraction) and their interaction influenced moderately stable organic P concentrations significantly (P < 0.01). Additional multiple comparison results for each factor can be viewed in Tables 1–4.

The concentrations of moderately stable organic P increased in soil aggregates first and then decreased with an increase in planting year (Table 1). The concentrations of moderately stable organic P in orchard soil aggregates were the lowest in the 11-year-old plants, at 9.1 mg kg–1, and the highest in the 25-year-old plants, at 10.6 mg kg–1. There were no significant differences in the concentrations of moderately stable organic P in soil aggregates between the 25-year-old and the 40-year-old orchards, and between the 11‑year-old and the 63-year-old plants, and there was a significant difference in the concentrations of moderately stable organic P between orchards of the two groups (P < 0.05). The concentrations of moderately stable organic P in soil aggregates decreased linearly with increase in soil depth (Table 2), which was 32.7% and 43.2% lower than that in the surface layer, with significant differences among the layers (P < 0.05). The concentrations of moderately stable organic P in soil aggregates were the highest in spring (Table 3), at 10.3 mg kg–1.From spring to summer, the concentrations of moderately stable organic P in soil aggregates decreased significantly (P < 0.05), and then increased significantly (P < 0.05) in autumn, reaching 10.2 mg kg–1. However, there were no significant difference in the concentrations of moderately stable organic P between spring and autumn (P > 0.05). In addition, the concentrations of moderately stable organic P were the highest in the <0.25 mm aggregate fraction (Table 4), at 12.7 mg kg–1, and the difference with other aggregate fraction is significant (P < 0.05). According to the results, moderately stable organic P is enriched relatively easily in the micro aggregates.

The concentrations of highly stable organic P in the 0–20 cm, 20–40 cm, and 40–60 cm layers of different planting years in the spring, summer, and autumn have been plotted as column charts based on the aggregates of different aggregate fractions (Figs. S10–S12). The results of ANOVA conducted on the highly stable organic P data showed that the four factors, including planting years, soil layer, season, and aggregate fraction, in addition to their interaction, influenced highly stable organic P concentrations significantly (P < 0.01). Further multiple comparisons results for each factor are listed in Tables 1–4.

Highly stable organic P concentrations in soil aggregates increased first and then decreased with an increase in plant years (Table 1). The concentrations of highly stable organic P in soil aggregates were the lowest in the plants grown for 11 years, at 10.4 mg kg–1, and the highest in the plants growth for 25 years, at 12.4 mg kg–1, which is significant difference with other orchards (P < 0.05). While there were no significant differences in highly stable organic P concentrations between 11 years and 40 years, and between 40 years and 63 years, there were significant differences in highly stable organic P concentrations between 63 years and 11 years (P < 0.05). In addition, the concentrations of highly stable organic P in soil aggregates decreased linearly with an increase in soil depth (Table 2), which is 45.28% and 64.83% lower than that in the surface layer, and there were significant differences among the layers (P < 0.05). From spring to summer, the concentrations of highly stable organic P in soil aggregates increased significantly (P < 0.05), reaching 12.3 mg kg–1, and then decreased significantly (P < 0.05) in autumn (Table 3). However, there were no significant difference in the concentrations of highly stable organic P between spring and autumn (P > 0.05). The concentrations of highly stable organic P in the <0.25 mm fraction were the highest (Table 4), reaching 15.3 mg kg–1, followed by the 0.25–0.5 mm fraction, which was 13.8 mg kg–1. There was a significant difference in the concentrations between the two fractions, and among all the fractions (P < 0.05). The results indicate that highly stable organic P is enriched relatively easily in small aggregates.

The concentrations of total extracted organic P in the 0–20 cm, 20–40 cm, and 40–60 cm layers of different planting years in spring, summer, and autumn have been plotted as column charts according to the aggregates of different aggregate size fraction (Figs. S13–S15). The results of ANOVA carried out on the total extracted organic P data showed that the influence of the four factors examined, including planting year, soil layer, season, and aggregate fraction, in addition to their interactions on labile organic P were significant (P < 0.01). More multiple comparison results for each factor are presented in Tables 1–4.

The concentrations of total extracted organic P in soil aggregates increased first and then decreased with an increase in planting years (Table 1). The total extracted organic P concentrations in the orchard soil aggregates were the lowest under the 11-year-old plants, at 68.5 mg kg–1. Conversely, the total extracted organic P concentrations in the orchard aggregates were the highest under the 25-year-old plants, at 145.6 mg kg–1. In addition, there were significant differences among the four orchards (P < 0.05). The concentrations of total extracted organic P in soil aggregates decreased linearly with an increase in soil depth (Table 2), which is 43.89% and 63.65% lower than that in the surface layer, with significant differences among layers (P < 0.05). The total extracted organic P concentrations in soil aggregates increased significantly from spring to summer (P < 0.05), reaching 113.2 mg kg–1, and decreased significantly in autumn (P < 0.05) (Table 3). There were no significant differences in concentrations between spring and autumn (P > 0.05). In addition, the concentrations of total extracted organic P were the highest in the <0.25-mm aggregate fraction, reaching 144.2 mg kg–1, followed by in the 0.25–0.5 mm aggregate fraction, at 120.6 mg kg-1 (Table 4). There were significant differences among the three aggregate fractions (P < 0.05). The concentrations of total extracted organic P decreased with an increase in aggregate size fraction. The results suggest that total extracted organic P is are enriched relatively easily in small aggregates.

The labile, moderately labile, moderately stable, highly stable, and total extracted organic P in soil aggregates increased first and then decreased with an increase in planting year. The concentrations were the lowest in the 11-year-old plants, the highest in the 25‑year-old plants, and began to decrease in the 40‑year-old plants. The concentrations in the 63-year-old plants were lower than in the 40-year-old plants, but higher than in the 11-year-old plants. This is mainly because the relatively young fruit trees (11 years) have not reached the fruiting period, so that there are only inputs without output. In addition, the input levels are low, the amount of litter entering the soil annually is low, and the rate of accumulation of organic P in the soil is low. Compared with the 11‑year-old orchard, the 25-year-old orchard had lush foliage, more roots, and high fruit yield. Although the 25-year-old orchard consumed higher amounts of nutrients, enhanced by increased levels of fertilization, so that higher amounts of organic matter were returned to the soil annually, leading to the highest organic P accumulation levels in the soil.

At 40 years, the fruit trees entered their most productive stages, with the highest yield, the highest levels of fertilization and the most consumption, which promoted the mineralization and absorption of the labile organic P. As a result of the balance between nutrient management, input, and return, and nutrient consumption, the organic P in the 40-year-old orchards decreased; however, there was no significant difference in activity and medium stable organic P between the 40‑year-old and the 25-year-old orchard (P > 0.05). In the 63-year-old orchard, the trees were aged, and yield decreased, the orchard management began to enter roughly, and the organic matter returned to the soil decreased annually, so that the organic P levels in the orchard aggregates in the 63-year-old trees were lower than those in the 25 and 40-year-old trees. With an increase in soil depth, the labile, moderately labile, moderately stable, highly stable, and total extracted organic P concentrations in soil aggregates decreased linearly. In addition, there were significant differences among the soil layers, which was consistent with the findings of Kitayama [16]. This is mainly because roots of fruit trees are concentrated mainly in the 20–60 cm depth, which is the main layer at which fruit trees absorb soil nutrients, so that the rates of mineralization and absorption organic P in the layer are high, while the roots of fruit trees at the surface layer (0–20 cm) are relatively few and plant litter are deposited directly on the layer.

With the progression of seasons from spring, summer, and autumn, the concentrations of labile organic P in soil aggregates tended to decrease gradually, which was mainly due to low biological consumption, low microbial activity, and low organic P mineralization rates in spring. In addition, an increase in biological activity in summer intensified labile organic P absorption and mineralization rates. Similarly, other forms of organic P are also transformed into labile organic P, forming the labile organic P. In autumn, biomass consumption decreased; however, the rate of formation of labile organic P was relatively low, and it began being transformed into a stable state. The concentrations of moderately labile and highly stable organic P in soil aggregates increased from spring to summer, and then decreased significantly in autumn. On the contrary, the concentrations of moderately stable organic P first decreased and then increased, which was mainly associated with a dynamic balance among biological consumption, organic matter input, and organic P component transformation.

Although there are higher rates of biological consumption in summer, there are also higher rates of organic matter input and input of organic P components. Overall, the concentrations of moderately stable organic P decreased, the concentrations of moderately labile and highly stable organic P increased, with the increase in moderately labile organic P being largest, which was the main reason for the increase in total extracted organic P concentrations in summer. In autumn, the input of organic matter decreased, biological activity declined, and the rate of the formation of organic P decreased, and some of the moderately labile organic P changed from aging to moderately stable organic P, resulting in the increase in the moderately stable organic P in autumn and the decrease in moderately labile organic P.

Based on aggregate fraction distribution, the labile, moderately labile, moderately stable, highly stable, total extracted organic P concentrations in soil aggregates were the highest in the <0.25 mm aggregate fraction, followed by the 0.25–0.5 mm aggregate fraction. The concentrations of total extracted organic P decreased with an increase in aggregate fraction, which was consistent with the findings of Sun [13]. Small aggregate aggregates, especially micro aggregates, have large specific surface area and surface energy, often have colloidal properties, have strong adsorption and retention properties [12, 18], and can easily organic-inorganic complexes [17], so that organic P enriched in small aggregate aggregates relatively easily.

Compared with other forms of organic P, the moderately labile organic P had the highest concentration, accounting for 54.9–74.6% of the total extracted organic P, regardless of planting year, soil layer, season, or aggregate fraction. The second most abundant P component was the highly stable organic P, and the most labile organic P was less than the moderately stable organic P. The results of Yang [20] from a study on the Loess soil and Han [33] from a study on fluvo-aquic soil are slightly inconsistent with the findings reported in the present study. The order of abundance in the present study is as follows: moderately labile organic P > moderately stable organic P > labile organic P and highly stable organic P. Yan [32] conducted a study on black soil and reported that the proportions of moderately labile organic P were the highest, followed by the proportions of moderately stable organic P and highly stable organic P, while the proportions of labile organic P were the lowest. In the present study was conducted on Haplic Luvisols, which could be the major reason for the inconsistencies between the findings of the present study and previous studies.

CONCLUSIONS

The labile, moderately labile, moderately stable, highly stable, and total extracted organic P concentrations in soil aggregates increased first and then decreased with an increase in planting year. The concentrations of the P components were the lowest in the 11-year-old plantations and the highest in the 25-year-old plantations. In addition, the concentrations of labile, moderately labile, moderately stable, highly stable, and total extracted organic P in soil aggregates decreased linearly with an increase in soil depth, and there were significant differences among different levels. With change in seasons from spring, summer, to autumn, the labile organic P concentrations in soil aggregates decreased gradually, and the moderately labile, highly stable, and total extracted organic P concentrations first increased and then decreased, while the moderately stable organic P concentrations first decreased and then increased. The labile, moderately labile, moderately stable, highly stable, total extracted organic P concentrations in soil aggregates were the highest in the <0.25 mm aggregate fraction, followed by the 0.25–0.5 mm aggregate fraction. The total extracted organic P concentrations decreased with an increase in aggregate size fraction. Organic P accumulates relatively easily in small aggregates. Moderately labile organic P is the major organic P form in the apple-pear orchards, followed by highly stable organic P.