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Journal of Resources and Ecology >

2024 , Vol. 15 >Issue 2: 422 - 430

DOI: https://doi.org/10.5814/j.issn.1674-764x.2024.02.016

Animal and Plant Ecology

Effect of a Cushion Plant, Androsace tapete, on Soil Net Nitrogen Mineralization and Enzyme Activities during the Growing Season

  • XING Shuo , 1, 2 ,
  • HE Yongtao , 1, 3, * ,
  • NIU Ben 1 ,
  • XU Xingliang 1 ,
  • SONG Qian 1, 4 ,
  • WANG Yingfan 1, 2
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  • 1. Lhasa Plateau Ecosystem Research Station, Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China
  • 2. University of Chinese Academy of Sciences, Beijing 100049, China
  • 3. College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 100190, China
  • 4. College of Geographical Sciences, Liaoning Normal University, Dalian, Liaoning 116029, China
*HE Yongtao, E-mail:

XING Shuo, E-mail:

Received date: 2022-11-20

  Accepted date: 2023-05-10

  Online published: 2024-03-14

Supported by

The National Natural Science Foundation of China(31770477)

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Abstract

Cushion plants are one kind of unique specie in alpine ecosystems. They have a compact perennial cushion structure and play a role in facilitating the survival of other associated species by improving the local micro-environment. They are called “engineers” in the alpine ecosystem and their enhancement of soil nutrient availability is one of the ways of their engineering effect. In this study, Androsace tapete, a species of cushion plant widely distributed on the Qinghai-Tibet Plateau, was selected to investigate the dynamics of this process during the growing season at elevations of 4500 m and 4800 m on the southern slope of the Nyenchenthanglha mountains in Damxung. The effects of A. tapete on soil nutrient availability were analyzed by comparing the inorganic nitrogen content, net nitrogen mineralization rate and soil enzyme activities during the growing season in the soil under A. tapete and ambient grassland (CK). The results showed three important aspects of this system. (1) Soil nitrate nitrogen and ammonium nitrogen did not show significant differences at 4500 m, but the contents of nitrate nitrogen and inorganic nitrogen under the A. tapete soil significantly increased in the middle of the growing season at 4800 m, with nitrate nitrogen increasing by 56% and inorganic nitrogen increasing by 74.5%. (2) The trend and rate of soil nitrogen mineralization were both changed under A. tapete. In the 4500 m sample site, soil net nitrogen mineralization under A. tapete was negative (nitrogen immobilization) in the middle of the growing season, and the rate was -0.11 μg g-1 d-1, while that of CK was positive (nitrogen mineralization) and the rate was 0.61 μg g-1 d-1; and the difference between them was significant. However, both were positive in the early and late growing season, and the difference did not reach a significant level. In the 4800 m sample site, the soil net nitrogen mineralization under A. tapete was positive in the early part of the growing season, and the rate was 0.07 μg g-1 d-1, while the mineralization for CK was negative, and the rate was -1.17 μg g-1 d-1; and the difference was significant. In the middle of the growing season, both of them were negative, but the soil net nitrogen mineralization rate under A. tapete (-1.95 μg g-1 d-1) was significantly lower than that of CK (-0.02 μg g-1 d-1). At the late stage of the growing season, both of them were negative, and the difference was not significant. (3) Activities of nitrate reductase and nitrite reductase in the soil were significantly increased under A. tapete. Compared to CK at the 4500 m sample site, the activities of nitrate reductase and nitrite reductase under A. tapete were increased by 9.1% and 15.7%, respectively; and they were increased by 22.5% and 16.1%, respectively, at the 4800 m sample site. The activities of these two enzymes were significantly correlated with the dynamics of inorganic nitrogen in the soil. These results indicated that, compared to CK, the cushion plant A. tapete can change the process of soil nitrogen mineralization and the content of inorganic nitrogen, but that change had seasonal dynamics and spatial differences, which implies that this process was affected not only by the engineering of the cushion plant but also by changes in the local environment. Therefore, the engineering effect of cushion plant A. tapete was not constant during the growing seasons, and further studies are needed to clarify this process, especially considering the rapidly changing climate on the Qinghai-Tibet Plateau.

Key words： cushion plant; Androsace tapete; inorganic nitrogen; net nitrogen mineralization; Qinghai-Tibet Plateau

Cite this article

XING Shuo , HE Yongtao , NIU Ben , XU Xingliang , SONG Qian , WANG Yingfan . Effect of a Cushion Plant, Androsace tapete, on Soil Net Nitrogen Mineralization and Enzyme Activities during the Growing Season[J]. Journal of Resources and Ecology, 2024 , 15(2) : 422 -430 . DOI: 10.5814/j.issn.1674-764x.2024.02.016

1 Introduction

Cushion plants represent one a kind of plant with special morphology, and they are widely distributed in polar and alpine regions. They form a compact cushion, and their lifespan can be as long as decades or even hundreds of years (Zhao et al., 2015). The long-lived compact cushion can improve the local soil temperature and water content, thus providing a more suitable place for the colonization, survival, growth and breeding of certain other plants. So the cushion plants have been called the “ecosystem engineers” in arctic and alpine ecosystems (He et al., 2010; Meng et al., 2013; He et al., 2022). On the other hand, due to the low temperature in alpine ecosystems, the mineralization rate of organic nitrogen is lower and the availability of soil nitrogen is one of the main factors limiting plant growth in those systems (LeBauer and Treseder, 2008; Wang et al., 2021a). However, under some improved local micro-environmental conditions under the cushion, such as the soil temperature, water content, soil physical, chemical properties and enzymes, the process and availability of soil nitrogen will be changed (Zhou and Ou, 2001). Research has shown that cushion plants can increase the soil temperature (Badano et al., 2006; He et al., 2010) and soil water content (Cavieres et al., 2007) compared with the ambient area (CK, or ambient grassland without cushion plants). This is mainly because the cushion plants have a compact and thick cushion body which can reduce the evaporation rate of soil water and improve the soil water holding capacity; and their dead leaves are retained for many years, which can not only increase the soil temperature but also promote the mineralization of soil nitrogen (He et al., 2013; He et al., 2014a). Moreover, the dead leaves of cushion plants can increase the organic matter content in the soil, and the difference between the contents under their cushion and CK can be more than twofold (Wang et al., 2016; Hupp et al., 2017; Zhao et al., 2020). Therefore, cushion plants can affect the nitrogen mineralization process and content of available nitrogen in soil by changing the local soil micro-environment, but many previous studies just conducted one field measurement for the availability of soil nutrition under the cushion (Cavieres et al., 2006; Liu et al., 2011; Liu et al., 2014), and the dynamics of this process during the growing season remain unclear.
In addition, enzymes are the main catalysts of biochemical processes in the soil, which can promote the mineralization of nitrogen in soil. Of these enzymes, proteases help to decompose the proteins and peptides of plant residues in soil into amino acids. Urease is the only hydrolase that can hydrolyze urea in soil (Wang et al., 2016; Ma et al., 2021), which can help in the conversion of organic nitrogen into the inorganic nitrogen in soil that can be used by plants and microorganisms. Nitrate reductase can catalyze the reduction of nitrate to nitrite, while nitrite reductase catalyzes the conversion of NO2- in soil to NH2OH or N2O (Kuypers et al., 2018; Yu et al., 2020). However, the activities of these soil enzymes will be affected by environmental factors, especially soil temperature and water content (Yan et al., 2017; Wang et al., 2020). Therefore, the local micro-environmental changes caused by cushion plants may lead to different soil enzyme activities, thus affecting the soil nitrogen mineralization.
As one of the important cushion plant populations, Androsace tapete has the most widely distributed area among cushion plants on the Qinghai-Tibet Plateau (Li et al., 1985; Li et al., 1987). According to one previous study, A. tapete has a significant ecosystem engineering effect, which can help other plants to cope with the harsh alpine environment on the Qinghai-Tibet Plateau (Pugnaire et al., 2015). At the same time, their dead leaves that are retained for many years will promote the mineralization of soil nitrogen at the low temperature in winter, thus providing a source of nutrients for the growth of other plants in the spring (He et al., 2014b). However, the mechanism by which A. tapete changes the soil nitrogen mineralization and enzyme activities during the growing season are still uncertain. Therefore, this study carried out field experiments on the southern slope of the Nyenchenthanglha Mountains in Damxung, and measured the inorganic nitrogen content, net nitrogen mineralization rate and enzyme activities in the soil under A. tapete and ambient grassland (CK) during the growing season, in order to explore the dynamic effects of cushion plants on changes in the availability of soil nitrogen.

2 Materials and methods

2.1 Study site

The study site is situated at the southern slope of Nyenchenthanglha Mountains in Damxung (91°05′E, 30°51′N). The average annual temperature is 1.3 ℃, the temperature of the coldest month (January) is -10.4 ℃, and the hottest month (July) is 10.7 ℃. The average annual precipitation is 476.8 mm, 85.1% of which is concentrated from June to August (Zong et al., 2013). Alpine meadows with Kobresia pygmaea as the dominant species are widely distributed along the slope, and A. tapete mixed within the alpine meadow is mainly distributed at elevations from 4500 m to 5200 m (He et al., 2013; Li et al., 2013). According to field meteorological monitoring along this slope, the annual average temperature declines by 0.61 ℃ (100 m)-1, and the growing season precipitation increases by 4-7 mm (100 m)-1 at elevations below 5100 m (Xie et al., 2009).
In this study, two elevations of 4500 m and 4800 m were selected as the experimental areas. Among them, 4500 m is the lowest distribution of A. tapete along the slope, with population coverage of about 1%; while the 4800 m site is the area where A. tapete has a concentrated distribution, and population coverage can reach 16.4%. The size of the cushions was predominantly above 100 cm2, and their coverage can reach one-third to one-half of the total coverage of A. tapete (He et al., 2013). At 4500 m, the grassland was mainly dominated by Artemisia desertorum, Stipa aliena and Anaphalis sp., with a total vegetation coverage of 40%; while at 4800 m, the main species include Kobresia pygmaea, Carex atrofusca and Potentilla spp., with a total vegetation coverage of about 85% (Ohtsuka et al., 2008). The basic physical and chemical properties of surface soil in the sample sites are shown in Table 1.
Table 1 Basic physical and chemical properties of surface soil (0-10 cm) in the experimental areas
Elevation (m) pH Organic carbon (g kg-1) Total N
(g kg-1)		 Bulk density (g cm-3) C/N
4500 7.03±0.22 29.71±4.12 2.65±0.39 1.05±0.10 11.69±0.10
4800 6.47±0.25 92.13±11.34 6.37±0.71 0.85±0.03 16.64±0.10

2.2 Experimental design and sample collection

In the field experiment, soil net nitrogen mineralization was measured by the cultivation method with PVC pipes (Raison et al., 1987). According to the seasonal dynamics of plant growth on the Qinghai-Tibet Plateau, the determination of soil net nitrogen mineralization was divided into three periods: the early period of the plant growth season (May 18 to June 15), the middle period of the plant growth season (July 21 to August 18) and the late period of the plant growth season (September 6 to October 4). The field incubation times were all 28 days.
Sample plots were set up at the 4500 m and 4800 m experimental sites, and the sampling area was about 20 m×20 m. At the beginning of each incubation, five medium sized A. tapete (150-200 cm2) were randomly selected in each sample plot, and one grassland plot of the same size but without A. tapete was selected as the control (CK). A pair of PVC tubes (diameter 3.5 cm) were put into each cushion body and the CK respectively, with a total length of 12 cm and buried to a depth of 10 cm, and the tube top was sealed with plastic wrap. The tubes were collected after 28 days of incubation and brought to laboratory, where the contents of ammonium nitrogen and nitrate nitrogen in the soil samples were analyzed.
At the same time of setting the PVC tubes in each sampling time, five medium sized A. tapete and five CK areas were selected within 10-20 cm around the tubes, and the 0-10 cm soil layers under the A. tapete and CK surface were collected with soil drills and brought to the laboratory for determining the initial values of soil nitrate nitrogen and ammonia nitrogen before the 28-day incubation.

2.3 Analysis and calculation methods

2.3.1 Soil samples

Fresh soil samples were taken to the laboratory as soon as possible. After removal of large roots and gravel, the soils were sieved through 0.25 mesh and thoroughly mixed. Each sample was then divided into three subsamples, one of which was used to determine soil water content, another for measuring soil enzyme activities, and the third sample was used to determine nitrate nitrogen and ammonium nitrogen.

2.3.2 Inorganic N

Before and after each incubation, the concentrations of total inorganic nitrogen were analyzed to calculate the rate of nitrogen mineralization. Ammonium nitrogen (NH4+-N) and nitrate nitrogen (NO3--N) were determined by extraction from 30 g fresh soil with 100 ml of 2M KCl solution on an oscillator for 30 min, and filtering through a qualitative filter paper (Wheatley et al., 1989). Filtrates were then analyzed with a Seal Automatic Analyzer 3 (Bran+Lubbe, Germany). All values were calculated based on the dry weight of the soil, and the total inorganic nitrogen content is the sum of nitrate nitrogen and ammonium nitrogen. Net nitrogen mineralization was estimated as the difference between total inorganic nitrogen content after and before incubation. The calculation formula is:

Net nitrogen mineralization=After incubation (NH4++NO3-)-Before incubation (NH4++NO3-)

The net mineralization rate of nitrogen was expressed as the average value per day during incubation (Raison et al., 1987), the calculation formula is:
R min = Δ c Δ t
where Rmin is the net nitrogen mineralization rate, Δc is the difference between inorganic nitrogen contents before and after incubation, and Δt is the incubation time (28 days). The ammoniation rate and nitrification rate refer to the differences of ammonium nitrogen and nitrate nitrogen during the incubation, respectively, and the calculation formula is the same as above.

2.3.3 Soil water content

To determine the soil water content, 50 g fresh soil was oven-dried at 105 ℃ for 24 h.

2.3.4 Soil enzyme activities

Soil enzyme activities (protease and urease) were determined by the colorimetric method with reference to Guan (1986). Protease activity was determined by the sodium caseinate analysis method. After incubation at 37 ℃ for 24 hours, the tyrosine produced (μg) in 5 g soil was calculated and expressed as μg g-1 h-1. The urease activity was determined by the phenol sodium hypochlorite colorimetry and ammonia release method after incubation at 37 ℃ for 24 hours, and expressed as NH3-N (mg g-1 h-1) in soil. The activities of nitrate reductase and nitrite reductase in soil were determined by incubation at 37 ℃ for 24 hours followed by phenol disulfonic acid colorimetry and Grignard reagent colorimetry, and the amount of reduced NO2--N in soil was measured and expressed as μg g-1 h-1 (Li et al., 2008). In order to eliminate the errors due to soil and reagents, three controlled soil-free replicates with the matrix were analyzed.

2.4 Statistical analyses

All statistical analyses and graph drawing were completed using R (version 4.1.3). Among the tests, one way ANOVA was used to compare the inorganic nitrogen content, net nitrogen mineralization rate, and four enzyme activities (protease, urease, nitrate reductase and nitrite reductase) in the soil under A. tapete and CK at different elevations. Pearson’s two-sided test was used to analyze the correlations between the four enzyme activities and net nitrogen mineralization. In all statistical analyses in this study, P< 0.01 represents an extremely significant difference, and P< 0.05 represents a significant difference. Before analysis, distribution normality and homogeneity of variance tests were performed on the data.

3 Results

3.1 Soil water content

For each site, the soil water contents under A. tapete and CK did not show significant differences at 4500 m, but did show significant differences with seasonal dynamics at 4800 m. In the early growing season at 4800 m, the soil water content under A. tapete was 57.8% lower than that of CK, however, in the middle growing season, the soil water content under A. tapete was 32.6% higher than that of CK, and in the late period it was 20.7% higher than that of CK.
Table 2 Soil water contents under A. tapete and CK
Sampling date Soil sampling plot
4500 m 4800 m
Under
A. tapete (%)		 CK(%) Under
A. tapete (%)		 CK(%)
2021-05-18 8.04±2.19a 9.20±0.99a 10.48±1.76b 16.54±5.76a
2021-07-21 20.37±2.71a 22.96±3.33a 48.46±8.81a 36.56±5.41b
2021-09-06 25.24±2.98a 25.69±1.40a 43.42±3.18a 35.98±9.72b

Note: Different letters indicate significant differences under A. tapete and CK.

In addition, the soil water contents both under A. tapete and in CK at 4800 m were significantly higher than those at 4500 m during the whole growing season. In the early growing season, the soil water content under A. tapete at 4800 m was 30.3% higher than at 4500 m, and 79.8% higher in the CK. In the middle growing season, the soil water content under A. tapete at 4800 m was 137.9% higher than at 4500 m, and 59.2% higher in the CK. In the late growing season, the soil water content under A. tapete at 4800 m was 71.6% higher than at 4500 m, and 40.1% higher in the CK.

3.2 Inorganic nitrogen content

Differences in the contents of the ammonium nitrogen, nitrate nitrogen and inorganic nitrogen between the soils under A. tapete and CK varied between the two elevations. The difference of inorganic nitrogen content in soil between the CK and A. tapete was not significant at 4500 m. At 4800 m, the contents of ammonium nitrogen in the soils under A. tapete and CK did not have a significant difference, but the nitrate nitrogen contents showed a significant difference in the early and middle growing seasons. The nitrate nitrogen content in soil under A. tapete in the early growing season (4.31 μg g-1) was significantly lower than that of CK (13.2 μg g-1), while in middle growing season, the nitrate nitrogen content in soil under A. tapete (24.67 μg g-1) was significantly higher than that of CK (15.81 μg g-1), showing an increase of 56% (Fig. 1d). In the late growing season, the difference between them was not significant. The total content of inorganic nitrogen in soil under A. tapete (35.49 μg g-1) was 74.5% greater than that of the CK (20.34 μg g-1) in the middle growing season (Fig. 1f).
Fig. 1 Dynamics of soil inorganic nitrogen under A. tapete and CK during the growing season

Note: CK: Without A. tapete; UA: Under A. tapete; EGS: Early growing season; MGS: Middle growing season; LGS: Late growing season; AGS: Average value of growing season. Different capital letters indicate the soil inorganic nitrogen content of CK is significantly different in the different growing periods (P<0.05). Different lowercase letters indicate the soil inorganic nitrogen content under A. tapete is significantly different in the different growing periods (P<0.05); ns: P>0.05; * indicates a significant difference between UA and CK (P<0.05). The same notations are used in subsequent figures.

During the whole growing season, the averages of A. tapete and CK showed no significant differences in the same altitude, however, the three indicators showed significant differences between the two elevations. In addition, the higher values of soil inorganic nitrogen content at both elevations appeared in the middle growing season, i.e., 6.21 μg g-1 and 27.92 μg g-1 at 4500 m and 4800 m respectively, which were significantly higher than those in early and late growing seasons at 4800 m. In addition, the contents of ammonium nitrogen, nitrate nitrogen and inorganic nitrogen in the soil at 4800 m all were higher than those at 4500 m, especially in the middle growing season. Among them, the inorganic nitrogen content under A. tapete at 4800 m was nearly five times as much as that at 4500 m, and nearly two times as much as in the CK (Fig. 1).

3.3 Net nitrogen mineralization rate

Net nitrogen mineralization in the soils under A. tapete and CK showed different trends and rates during the growing season, and significant differences were also apparent between the two elevations. At 4500 m, net nitrogen mineralization in the soil under A. tapete was negative, while it was positive in the soil of CK in middle growing season. The ammonification rate and net nitrogen mineralization rate were -0.20 μg g-1 d-1 and -0.11 μg g-1 d-1, respectively, in the soil under A. tapete, but 0.82 μg g-1 d-1 and 0.61 μg g-1 d-1, respectively, in the soil of the CK; and both showed significant differences between the soils under A. tapete and CK (Fig. 2a, e), but they did not show significant differences between the early and late growing seasons.
Fig. 2 Soil net nitrogen mineralization rates under A. tapete and CK during the growing season
At 4800 m, net nitrogen mineralization in the soil under A. tapete was positive in the early growing season (0.07 μg g-1 d-1), while it was negative for CK (-1.17 μg g-1 d-1). In the middle growing season, net nitrogen mineralization was negative for both, but the rate for A. tapete soil (-1.95 μg g-1 d-1) was significantly lower than that of CK (-0.02 μg g-1 d-1). It was also negative in the late growing season, but there was no significant difference between soils under A. tapete and CK (Fig. 2). The ammonification rate of nitrogen in the soil under A. tapete was negative (-0.94 μg g-1 d-1) in middle growing season, while it was positive for CK (0.62 μg g-1 d-1). Both were negative in the early growing season and positive in the late growing season, but the difference between the soils under A. tapete and CK was not significant. The nitrification of nitrogen was positive in the soil under A. tapete (0.38 μg g-1 d-1) but negative in CK (-0.99 μg g-1 d-1) in the early growing season. Both were negative in the middle and late growing seasons, but the difference between the soils under A. tapete and CK was not significant.
During the whole growing season, there were no significant differences between the averages of A. tapete and CK at the same elevation, but the net nitrification rate and net mineralization rate were significantly different at two elevations. The average net nitrification rates of A. tapete and CK at 4800 m (-0.37 μg g-1 d-1, -0.74 μg g-1 d-1) were significantly lower than at 4500 m (-0.01 μg g-1 d-1, -0.02 μg g-1 d-1); while the average net mineralization rates of A. tapete and CK at 4800 m (-0.71 μg g-1 d-1, -0.60 μg g-1 d-1) were also significantly lower than at 4500 m (0.07 μg g-1 d-1, 0.4 μg g-1 d-1).

3.4 Soil enzyme activities

For the enzyme activities, there were no significant differences in urease or protease between the soils under A. tapete and CK at either of the two elevations. However, the enzyme activities of nitrate reductase and nitrite reductase in the soil under A. tapete were significantly higher than those of CK at 4500 m. At 4800 m, the nitrate reductase activity in the soil under A. tapete was also significantly higher than that of CK; while the nitrite reductase activity in the soil under A. tapete was 16.1% higher than that of CK, and the difference was extremely significant.
Table 3 Soil enzyme activities under A. tapete and CK
Soil
enzyme		 Soil sampling plot
4500 m 4800 m
Under A. tapete CK Under A. tapete CK
Urease 52.30±9.83a 50.08±9.47a 81.57±18.91a 84.23±9.47a
Protease 14.85±1.34a 14.39±1.06a 16.78±1.66a 16.15±1.65a
Nitrate reductase 100.23±7.39a 91.86±7.75b 121.05±16.18a 98.83±16.87b
Nitrite
reductase		 43.28±12.73a 37.40±13.34b 25.15±3.96a 21.66±6.26b

Note: Different letters indicate significant differences under A. tapete and CK.

The correlation analysis showed that the activities of urease and protease had no significant correlations with contents of nitrate nitrogen, ammonium nitrogen or inorganic nitrogen in the soil (Table 4). The activities of nitrate reductase showed an extremely significantly positive correlation with the contents of nitrate nitrogen and inorganic nitrogen in soil, with correlation coefficients of 0.480 and 0.451, respectively; and it was also significantly positively correlated with the ammonium nitrogen content in soil, with a correlation coefficient of 0.348. Nitrite reductase showed extremely significantly positive correlation with ammonium nitrogen in soil, and a significantly positive correlation with inorganic nitrogen content, with correlation coefficients of 0.413 and 0.309, respectively, but it did not show a significant correlation with soil nitrate nitrogen content.
Table 4 Correlations between soil enzyme activities and soil net nitrogen mineralization
Type Nitrate
nitrogen		 Ammonium nitrogen Inorganic nitrogen Soil water content
Urease 0.015 0.102 0.156 0.009
Protease 0.173 0.164 0.168 0.073
Nitrate
reductase		 0.480** 0.348* 0.451** 0.019
Nitrite
reductase		 0.224 0.413** 0.309* 0.025

Note: **P<0.01 indicates the difference is extremely significant; *P<0.05 indicates the difference is significant.

4 Discussion

The results of this study showed that the inorganic nitrogen content in the soil under A. tapete was significantly higher than that of CK but only at 4800 m in the middle growing season. The main reason for this is that although the temperature was higher at the 4500 m sample plot (Xie et al., 2009), the soil organic carbon, total nitrogen and water contents were lower, of which the organic carbon and total nitrogen were only 32.2% and 41.3% of the levels at the 4800 m sample plot. The lower carbon, nitrogen and water contents will limit the process of soil nitrogen mineralization, thus reducing the content of inorganic nitrogen in the soil (Wang et al., 2018; Li et al., 2020; Xiang et al., 2021). On the other hand, at the 4800 m sample plot, which had the most concentrated distribution area of A. tapete, the nitrate reductase activity in the soil was higher than at 4500 m, and the nitrite reductase activity was lower. The difference in enzyme activities will also affect the inorganic nitrogen content in the soil (Wang et al., 2016; Ma et al., 2021). These results indicated that the cushion plant A. tapete could change the soil nitrogen mineralization and affect the soil available nitrogen content, but this process was also affected by environmental conditions. Other studies also showed that the cushion plants under different environmental conditions had significant differences in improving their surrounding micro-environment and soil nutrient conditions (Liu et al., 2011; Schöb et al., 2012; Liu et al., 2014; Cavieres et al., 2014; Mihoč et al., 2016).
The difference in net nitrogen mineralization between the soil under A. tapete and the CK showed that the cushion plant A. tapete could affect the soil nitrogen mineralization, but that effect had seasonal dynamics, and was more significant in the middle growing season. The reason for this seasonal difference could be due to the seasonal changes of precipitation and temperature (Stanford and Epstein, 1974; Liu and Ma, 2021; Wang et al., 2021b), and the difference in micro-environment was also important. At 4500 m, the net nitrogen mineralization rate in the soil of CK was positive throughout the whole growing season, while it was negative at 4800 m. This difference may be due to the richer soil organic matter and higher plant coverage at 4800 m, thus driving the competitive uptake of soil available nitrogen by plants and microorganisms, leading to a reduction in the inorganic nitrogen content (He et al., 2013; Ma et al., 2020). The net nitrogen mineralization rate in the soil under A. tapete showed a different pattern, which was positive in the early growing season, negative in the middle growing season, and almost balanced in the late growing season. Another study also showed that cushion plants can change the mineralization trend of nitrogen in the soil through dead leaves, but that change was affected by temperature (He et al., 2014b). The results of this study further indicated that the presence of cushion plants can significantly change the trend and rate of net nitrogen mineralization, thereby changing the available inorganic nitrogen in the soil. However, this effect had significant spatial variations and seasonal differences due to changes in the local environments.
In addition, soil enzyme activities are also one of the important factors affecting the net nitrogen mineralization rate (Kuypers et al., 2018; Yu et al., 2020). In this study, the four soil enzyme activities were significantly increased under the influence of cushion plant A. tapete, especially the nitrate reductase and nitrite reductase, and they had significantly positive correlations with the contents of ammonium nitrogen and inorganic nitrogen, which is similar to the results found in grassland (Yan et al., 2017). These results indicated that the activity of soil enzymes, especially the nitrate reductase and nitrite reductase, was also one of the important ways to affect the soil nitrogen mineralization process and the available nitrogen content under A. tapete.

5 Conclusions

The results of this experiment showed that the cushion plant A. tapete has obvious effects on the content and net mineralization of inorganic nitrogen in soil, but there were also significant temporal and spatial variations. The soil under A. tapete can have an increased inorganic nitrogen content, especially the nitrate nitrogen at 4800 m in middle growing season; and the trend and rate of soil net nitrogen mineralization can be changed by A. tapete, but this effect also is not constant. In addition, the activities of four kinds of soil enzymes were increased by different degrees, especially the activities of soil nitrate reductase and nitrite reductase which were significantly increased, but all of the above processes showed variations between the two elevations and during the different parts of the growing season. Therefore, the effects on soil nitrogen mineralization by cushion plant A. tapete were not only caused by the plant itself, but also by the local environment. In the future, further research is needed to clarify the effects and influencing factors on changes in soil nutrient availability caused by cushion plants.

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