Distribution Characteristics of Soil Phosphorus Fractions in Lichen Crusts at Different Slope Positions in the Gurbantunggut Desert

YANG Ziyue¹,², YIN Benfeng²,³, ZHANG Shujun²,³,⁴, HUANG Yunjie²,³,⁴, YANG Ao²,⁵, ZHANG Yuanming²,³, GAO Yingzhi¹, JING Changqing¹

¹Key Laboratory of Grassland Resources and Ecology, Key Laboratory of Grassland Resources and Ecology of Western Arid Region, Ministry of Education, College of Grassland Science, Xinjiang Agricultural University, Urumqi 830052, Xinjiang, China
²State Key Laboratory of Ecological Safety and Sustainable Development in Arid Lands, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, Xinjiang, China
³Xinjiang Key Laboratory of Biodiversity Conservation and Application in Arid Lands, Xinjiang Institute of Ecology and Geography, Chinese Academy of Sciences, Urumqi 830011, Xinjiang, China
⁴University of Chinese Academy of Sciences, Beijing 100049, China
⁵College of Life Sciences, Xinjiang Normal University, Urumqi 830054, Xinjiang, China

Abstract

As the fundamental terrain unit of deserts, sand ridges create distinct surface water and thermal environments at different slope positions that profoundly influence the development and spatial distribution patterns of biological soil crusts. Lichen crusts are widely distributed on desert surfaces; however, scientific questions regarding how lichen crusts at different slope positions affect soil phosphorus cycling and what key factors influence this process remain unclear. This study addresses these questions through systematic analysis of phosphorus fractions and related enzyme activities in lichen crust layers and underlying 0–5 cm soils across different slope positions in the Gurbantunggut Desert. Results demonstrate that stable phosphorus fractions (HCl-Pi, HHCl-Po, HHCl-Pi, and Residual-P) accounted for over 75% of total phosphorus, followed by medium labile phosphorus (NaOH-Pi, NaOH-Po, NaHCO3-Po) and labile phosphorus (Resin-P, NaHCO3-Pi). Slope position significantly affected stable phosphorus, while soil layer significantly influenced medium labile phosphorus (P <0.05). Total phosphorus, organic phosphorus (Po), and inorganic phosphorus (Pi) contents in the crust layer were significantly higher at the slope bottom compared to east and west slopes, whereas in the underlying 0–5 cm soil layer, west slope values were significantly lower than those at the slope bottom and east slope (P <0.05). The content of NaOH-Pi was significantly higher on east and west slopes than at the slope bottom in the crust layer, and significantly higher on the west slope than on the east slope and slope bottom in the 0–5 cm soil layer. Regarding soil enzymes, the east slope exhibited the lowest alkaline phosphatase (ALP) and β-glucosidase (GC) activities in the crust layer but the highest activities in the underlying 0–5 cm soil layer. Random forest model analysis revealed that moisture and temperature variations induced by slope position were the most critical factors affecting labile and stable phosphorus contents, respectively. These findings provide scientific support for enriching theoretical frameworks of soil phosphorus cycling in desert ecosystems.

Keywords: biological soil crusts; lichen crusts; phosphorus cycling; temperate deserts; slope position; Gurbantunggut Desert

Introduction

Phosphorus is a key constituent of plant cell membranes, nucleic acids, and energy compounds, representing one of the critical limiting nutrients affecting terrestrial ecosystem productivity [1]. Soil phosphorus primarily originates from parent material weathering and minor atmospheric deposition, yet most phosphorus exists in occluded forms that are difficult for plants to absorb and utilize [2]. Based on soil morphology, phosphorus can be divided into organic phosphorus (Po) and inorganic phosphorus (Pi), and further categorized by bioavailability into labile phosphorus, medium labile phosphorus, and stable phosphorus [3]. Different phosphorus forms exhibit significant differences in plant availability [4]. Generally, labile phosphorus can be directly absorbed by plants in the short term [5]; medium labile phosphorus is readily adsorbed and fixed by minerals such as iron and aluminum oxides and requires biological processes (e.g., extracellular enzymes, organic acids) or abiotic processes (e.g., H⁺ ions) to transform it into labile phosphorus for plant uptake [6]; stable phosphorus is difficult for plants to directly utilize and may require hundreds to thousands of years for transformation [7].

In desert ecosystems, traditional soil nutrient stoichiometric analysis suggests these regions are nitrogen-limited with abundant soil phosphorus [8], which has somewhat constrained research development on soil phosphorus cycling in desert ecosystems. However, stoichiometry uses total nitrogen to total phosphorus ratios, and although total phosphorus content is high, bioavailable phosphorus that can be directly utilized by plants remains relatively low, severely limiting primary productivity in desert ecosystems [9]. Therefore, investigating the composition of various soil phosphorus forms and their influencing factors is crucial for understanding mechanisms that maintain desert ecosystem stability and sustainability.

Soil phosphorus fraction transformation is jointly influenced by abiotic and biotic factors [10]. Among abiotic factors, geochemical processes and climate (e.g., temperature, precipitation) profoundly affect soil phosphorus transformation [11]. Geochemical processes control phosphorus form transformations through weathering, adsorption-desorption, and precipitation-dissolution. Temperature increases promote conversion of labile and medium labile phosphorus to stable phosphorus, while precipitation enhances soil metal ion diffusion and pH changes, affecting physicochemical processes that ultimately influence phosphorus bioavailability [12]. Beyond direct effects, temperature and precipitation indirectly affect phosphorus cycling by influencing surface plants and soil microorganisms. Regarding biotic factors, plants and microorganisms regulate soil phosphorus through litter production, mycelium release, extracellular enzyme secretion, and organic acid exudation [13]. Under phosphorus limitation, plants and microorganisms release phosphatases to mineralize Po or exude organic acids to transform recalcitrant phosphorus into bioavailable forms, thereby enhancing phosphorus bioavailability [14].

In desert ecosystems, scarce precipitation prevents phosphorus leaching, making its activity primarily dependent on surface organisms [15]. Biological soil crusts, as important carriers of surface life in arid regions, are organic complexes formed by cryptogamic plants (cyanobacteria, lichens, mosses) cemented with soil surface particles, covering up to 70% of some arid areas [16]. Their development improves hydrological processes and microbial activities, promoting carbon, nitrogen, and phosphorus cycling [17]. Through crust succession, lichen crusts become widely distributed in deserts, occupying 6% of global terrestrial area [18]. Lichen crusts penetrate desert surfaces through rhizines and hyphal networks, fixing surface particles, and their rough, uneven post-colonization surfaces promote rock weathering and intercept weathering-accumulated phosphorus [19]. As desert fundamental terrain units, sand ridges alter soil physicochemical properties through different slope-specific water-thermal environments, thereby affecting biological soil crust development and spatial distribution [20]. Research indicates that compared to east slopes, biological soil crusts on west slopes better utilize early morning dew for growth [21]. How slope position affects phosphorus turnover in lichen crusts through altered surface water-thermal conditions remains unclear.

Therefore, we propose two scientific hypotheses: (1) Environmental differences created by slope position affect soil phosphorus fractions in lichen crusts, with higher phosphorus availability on west slopes compared to east slopes; (2) Biotic factors are key drivers of phosphorus cycling in the crust layer, while abiotic factors dominate phosphorus cycling in the underlying soil layer. To test these hypotheses, we selected the Gurbantunggut Desert, China's largest fixed and semi-fixed desert, as our study area, focusing on lichen crusts. By collecting lichen crust layers and underlying 0–5 cm soils from different slope positions, we examined how slope position affects phosphorus fraction characteristics, providing theoretical support for understanding soil phosphorus cycling in desert ecosystems.

1.1 Study Area Overview

The study area was located in the Gurbantunggut Desert within the Junggar Basin (44°15′~46°50′N, 84°50′~91°20′E). As China's second largest desert and largest fixed/semi-fixed desert, it covers approximately 4.88×10⁴ km². Influenced by westerly circulation, the desert features linear sand ridges, honeycomb dunes, and barchan dunes, with north-south oriented linear ridges dominating. The region has hot summers and cold, snowy winters with 100–150 days of stable snow cover, mean annual temperature of 5–7°C, mean annual precipitation of 70–150 mm, and mean annual evaporation exceeding 2000 mm, representing a typical temperate continental climate [22]. Early spring snowmelt provides abundant water and thermal conditions for plant germination and growth. Dominant shrubs include Haloxylon ammodendron, Haloxylon persicum, Calligonum mongolicum, and Artemisia ordosica, while major herbaceous plants are Erodium oxyrhinchum, Ceratocarpus arenarius, and Centaurea pulchella. The desert supports well-developed biological soil crusts (algal, lichen, and moss crusts), with lichen crusts dominating and showing differential distribution across dune slope positions [23].

1.2 Plot Setup and Sampling

In May 2023, we established study plots in the long-term desert ecosystem monitoring site in the Gurbantunggut Desert interior. Typical north-south oriented sand ridges were selected, and three 100 m transects (perpendicular to ridge orientation) were set up on west slopes, slope bottoms, and east slopes. Within each transect, five 2 m × 2 m quadrats were established (>2 m apart). Well-developed lichen crusts within each quadrat were sampled for both crust layer and underlying 0–5 cm soil, yielding 90 samples total. Samples were stored in ziplock bags at -20°C for ammonium nitrogen (NH₄⁺-N) and enzyme activity analyses. Simultaneously, soil temperature data across slope positions were collected using data loggers from the long-term monitoring site.

1.3 Chlorophyll Content Measurement

Chlorophyll content was measured using the ethanol method to characterize lichen crust biomass [26]. Fresh lichen crust samples (1.00 g) were ground with 10 mL of 95% ethanol. The mixture was kept in darkness for 30 min, after which absorbance was measured at 665 nm and 649 nm. Chlorophyll a (Chl a), chlorophyll b (Chl b), and total chlorophyll (Chl) were calculated as:
Chl a (mg∙L⁻¹) = 13.95 × A₆₆₅ - 6.88 × A₆₄₉
Chl b (mg∙L⁻¹) = 24.96 × A₆₄₉ - 7.32 × A₆₆₅
Chl (mg∙L⁻¹) = Chl a + Chl b
Where X is pigment content (mg∙g⁻¹), C is pigment concentration (mg∙L⁻¹), N is dilution factor, M is sample mass (g), and V is extraction volume (mL).

1.4 Soil Physicochemical Properties Measurement

Soil water content (SWC) was determined gravimetrically. Soil total carbon (TC) was measured after removing inorganic carbon with 1 mol∙L⁻¹ HCl. Total nitrogen (TN) was measured by Kjeldahl digestion, total phosphorus (TP) by molybdenum-antimony colorimetry, and available phosphorus (AP) by calcium chloride-sodium bicarbonate extraction (Olsen method). Soil pH and electrical conductivity (EC) were measured potentiometrically at a 1:2.5 soil:water ratio. Nitrate (NO₃⁻-N) and ammonium (NH₄⁺-N) were determined by continuous flow analyzer.

1.5 Soil Enzyme Activity Measurement

We measured alkaline phosphatase (ALP) and β-glucosidase (GC) activities related to phosphorus cycling using assay kits (Suzhou Grace Biotechnology Co. Ltd., Jiangsu, China). ALP activity was determined by treating p-nitrophenyl phosphate to generate yellow p-nitrophenol, measured at 405 nm. GC activity was determined by catalyzing hydrolysis of p-nitrophenyl-β-D-glucopyranoside to p-nitrophenol, measured at 400 nm. Enzyme activity was expressed as nmol substrate released per gram dry soil per hour (nmol∙g⁻¹∙h⁻¹).

1.6 Soil Phosphorus Fractions Measurement

Phosphorus fractions were determined using a modified Hedley sequential extraction [27]. Soil samples were air-dried, homogenized, and sieved (100 mesh). A 0.5 g subsample was sequentially extracted to obtain: resin phosphorus (Resin-P) via anion resin membrane; sodium bicarbonate inorganic and organic phosphorus (NaHCO₃-Pi, NaHCO₃-Po) via 0.5 mol∙L⁻¹ NaHCO₃; sodium hydroxide inorganic and organic phosphorus (NaOH-Pi, NaOH-Po) via 0.1 mol∙L⁻¹ NaOH; and dilute hydrochloric acid phosphorus (HCl-Pi) via 1 mol∙L⁻¹ HCl. Subsequent concentrated HCl (6 mol∙L⁻¹) extraction yielded concentrated HCl inorganic and organic phosphorus (HHCl-Pi, HHCl-Po). Finally, residual phosphorus (Residual-P) was obtained by digesting the remaining soil with concentrated H₂SO₄-HClO₄. All supernatants were measured by molybdenum blue colorimetry. NaHCO₃-Po content was calculated as the difference between total NaHCO₃-extractable phosphorus and NaHCO₃-Pi [28]. Based on previous research, phosphorus fractions were categorized by activity [29] as: labile phosphorus (Resin-P, NaHCO₃-Pi), medium labile phosphorus (NaOH-Pi, NaOH-Po, NaHCO₃-Po), and stable phosphorus (HCl-Pi, HHCl-Pi, HHCl-Po, Residual-P).

1.7 Data Analysis

We used R 4.1.2 (https://www.r-project.org/) for data processing, statistical testing, and visualization. Data normality and homogeneity of variance were verified to meet statistical assumptions. Two-way ANOVA tested effects of slope position and soil layer on phosphorus fractions and enzyme activities, with least significant difference (LSD) multiple comparisons. Pearson correlation analysis examined relationships among environmental factors, nutrients, and phosphorus fractions. Random forest analysis identified key factors influencing phosphorus fractions using the randomForest package.

Results

2.1 Characteristics of Soil Phosphorus Fractions in Lichen Crusts at Different Slope Positions

Stable phosphorus (HCl-Pi, HHCl-Po, HHCl-Pi, Residual-P) exceeded 75% of total phosphorus, followed by medium labile (NaOH-Pi, NaOH-Po, NaHCO₃-Po) and labile fractions (Resin-P, NaHCO₃-Pi) (Figure 2). Two-way ANOVA showed significant effects of slope position, soil layer, and their interaction on phosphorus fractions (Table 1). Slope position significantly affected stable fractions (HCl-Pi, HHCl-Po, HHCl-Pi, Residual-P), while soil layer significantly affected medium labile fractions (NaOH-Pi, NaOH-Po). Their interaction significantly influenced stable fractions HCl-Pi and Residual-P (P <0.05). Total phosphorus, organic phosphorus (Po), and inorganic phosphorus (Pi) in the crust layer were significantly higher at the slope bottom than on east and west slopes, while in the 0–5 cm soil layer, west slope values were significantly lower than at the slope bottom and east slope (P <0.05). NaOH-Pi content was significantly higher on east and west slopes than at the slope bottom in the crust layer, and significantly higher on the west slope than on the east slope and slope bottom in the 0–5 cm soil layer.

2.2 Effects of Different Slope Positions on Soil Enzymes

Soil layer more significantly affected ALP and GC activities than slope position (Table 1). The slope position × soil layer interaction significantly influenced ALP activity (Table 1). Both ALP and GC activities in the crust layer were significantly higher than in the underlying 0–5 cm soil across all slope positions (P <0.05). In the crust layer, east slope ALP activity was lower than on west slopes and slope bottom, but differences among slope positions were not significant (Figure 4); GC activity showed similar non-significant trends (P >0.05). In the underlying 0–5 cm soil, ALP and GC activities showed opposite trends to those in the crust layer, but differences remained non-significant (P >0.05).

2.3 Key Factors Influencing Soil Phosphorus Fractions

Correlation analysis revealed that soil water content was significantly positively correlated with NaHCO₃-Pi and NaHCO₃-Po, positively correlated with NaOH-Po and medium labile phosphorus, and significantly negatively correlated with Residual-P and stable phosphorus. Soil temperature was significantly positively correlated with NaOH-Pi and NaOH-Po, and significantly negatively correlated with Residual-P (Figure 5). In the crust layer, NaHCO₃-Pi content was significantly negatively correlated with temperature and significantly positively correlated with NH₄⁺-N. Soil pH was significantly negatively correlated with NaHCO₃-Po content, and both labile and medium labile phosphorus showed significant negative correlations with pH. Soil EC was significantly positively correlated with NaHCO₃-Po, and both labile and medium labile phosphorus showed significant positive correlations with EC (Figure 5). Random forest modeling identified key predictors of phosphorus fraction transformation (Figure 6). Soil water content (SWC) was the primary factor influencing labile phosphorus transformation, followed by GC activity and NH₄⁺-N. Soil temperature (ST) was the key factor for medium labile phosphorus transformation. Slope position, ST, and pH were the key factors for stable phosphorus transformation (Figure 6).

Discussion

3.1 Effects of Slope Position on Phosphorus Fractions in Lichen Crusts

Consistent with our hypotheses, slope-mediated water-thermal and physicochemical changes affected soil phosphorus fractions in lichen crusts. West slopes showed higher labile phosphorus content in crust layers than east slopes, attributable to more favorable water-thermal conditions promoting crust development and phosphorus turnover [31]. Although east slopes as shady aspects have higher daily mean soil water content and lower temperatures [32], their steeper windward gradients and west slopes' higher clay content enhance water-holding capacity and dew accumulation [33]. West slopes' later morning sun exposure also facilitates dew utilization for crust growth, with previous studies confirming higher lichen crust biomass per unit area on west slopes [23]. Beyond secreting extracellular enzymes and organic acids to promote phosphorus turnover, crust development enhances soil microbial diversity and abundance, facilitating phosphorus cycling [34]. Temperature differences among slope positions also matter, with west slopes receiving more solar radiation. As sun-loving organisms, lichen crusts respond to these differences [35]. Increased temperature enhances microbial activity and metabolism, providing carbon sources that promote iron-aluminum oxide redox reactions [36], reducing Fe³⁺ to Fe²⁺ and transforming stable phosphorus to bioavailable forms. Our significant negative correlation between temperature and stable phosphorus further confirms that warming promotes available phosphorus accumulation.

3.2 Key Factors Influencing Phosphorus Fractions in Lichen Crusts

Soil physicochemical properties critically affect phosphorus cycling, as our results confirm. Lichen crusts at slope bottoms had higher SWC and lower ST. SWC accumulation was significantly negatively correlated with NaHCO₃-Po but positively correlated with NaOH-Po and labile/medium labile phosphorus. Higher water content at slope bottoms promoted lichen crust growth, which absorbed more readily available Po and transformed Pi to Po. High water content increases soil solution mobility, enhancing phosphate-metal ion contact and promoting stable and medium labile phosphorus formation [37]. SWC affects phosphorus availability through both biological activity and physicochemical processes [38]. In alkaline soils, biological crust development reduces pH toward neutrality, increasing plant and microbial activity and promoting phosphorus turnover [39]. Our results confirm that pH reduction enhanced labile and medium labile phosphorus accumulation, particularly NaHCO₃-Po. Studies show that pH reduction promotes labile phosphorus accumulation [40]. Exchangeable calcium in soil combines with free inorganic phosphorus to form stable phosphorus in alkaline conditions [41]; pH reduction promotes conversion of calcium-bound phosphates to labile and medium labile forms while increasing iron-aluminum phosphate adsorption, creating complex effects on phosphorus bioavailability. Notably, EC reduction also weakens Ca²⁺ adsorption [42].

In arid and semi-arid regions, water is the primary limiting factor for plant growth [43]. Lower terrain positions with higher soil water content benefit plant development and microbial community activity, enhancing plant-microorganism phosphorus absorption and utilization, consistent with our findings [44]. We also found that labile phosphorus NaHCO₃-Pi was significantly positively correlated with NH₄⁺-N, while NaHCO₃-Po showed no significant correlation with NH₄⁺-N.

Conclusion

Soil phosphorus fractions beneath lichen crusts in the Gurbantunggut Desert are dominated by stable phosphorus (>75% of total phosphorus). Slope position affects phosphorus fraction contents by influencing surface water-thermal conditions. In crust layers, total phosphorus, organic phosphorus, and inorganic phosphorus contents were significantly higher at slope bottoms than on east and west slopes, while in underlying 0–5 cm soils, west slopes had significantly lower values than slope bottoms and east slopes. Random forest analysis revealed that labile phosphorus content was primarily affected by soil water content; medium labile phosphorus by ammonium nitrogen, GC activity, soil layer, and temperature; and stable phosphorus by temperature, slope position, and pH.

References

[1] Amadou I, Faucon M P, Houben D. Role of soil minerals on organic phosphorus availability and phosphorus uptake by plants[J]. Geoderma, 2022, 428: 116125.

[2] Helfenstein J, Pistocchi C, Oberson A, et al. Estimates of mean residence times of phosphorus in commonly considered inorganic soil phosphorus pools[J]. Biogeosciences, 2020, 17(2): 441-454.

[3] Hedley M J, Stewart J W B, Chauhan B S. Changes in inorganic and organic soil phosphorus fractions induced by cultivation practices and by laboratory incubations[J]. Soil Science Society of America Journal, 1982, 46(5): 970-976.

[4] Johnson A H, Frizano J, Vann D R. Biogeochemical implications of labile phosphorus in forest soils determined by the Hedley fractionation procedure[J]. Oecologia, 2003, 135(4): 487-499.

[5] O'Connell C S, Ruan L, Silver W L. Drought drives rapid shifts in tropical rainforest soil biogeochemistry and greenhouse gas emissions[J]. Nature Communications, 2018, 9: 1348.

[6] Hou E, Chen C, Luo Y, et al. Effects of climate on soil phosphorus cycle and availability in natural terrestrial ecosystems[J]. Global Change Biology, 2018, 24(8): 3344-3356.

[7] Dixon J L, Chadwick O A, Vitousek P M. Climate driven thresholds for chemical weathering in postglacial soils of New Zealand[J]. Journal of Geophysical Research: Earth Surface, 2016, 121(9): 1619-1634.

[8] Li Chengyi, He Mingzhu, Tang Liang. Advances on phosphorus cycle and their driving mechanisms in desert ecosystems: A review[J]. Acta Ecologica Sinica, 2022, 42(12): 5115-5124.

[9] Gao Y, Tariq A, Zeng F, et al. Allocation of foliar P fractions of Calligonum mongolicum and its relationship with soil P fractions and soil properties in a hyperarid desert ecosystem[J]. Geoderma, 2022, 407: 115546.

[10] Fan Y, Lin F, Yang L, et al. Decreased soil organic P fraction associated with ectomycorrhizal fungal activity to meet increased P demand under N application in a subtropical forest ecosystem[J]. Biology and Fertility of Soils, 2018, 54(1): 149-161.

[11] Zhang H, Shi L, Fu S. Effects of nitrogen deposition and increased precipitation on soil phosphorus dynamics in a temperate forest[J]. Geoderma, 2020, 380: 114650.

[12] Song X, Fang C, Yuan Z Q, et al. Long-term alfalfa (Medicago sativa L.) establishment could alleviate phosphorus limitation induced by nitrogen deposition in the carbonate soil[J]. Journal of Environmental Management, 2022, 324: 116346.

[13] Zang Y X, Min X J, de Dios V R, et al. Extreme drought affects the productivity, but not the composition, of a desert plant community in Central Asia differentially across microtopographies[J]. Science of The Total Environment, 2020, 717: 137251.

[14] Zhang J, Liu Y, Hou F. Changes in vegetation and soil coupling induced by biocrusts: New thinking on the segmented control of soil and water loss in the Loess Plateau, China[J]. Ecological Indicators, 2024, 161: 111953.

[15] Rodriguez Caballero E, Belnap J, Buedel B, et al. Dryland photoautotrophic soil surface communities endangered by global change[J]. Nature Geoscience, 2018, 11(3): 185-189.

[16] Weber B, Belnap J, Budel B, et al. What is a biocrust? A refined, contemporary definition for a broadening research community[J]. Biological Reviews, 2022, 97(5): 1768-1785.

[17] Zhang J, Zhang Y. Ecophysiological responses of the biocrust moss Syntrichia caninervis to experimental snow cover manipulations in a temperate desert of Central Asia[J]. Ecological Research, 2020, 35(1): 198-207.

[18] Zhang Tingting, Cheng Xiangmin, Wei Xinli, et al. Research progress on desert lichen crust[J]. Mycosystema, 2021, 40(1): 1-13.

[19] Zhang Yuanming, Yang Weikang, Wang Xueqin, et al. Influence of cryptogamic soil crusts on accumulation of soil organic matter in Gurbantunggut Desert, northern Xinjiang, China[J]. Acta Ecologica Sinica, 2005, 25(12): 3420-3425.

[20] Tao Y, Liu Yaobin, Wu Ganlin, et al. Regional scale ecological stoichiometric characteristics and spatial distribution patterns of key elements in surface soils in the Junggar Desert, China[J]. Acta Prataculturae Sinica, 2016, 25(7): 13-23.

[21] Jacobs A F G, Heusinkveld B G, Berkowicz S M. Dew measurements along a longitudinal sand dune transect, Negev Desert, Israel[J]. International Journal of Biometeorology, 2000, 43(4): 184-190.

[22] Tao Y, Zhou X B, Zhang S H, et al. Soil nutrient stoichiometry on linear sand dunes from a temperate desert in Central Asia[J]. Catena, 2020, 195: 104847.

[23] Zhang S, Yang A, Zang Y, et al. Slope position affects nonstructural carbohydrate allocation strategies in different types of biological soil crusts in the Gurbantunggut Desert[J]. Plant and Soil, 2024. http://doi.org/10.1007/s11104-024-06951-w.

[24] Yin B, Zhang Q, Li Y, et al. Moss mortality significantly altered topsoil multifunctionality and microbial networks in a temperate desert[J]. Land Degradation & Development, 2024, 35(6): 2034-2045.

[25] Han Binghong, Niu Decao, He Lei, et al. A review on the development and effect of biological soil crusts[J]. Pratacultural Science, 2017, 34(9): 1793-1801.

[26] Castle S C, Morrison C D, Barger N N. Extraction of chlorophyll a from biological soil crusts: A comparison of solvents for spectrophotometric determination[J]. Soil Biology and Biochemistry, 2011, 43(4): 853-856.

[27] Tiessen H, Moir J. Characterization of available P by sequential extraction[J]. Soil Sampling and Methods of Analysis, 1993, 7: 75-86.

[28] Helfenstein J, Pistocchi C, Oberson A, et al. Estimates of mean residence times of phosphorus in commonly considered inorganic soil phosphorus pools[J]. Biogeosciences, 2020, 17(2): 441-454.

[29] Zavisic A, Polle A. Dynamics of phosphorus nutrition, allocation and growth of young beech (Fagus sylvatica L.) trees in P rich and poor forest soil[J]. Tree Physiology, 2018, 38(1): 37-51.

[30] Mata González R, Pieper R D, Cárdenas M M. Vegetation patterns as affected by aspect and elevation in small desert mountains[J]. Southwestern Naturalist, 2002, 47(3): 440-448.

[31] Lange O L, Meyer A, Zellner H, et al. Vegetation patterns as affected by aspect and elevation in small desert mountains[J]. Functional Ecology, 1994, 8(2): 253-264.

[32] Baumann K, Siebers M, Kruse J, et al. Biological soil crusts as key player in biogeochemical P cycling during pedogenesis of sandy substrate[J]. Geoderma, 2019, 338: 145-158.

[33] Wang C, Kuzyakov Y. Soil organic matter priming: The pH effects[J]. Global Change Biology, 2024, 30(6): e17349.

[34] Zhang H, Shi L, Lu H, et al. Drought promotes soil phosphorus transformation and reduces phosphorus bioavailability in a temperate forest[J]. Science of The Total Environment, 2020, 732: 139285.

[35] Xue R, Yang Q, Miao F, et al. Slope aspect influences plant biomass, soil properties and microbial composition in alpine meadow on the Qinghai-Tibetan Plateau[J]. Journal of Soil Science and Plant Nutrition, 2018, 18(1): 1-12.

[36] X X, Yang X, Ren F, et al. Neutral effect of nitrogen addition and negative effect of phosphorus addition on topsoil extracellular enzymatic activities in an alpine grassland ecosystem[J]. Applied Soil Ecology, 2016, 107: 205-213.

[37] Tian D, Niu S. A global analysis of soil acidification caused by nitrogen addition[J]. Environmental Research Letters, 2015, 10(2): 024019.

[38] Ragot S A, Huguenin-Elie O, Kertesz M A, et al. Total and active microbial communities and P cycling as affected by phosphate depletion and pH in soil[J]. Plant and Soil, 2016, 408(1): 15-30.

[39] Gebrelibanos T, Assen M. Effects of slope aspect and vegetation types on selected soil properties in a dryland Hirmi watershed and adjacent agro-ecosystem, northern highlands of Ethiopia[J]. African Journal of Ecology, 2014, 52(3): 292-299.

[40] Han Zhili, Yin Benfeng, Yang Ziyue, et al. Effects of snow cover change on soil phosphorus fractions of Syntrichia caninervis crust in temperate desert[J]. Acta Ecologica Sinica, 2024, 44(16): 7119-7129.

[41] Lei Feiya, Li Xiaoshuang, Tao Ye, et al. Characterization of soil multifunctionality and its determining factors under moss crust cover in the arid regions of Northwest China[J]. Arid Zone Research, 2024, 41(5): 812-820.

[42] Dong Peng, Ren Yue, Gao Guanglei, et al. Stoichiometry of carbon, nitrogen, and phosphorus in the litter and soil of Pinus sylvestris var. mongolica in the Hulunbuir Sandy Land[J]. Arid Zone Research, 2024, 41(8): 1354-1363.

[43] Liu Chunzeng, Zhang Chenglan, Zhang Lin, et al. Effects of long-term Chinese milk vetch application coupled with reduced chemical fertilizer usage on soil ammonium nitrogen adsorption and desorption characteristics[J]. Soil and Fertilizer Sciences in China, 2024(6): 11-17.

[44] Feng Huanhuan, Gao Siqi, Gao Jinli, et al. Effect of nitrogen addition on typical plant leaf chlorophyll and nutrient content in peatland of the Great Hing'an Mountains[J/OL]. Chinese Journal of Ecology, 1-10[2025-04-22]. http://kns.cnki.net/kcms/detail/21.1148.Q.20240612.1213.004.html.