ORIGINAL PAPER

Distribution Characteristics of Soil Organic Phosphorus Fractionsin the Inner Mongolia Steppe

Xiaoya Zhu1& Xiaorong Zhao1

& Qimei Lin1& Alamus2 & Hai Wang2

& Honglin Liu2& Wenxue Wei3 & Xuecheng Sun4

&

Yongtao Li5 & Guitong Li1

Received: 10 February 2020 /Accepted: 21 July 2020# Sociedad Chilena de la Ciencia del Suelo 2020

AbstractPhosphorus (P) is one of the limiting nutrients in Inner Mongolia steppe soil, which seriously affect steppe produc-tivity. Therefore, it is necessary to understand the distribution characteristics of organic P (Po) fractions and theirinfluencing factors in Inner Mongolia steppe soil and to identify the contribution of Po fractions to soil available P(AP) to maintain the sustainable development of the Inner Mongolia steppe by improving the utilization rate of Po.The contents of soil Po fractions such as H2O-extractable Po (H2O-Po), NaHCO3-extractable Po (NaHCO3-Po), HCl-extractable Po (HCl-Po), NaOH-extractable Po (NaOH-Po), and phytate P (Phyt-P) were determined in soil samples (0–15 cm) from 15 sampling sites representing three types of grassland (i.e., desert steppe, typical steppe, and meadowsteppe) in Inner Mongolia. The influencing factors of the soil Po fractions were determined by redundancy analysis(RDA). Soil Po content accounted for 61.0% of the total P (TP) on average. NaOH-Po was the main fraction of Po,accounting for 49.1% of Po on average; H2O-Po content accounted for the least amount of Po (mean 1.3 mg kg−1).H2O-Po and HCl-Po were not significantly different among the three steppes. The contents of NaHCO3-Po increased inthe order of desert steppe < typical steppe < meadow steppe, and the trend of NaOH-Po and Phyt-P contents weredesert steppe < meadow steppe < typical steppe. Pearson correlation analysis showed that NaHCO3-Po was positivelycorrelated with AP (r = 0.86, p < 0.01). HCl-Po was negatively correlated with AP (r = − 0.56, p < 0.05). NaOH-Po andPhyt-P were significantly positively correlated with NaHCO3-extractable inorganic P (NaHCO3-Pi); Phyt-P was alsonegatively correlated with HCl-extractable Pi (HCl-Pi) (r = − 0.61, p < 0.05). These correlations were mainly caused bydifferences in steppe types and soil properties caused by climatic conditions, as shown by the result of RDA analysis.Soil Po plays an indispensable role in the supply of soil P in the semi-arid steppe of Inner Mongolia, where NaHCO3-Po and HCl-Po strongly contributed to AP. In addition, NaOH-Po and Phyt-P as a part of stable pools are important forproviding P to other P pools. Po fractions in steppe soils were mainly regulated by climatic conditions and are closelyrelated to the soil organic matter and pH.

Keywords Steppe types . Climate . Vegetation . Organic phosphorus fractions

Electronic supplementary material The online version of this article(https://doi.org/10.1007/s42729-020-00305-y) contains supplementarymaterial, which is available to authorized users.

* Xiaorong Zhaozhaoxr@cau.edu.cn

1 College of Land Science and Technology, China AgriculturalUniversity, Beijing 100193, China

2 Grassland Research Institute, Chinese Academy of AgriculturalSciences, Hohhot 010010, Inner Mongolia, China

3 Institute of Subtropical Agriculture, Chinese Academy of Sciences,Changsha 410125, Hunan, China

4 College of Resources and Environment, Huazhong AgriculturalUniversity, Wuhan 430070, Hubei, China

5 College of Resources and Environment, South China AgriculturalUniversity, Guangzhou 510642, Guangdong, China

Journal of Soil Science and Plant Nutritionhttps://doi.org/10.1007/s42729-020-00305-y

1 Introduction

Phosphorus (P) is one of the essential nutrients for all livingorganisms and is considered the key element in pedogenesisbecause of its great ecological significance (Walker 1965;Vitousek et al. 2010), which is one of the important nutrientsdetermining the function and primary productivity of terres-trial ecosystems (Aerts and Chapin 1999; Elser et al. 2007). Pis also one of the most restrictive mineral nutrients commonlyfound in natural ecosystems (Elser et al. 2007; Zhang et al.2019). During the development of ecosystems in climate andpedogenesis, the P pool changes its composition, abundance,and bioavailability. Natural soil P is mainly derived from geo-chemical weathering of soil parent materials because of lowatmospheric P deposition (Chadwick et al. 2003; Walker andSyers 1976; Weihrauch and Opp 2018). P is depleted throughplant biomass removal, leaching, and erosion (Izquierdo et al.2013; Khan et al. 2019; Walker and Syers 1976), and this lossof P cannot be compensated in unfertilized soils. Thus, the Pavailability for primary productivity becomes increasingly re-stricted with ecosystem succession (Elser et al. 2007). In ad-dition, P has limited mobility and availability as nutrient toplants in most soil conditions because of the strong reactivityof PO4

3− with diverse soil minerals. The movement of phos-phate ions in soils is particularly sensitive to soil moistureregimes (He et al. 2002; Smith 2002). P nutrition is also es-sential for plants to tolerate aridity (He et al. 2002).Consequently, P is often the primary limiting nutrient in manyarid and semi-arid regions. Organic P (Po) accumulates undernitrogen (N) limitation in the early stage of ecosystem devel-opment, while at advanced stages of ecosystem development,Po concentrations decline under conditions of P limitation, andthe P cycle is regulated by both geochemical and biologicalprocesses (Turner et al. 2007a). When soil maturity is reachedin chrono-sequences, whereby primary mineral P isexhausted, total P (TP) is low, and the remaining P is predom-inantly in organic and occluded inorganic forms (Selmantsand Hart 2010; Walker and Syers 1976). In undisturbed ter-restrial ecosystems, P mainly exists in the form of Po (Krämerand Green 1999; Oberson et al. 1996), accounting for morethan 50% of the TP in natural ecosystems (Chen et al. 2014;Tyler 2002). For example, Zhao et al. (2007) showed that soilPo accounted for 40–80% of TP and claimed it was the mainsource of plant P nutrients in the southeast Horqin sandy land.Pei et al. (2001) also demonstrated that Po was the main sourceof available P (AP) in meadow soil of the Qinghai-Tibet pla-teau; its content was above 300 mg kg−1, accounting for 50–84% of TP. Consequently, Po is the largest contributor of Pnutrients to plants (Bünemann et al. 2011), especially in grass-land and forest soils with low inorganic P (Pi) content.

The widespread Inner Mongolia steppe, a typical Eurasiansteppe, represents approximately 22% of the grassland inChina. Its climate features an obvious longitudinal zonal

distribution (Han and Li 2012; Klaus et al. 2016): from westto east, the temperature decreases but precipitation increasesgradually, and the steppe type also changes from desert steppeto typical steppe to meadow steppe, which is mainly reflectedin the variation of the dominant vegetation structure (Fenget al. 2015; Niu 2000; Wang et al. 2016). The rich diversityin steppe and vegetation types highlights the indispensableposition of vegetation in ecosystem protection by providingsandstorm prevention, soil and water conservation, and cli-mate regulation (Lu 2012). However, some studies showedthat a lack of P has seriously restricted the productivity ofthe Inner Mongolia steppe (Elser et al. 2007; Shi 2013).Therefore, it is necessary to improve the availability of soilP in the Inner Mongolia steppe. Wang et al. (2019) studied thePo fractions in the formation process of Bavarian alpine forestsoil. The results showed that a large amount of Po in the soilwas fixed on calcareous parent material due to the long-terminput of coniferous tree organic matter, and the soil Po stocksin the organic layer could be considerably large, e.g., up to85 kg P ha−1 (Prietzel et al. 2015). Similarly, the soil types ofInner Mongolia grassland change from Calcic Xerosols toCalcic Kastanozems and then to Calcic Chernozems fromwest to east. The formation of these three types of soil in-volves different degrees of humus accumulation and calciumaccumulation, which have an important contribution to theformation of the soil Po pool (Han 2009; Han and Li 2012).Therefore, the key tomaintaining the sustainable developmentof the Inner Mongolia steppe is to improve the utilization rateof Po in steppe soil, but the distribution characteristics of thefractions and stocks of Po in the whole Inner Mongolia steppeare unknown at present.

The original sequential extraction procedure, developed byBowman and Cole (1978), has been considered to be suitablefor distinguishing different activity’s Po fractions across dif-ferent soil types, especially which can distinguish the fulvicand humic substances. Despite the disputes in chemical Pfractionation (Barrow et al. 2020; Gu and Margenot 2020),the method is still in vogue. This P fractionation includesNaHCO3-extractable Po (NaHCO3-Po), HCl-extractable Po(HCl-Po), and NaOH-extractable Po (NaOH-Po) which repre-sent labile Po, moderately labile Po, moderately stable Po(NaOH-Po, without precipitation), and stable Po (NaOH-Po,with precipitation), respectively. A large number of studieshave shown that HCl-Po and NaOH-Po are the main Po frac-tions in soil under natural vegetation conditions (Chen et al.2014; Dong 2008). Po fractions play varied roles in P supplybecause of their different activities, e.g., labile Po is the sourceof soil available P (AP), and stable Po is a sink of soil AP(Cabeza et al. 2019; Sales et al. 2017; Sharpley and Smith1985). H2O-extractable Po (H2O-Po), as a part of labile Po,can provide available nutrients for plants in natural grasslandand forest soils and is significantly related to soil organicmatter (SOM) and pH (Ciampitti et al. 2011; MacDowell

J Soil Sci Plant Nutr

2007). Phytate P (Phyt-P), as a part of the stable Po fraction,accounts for 30–60% of Po; it can be used as a soil P sink, andwhen the content of soil AP is low, Phyt-P can be hydrolyzedinto an orthophosphate by phytase produced by plants andmicroorganisms, enabling plant uptake and utilization(Azeem et al. 2015). There are differences among the Po frac-tions contributing to soil P pools in different ecosystems. Thechanges in soil Po fractions are mainly caused by a change inmoderately labile Po in non-fertilized areas of disturbed grass-land (Zhang et al. 1990). The rapid growth of forage grass inlow-temperature grassland soil is associated with an increasein labile Po, high microbial activity, and low residual P levels.This indicates that the less available Po residues are convertedinto the more available labile Po under the action of microor-ganisms, thus continuously providing the P needed for foragegrowth (Zhao et al. 2009). Sales et al. (2017) found that bothlabile and stable soil P pools were significant sources of soilAP, which mainly depended on the content of SOM. Soil withlow to medium SOM content and a labile P pool was the mainsource of AP, while soil with a high SOM content and APdepended on the stable P pool to a great extent. However, wehave very limited knowledge about the contribution of Pofractions to soil AP in the Inner Mongolia steppe.

In this study, we investigated the variations of Po fractionsin three steppe types (desert steppe, typical steppe, and mead-ow steppe) in the Inner Mongolia of China. We aimed to (1)identify the contents and characteristics of high-bioavailabilityPo fractions in the three steppes using the fractionation proce-dure described by Bowman and Cole (1978) and compare thedistribution differences of Po fractions in the three steppes; (2)understand how these patterns vary among different Po frac-tions and the effects of environmental factors (i.e., climate,vegetation, soil properties) on the soil Po fractions using re-dundancy analysis (RDA); and (3) clarify the contribution ofPo fractions to soil AP in the Inner Mongolia steppe soil. Wehypothesized that soil Po fractions in the Inner Mongoliandesert, typical, and meadow steppes were significantly differ-entiated due to their differences in climate and vegetation. SoilPo fractions were closely related to soil pH and SOM content,which had a strong impact in determining the soil P supply.

2 Materials and Methods

2.1 Site Description

The study was conducted in the Inner Mongolia AutonomousRegion (37° 24′−53° 23′ N, 97° 12′−126° 04′ E). The totalarea is 118.3 km2, and it is dominated by a temperate conti-nental climate. The mean annual temperature (MAT) in thewhole region is 6.1 °C, and the mean annual precipitation(MAP) is 322.9 mm. Nearly 80% of the precipitation falls inthe summer (June–September). The spatial distribution of

steppe types in Inner Mongolia is determined by the distribu-tion of hydrothermal conditions. Desert steppe develops in atemperate arid climate, and vegetation is mainly composed ofperennial xerophytic tufted grass and a certain number ofstrong xerophytic subshrubs and shrubs. Typical steppe isformed in a temperate semi-arid climate and is the most rep-resentative and largest proportion of steppe types in semi-aridregions. Typical xerophytic perennial tufted grasses are thedominant vegetation. Meadow steppe develops in a temperatesemi-humid climate and is the wettest area of the steppe types.It is mainly composed of xerophytic perennials, rhizomatousgrasses, mesophytic weeds, and more or less mixed with me-sophytic shrubs. Because of its poor water condition, the pro-duction of vegetation in the desert steppe is lower than that ofthe typical steppe and meadow steppe.

The sampling area spans the whole InnerMongolian steppefrom Hohhot to Hulunbuir, covering three main steppe typesof grassland habitats: desert steppe, typical steppe, and mead-ow steppe (Fig. 1). The elevation ranges from 592 to 1447 m.From southwest to northeast, the temperature decreases (aver-age from 2.5 to − 1 °C), but the precipitation increases (aver-age from 210 to 400 mm) gradually. Meteorological data canbe downloaded from http://data.cma.cn/data/weatherbk.html.The MAP and MAT of each meteorological station in InnerMongolia from 2015 to 2019 were used to interpolate inArcGIS 9.2 software to obtain relevant meteorologicalparameters. More details are provided in the ElectronicSupplemental Material (ESM. Table S1).

2.2 Sampling and Sample Preparation

Soil samples were collected in July 2017. In total, 15 samplingsites were selected based on the steppe types and distance, andany two sampling sites were at least 50 km apart. Five sam-pling sites were selected in each steppe type, and three soilsamples were collected at intervals of 15 m at each samplingsite. Surface soils of 0–15-cm depths were randomly collectedwith a soil auger (5 cm in diameter). Each soil sample was acomposite sample mixed with at least 20 soil cores. In thelaboratory, after removing plant residues, roots, and stones,the soil samples were air-dried and sieved through a 2-mmmesh to thoroughly homogenize the soil before analysis.The soils in these sampling sites were mainly derived fromgranite. The dominant plant species and soil types (FAO-UNESCO 1974) were also identified at each site (Table 1).

2.3 Soil Physical and Chemical Properties

Soil pH was measured in a suspension with a 1:2.5 soil towater ratio (w/v) (Skjemstad and Baldock 2007). SOM wasdetermined by potassium dichromate digestion (Nelson andSommers 1982). The soil TP was determined by the HClO4-H2SO4 digestion method followed by colorimetric

J Soil Sci Plant Nutr

spectrophotometry (Thomas et al. 1967). Total Po was mea-sured by the ignition method (Saunders and Williams 1955).Soil AP was extracted with 0.5-M NaHCO3 (pH 8.5) at a soilto solution ratio of 1:20 (Olsen et al. 1954) followed by mo-lybdate colorimetry (Murphy and Riley 1962). Soil total N(TN) was determined by steam distillation after Kjeldahl di-gestion at 370 °C (Zhao et al. 2009). Soil alkali-hydrolyzed N(AN) was determined by the alkali-hydrolysis diffusion meth-od (Bao 2000). Soil texture was measured by a Malvern par-ticle size analyzer (Malvern Mastersizer 2000).

H2O-Po was extracted with deionized water (soil towater ratio of 1:10 (w/v)) and then filtered using a cellu-lose acetate membrane (0.45 μm) (Mai et al. 2017).NaHCO3-Po, HCl-Po, and NaOH-Po were sequentially ex-tracted by shaking 1.0 g of soil with 50 ml of 0.5-MNaHCO3 (pH 8.5), 1-M HCl, and 0.5-M NaOH for30 min, 3 h, and 6 h, respectively (Bowman and Cole1978). The filtrates were filtered through a 0.45-μm cel-lulose membrane filter. The TP concentration in each frac-tion was determined after digestion with potassium

persulfate and 0.9-M H2SO4 (Tiessen and Moir 1993).The Pi concentration in the extracts from each fractionwas measured by the colorimetric method using ascorbicacid (Murphy and Riley 1962). The Po was calculated bythe difference between TP and Pi in the extracts. Phyt-Pwas measured by the Hayes et al. (2000) method. Briefly,2.5 g of soil was added into a centrifuge tube and extract-ed with 50 ml of 0.5-M NaHCO3 solution for 30 min at180 rpm at 25 °C. The soil extract obtained by filtrationwas adjusted to pH 5.5, phytase solution (100 mg ofphytase powder dissolved in 30 ml of 2-N-morpholino-ethanesulfonic acid (MES)) was added, and the mixturewas incubated at 27 °C for 6 h. Then, 25% trichloroaceticacid solution was added to stop the reaction. At the sametime, a sample of the reaction was stopped before incuba-tion as a control. After stopping the reaction, the mixturewas centrifuged at 12,000 rpm at 4 °C, and the P contentin the supernatant was determined by the molybdenum-antimony colorimetric method. The difference betweenthe two results was the Phyt-P.

Fig. 1 The location of study areadistribution of sampling points

Table 1 The information of the different steppes in Inner Mongolia

Steppe types Sample No. Coordinates Soil types Vegetation

Desert steppe 5 N 41° 49.93′–N 43° 57.07′E 111° 53.84′–E 114° 38.69′

Calcic Xerosols Stipa breviflora Griseb; S. klemenzii Roshev

Typical steppe 5 N 44° 25.74′–N 46° 07.55′E 117° 00.53′–E 119° 12.82′

Calcic Kastanozems Leymus chinensis; S. grandis

Meadow steppe 5 N 49° 30.27′–N 49° 27.10′E 118° 15.77′–E119° 47.36′

Calcic Chernozems L.s chinensis; S. baicalensis

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2.4 Statistical Analysis

The coefficient of variation (CV) was used to express variation inan index,whichwas consideredweakwhenCV≤ 10%,moderatewhen 10%<CV<100%, and strongwhenCV ≥ 100% (Chartres1985). The distribution characteristics of the Po fractions in differ-ent steppe types are shown by a violin plot (Origin 2019). One-wayANOVAwas used to test for significant differences of soil Pofractions in the different steppe types. The Pearson correlation andredundancy analysis (RDA) were used to identify dependenciesamong Po fractions, climatic parameters (MAT, MAP), vegeta-tion (NDVI), and soil properties (SOM, pH, available N and P)(SPSS23.0). RDAbased onBray-Curtis distanceswas performedusing Canoco 5.0 (Microcomputer Power, Ithaca, NY, USA).Environmental factor effects were assessed through variancepartitioning based on the simple effect and conditional effect (λ-A) of each environmental variable, and ranking of the importanceof environmental factors was based on the significance of thedisplacement test (p value). The simple effect was defined asthe rate of change in the dependent variable when each environ-mental factor was used as an explanatory variable, while theconditional effect was determined by using environmental vari-ables as explanatory variables for RDA. Considering the collin-earity of some indicators, such as the general linear relationshipbetween SOM and TN, only SOM was considered.

3 Results

3.1 Soil Physical and Chemical Properties

The InnerMongolia grassland soil is sandy loamwith silt contentranging from 33.6 to 45.3% and clay content of just about 0.5%(Table 2). The variation in the pH value was very small (CV3.1%), with an average of 7.1. There were significant differencesin the nutrient contents of different steppe types except for TP(p< 0.05). The mean content of TP in the three steppe types was215.8 mg kg−1. The mean content of SOM was 23.8 g kg−1

(range 2.6–54.8 g kg−1), which varied significantly between dif-ferent steppe soils (CV 65.1%). The average content of SOMwas the highest in the meadow steppe, and it was approximatelyfive times higher than that in the desert steppe. The contents ofTN, AN, and AP showed the same variation trend: desert steppe< typical steppe < meadow steppe.

3.2 Distribution Characteristics of Soil OrganicPhosphorus Fractions

Po varied between 50.0 and 188.1 mg kg−1, accounting for28.8–81.8% of TP in the Inner Mongolia steppe soil (ESM,Table S2), and had a dispersed distribution in different steppetypes (Fig. 2a). The contents of Po increased significantly inthe order of desert steppe < meadow steppe < typical steppe.The soil Po fraction was dominated by NaOH-Po with an av-erage content of 61.7 mg kg−1 (19.3–89.2 mg kg−1), whichaccounted for 49.1% of Po on average, followed by HCl-Poand Phyt-P with an average content of 16.0 mg kg−1 and14.8 mg kg−1, respectively. H2O-Po was present at the lowestcontent of 0.5–2.3 mg kg−1 in the soil Po fractions, accountingfor only 0.9% of Po on average.

The contents of Po fractions varied among different steppetypes. Among them, the contents of H2O-Po and HCl-Po wererelatively stable in the three steppes except for some abnormalvalues (Fig. 2b, d) and had no significant differences amongthe three steppes (p > 0.05) (ESM, Table S3). The NaHCO3-Po content in the meadow steppe and the NaOH-Po content inthe three steppes showed a dispersed distribution (Fig. 2c, e).The variation in NaHCO3-Po was the largest (CV 113.0%).The content of NaHCO3-Po in the meadow steppe was thehighest (average 17.3 mg kg−1) and was 6 and 17 times higherthan that in the typical and desert steppes, respectively (ESM,Table S3). The content of Phyt-P showed moderate variation(CV 71.9%), especially in the typical steppe (Fig. 2f). Theaverage content of Phyt-P in the typical steppe was28.5 mg kg−1 and was 3 and 4 times higher than that in thedesert and meadow steppes, respectively (ESM, Table S3).

Table 2 Soil physical and chemical properties in Inner Mongolia grassland

Steppe types pH SOM TN TP AN AP Sand Silt Clay(g kg−1) (g kg−1) (mg kg−1) (mg kg−1) (mg kg−1) (%) (%) (%)

Desert steppe 7.2 ± 0.3 a 8.0 ± 5.3 c 0.7 ± 0.3 b 206.1 ± 65.8 a 24.4 ± 16.8 c 5.2 ± 1.6 c 64.9 ± 15.0 a 33.6 ± 2.2 a 0.3 ± 0.3 a

Typical steppe 7.3 ± 0.1 a 24.4 ± 3.1 b 1.7 ± 0.2 ab 236.5 ± 84.6 a 71.5 ± 8.1 b 9.1 ± 1.5 b 60.7 ± 10.8 a 38.9 ± 2.5 a 0.4 ± 0.1 a

Meadow steppe 6.9 ± 0.1 b 39.0 ± 16.1 a 2.2 ± 0.7 a 204.8 ± 41.1 a 108.5 ± 32.1 a 16.3 ± 3.9 a 54.2 ± 11.2 a 45.3 ± 1.9 a 0.6 ± 0.5 a

CV (%) 3.1 65.1 47.7 28.3 57.8 50.7 20 29.1 81.8

a SOM, soil organic matter; TN, total nitrogen; TP, total phosphorus; AN, available nitrogen; AP, available phosphorus; CV, coefficient of variationbData represent mean ± standard deviation (n = 5)c ANOVA was used to test the differences among the steppe types. Different lowercase letters (a, b, c) in the same column represent significantdifferences at p < 0.05

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3.3 Relationships Between the Soil OrganicPhosphorus Fractions and Environmental Factors

Environmental factors had a significant effect on soil Po fractions(p< 0.05) (Table 3). H2O-Po, NaHCO3-Po, and HCl-Po were allsignificantly correlated with MAT, MAP, and NDVI, whichindicated that soil Po fractions were not only affected by soilproperties but also closely related to climatic conditions and veg-etation. H2O-Po, NaHCO3-Po, and NaOH-Po were positivelycorrelated with SOM and TN, with Pearson correlation coeffi-cients (r) between 0.58 and 0.82 (p < 0.01). H2O-Po andNaHCO3-Po also had positive correlations with AN, whileHCl-Po had a negative correlation with AN. NaHCO3-Po andHCl-Po were significantly correlated with soil pH (p< 0.05).

There was no significant correlation between soil Po frac-tions and soil TP (p > 0.05). NaHCO3-Po was positively

correlated with AP (r = 0.86, p < 0.01), which indicated thatNaHCO3-Po was an important source of soil AP. However,HCl-Po was negatively correlated with AP (r = − 0.56,p < 0.05). NaOH-Po and Phyt-P were positively correlatedwith NaHCO3-extractable Pi (NaHCO3-Pi), and their correla-tion coefficients were 0.58 and 0.56, respectively (p < 0.05).Phyt-P was also negatively correlated with HCl-extractable Pi(HCl-Pi) (r = − 0.61, p < 0.05).

3.4 Explaining the Variance in Soil OrganicPhosphorus Fractions

RDA was used to further explain how environmental factorsinfluenced the Po fractions. The results showed that the distri-bution of soil Po fractions was obviously separated by steppetype (Fig. 3). The examined environmental factors explained

Fig. 2 Soil organic phosphorusfractions in Inner Mongoliagrassland. a Po. b H2O-Po. cNaHCO3-Po. d HCl-Po. e NaOH-Po. f Phyt-P. H2O-Po, NaHCO3-Po, NaOH-Po, and HCl-Porepresent organic phosphorusextracted by deionized water, 0.5-MNaHCO3, 1-MHCl, and 0.5-MNaOH, respectively. Phyt-P,phytate phosphorus

J Soil Sci Plant Nutr

85.7% of the variations in the Po fractions (Table 4). Simpleeffect analysis showed that MAT,MAP, NDVI, and soil prop-erties (pH, SOM, AP, and AN) all had significant effects onthe Po fractions (p < 0.01) (ESM, Table S4). RDA1 and RDA2explained 56.0% and 18.0% of the Po fraction variation, re-spectively. Conditional effect analysis showed that MAT, pH,NDVI, and AP were significant factors in shaping the soil Pofractions distribution, and respectively explained 49.3%,13.6%, 11.1%, and 6.7% of the total variances observed inthe Po fractions (p < 0.05). However, we found the Po fractionsmainly diverged along the RDA1. Along the RDA1, MATwas regarded as the main environmental driving force affect-ing Po fractions, which explained 49.3% (p = 0.002) of thevariations in the Po fractions.

4 Discussion

4.1 Distribution Characteristics of Soil PhosphorusContent

This study showed that the average TP content of steppe soilin Inner Mongolia was 215.8 mg kg−1, with P mainly in theform of Po, which accounted for 61.0% of TP (ESM,Table S2). Tyer (2002) surveyed 110 grassland sample sites

in southeastern Sweden, which had a TP of 328–596 mg kg−1

and Po accounted for 49.5–77.3% of the TP. Nash et al. (2014)reported that the average TP content of grassland soils inEurope and the USA was 939–1533 mg kg−1, with Po ac-counting for 22.76–40.68% of TP. Feng et al. (2016) investi-gated 52 sites across arid and semi-arid grasslands of northern

Table 3 Correlation coefficients between soil organic phosphorusfractions and environmental factors

P fractions H2O-Po NaHCO3-Po

HCl-Po NaOH-Po

Phyt-P

MAT − 0.53* − 0.85** 0.74** − 0.3 − 0.34MAP 0.69** 0.74** − 0.63* 0.45 0.38

NDVI 0.71** 0.79** − 0.59* 0.5 0.38

pH − 0.35 − 0.59* 0.74** 0.09 0.2

SOM 0.58* 0.82** − 0.49 0.58* 0.34

TN 0.59* 0.82** − 0.48 0.59* 0.31

TP 0.16 0.09 0.16 0.31 − 0.08AN 0.57* 0.80** − 0.55* 0.51 0.27

AP 0.50 0.86** − 0.56* 0.43 0.21

H2O-Pi 0.05 0.52* − 0.34 0.3 − 0.1NaHCO3-Pi 0.05 0.25 0.13 0.58* 0.56*

HCl-Pi 0.03 − 0.11 0.28 0.08 − 0.61*

NaOH-Pi − 0.02 − 0.41 0.5 0.47 0.41

aMAT, mean annual temperature; MAP, mean annual precipitation;NDVI, normalized difference vegetation index; SOM, soil organic matter;TN, total nitrogen; TP, total phosphorus; AN, available nitrogen; AP,available phosphorus; H2O-P, NaHCO3-P, HCl-P, andNaOH-P representphosphorus extracted by deionized water, 0.5-MNaHCO3, 1-MHCl, and0.5-M NaOH, respectively; Po, organic phosphorus; Pi, inorganic phos-phorus; Phyt-P, phytate phosphorusb* p < 0.05; ** p < 0.01 (Pearson correlation coefficient, n = 15)

Fig. 3 The effects of soil properties, vegetation, and climatic conditionson soil organic phosphorus fractions based on the RDA. SOM, soilorganic matter; AN, available nitrogen; AP, available phosphorus;MAT, mean annual temperature; MAP, mean annual precipitation;NDVI, normalized difference vegetation index

Table 4 Variation portioning into organic phosphorus fractionsexplained by soil properties (pH, AP, SOM, and AN), vegetation(NDVI), and climatic parameters (MAT and MAP)

Environmental factorsa % of all variationb pc

MAT 49.3 0.002**

pH 13.6 0.012*

NDVI 11.1 0.008**

AP 6.7 0.024*

SOM 2.0 0.390

AN 1.7 0.488

MAP 1.3 0.570

Total 85.7

a SOM, soil organic matter; AN, available nitrogen; AP, available phos-phorus; MAT, mean annual temperature; MAP, mean annual precipita-tion; NDVI, normalized difference vegetation indexb Environmental factors’ effect was assessed through variancepartitioning based on the conditional effect (λ-A) of each environmentalvariable. Forward selection on 499 permutations was used to test thesignificant contributions of each factorc* indicates significant difference at p < 0.05; ** indicates significantdifference at p < 0.01

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China with TP contents of 300–600 mg kg−1, but Po

accounted for only 19% (4–55%) of the TP on average. TheTP contents in that study were much higher than those in ourstudy, but the proportions of Po were much lower than in ourstudy. Consequently, mineralization of Po might be a limitingprocess in soil P cycling in the Inner Mongolia steppe. Thisresult differs frommost of the previous studies that have dem-onstrated the importance of Pi and geochemical controls onsoil P cycling in arid and semi-arid grassland and shrubland(Cross and Schlesinger 2001). Walker and Syers (1976) re-ported that TP decreased continuously with increasing pedo-genesis, and natural soil P was almost entirely derived fromgeochemical weathering of soil parent materials due to lowatmospheric deposition return (Chadwick et al. 2003). In thisstudy, different steppe soils have the same parent material, i.e.,granite, so their TP contents are similar. Feng et al. (2016)proved that TP decreased initially and then increased withdecreasing aridity, and Po, with the highest value in meadowsteppe, gradually increased along the climosequence. We ob-tained a similar result for Po content (ESM, Table S2), whichwas nearly 50% higher in the typical and meadow steppesthan that in the desert steppe. It can be concluded that thecontents of TP and Po in the soil are related to the parentmaterial, steppe type, geographical location, and climaticconditions.

The form of soil P could be associatedwith calcium contentin basic soil (Cross and Schlesinger 2001; Motaghian et al.2019), and calcium phytate as an important component ofstable Po is soluble at pH < 6.0 (Fan and Li 2004), whichmay be a result of the high content of HCl-Po. However, thesoil Po fraction was dominated by NaOH-Po (ESM, Table S1)in this study. We found the content of HCl-Pi was very high(average 66.9 mg kg−1) (ESM, Table S2), suggesting Ca-bound P mainly existed in an inorganic form. These resultssupport the study of Lajtha and Schlesinger (1988), whichshowed that geochemical processes dominate P cycling insemi-arid soils when calcium carbonate (CaCO3) is abundantin the soil profile. However, P availability to plants and themicrobial biomass is determined by the labile, surface-adsorbed phosphate, rather than the CaCO3-bound, crystallineforms in the steppe soil, and the availability of crystallineforms is minimal owing to the low surface area of calciumphosphates (Cross and Schlesinger 2001). It is an intriguingfact that Phyt-P was below the detection limit in all of oursoils, as it is considered to be widely distributed as a predom-inant form of Po in soils (Doolette et al. 2011; Turner et al.2003). Previous studies attributed the absence of Phyt-P inwetland soils and peats to anaerobic conditions, which led torapid Phyt-P decomposition (Turner et al. 2007a, b). Thisstudy found no evidence of permanent perched water tablesor water saturation, even though a high water storage capacitywas exhibited (Prietzel et al. 2013). Presumably, the reason forthe absence of Phyt-P was simply that the current vegetation

species and microorganisms did not contribute to an input ofPhyt-P. Thus, it cannot be generalized that Phyt-P is abundantin all soils (Turner et al. 2007a). However, the content of Phyt-P was higher in the typical steppe than in the other steppes,which indicated that the accumulation of Phyt-P was morefavorable in the typical steppe.

4.2 Effects of Environmental Factors on Soil OrganicPhosphorus Fractions

In this study, the contents of the Po fractions in the three steppetypes had significant differences (ESM, Table S3). RDA alsoshowed that the distribution of soil Po fractions was differentfor different steppe types (Fig. 3), indicating that this differ-ence wasmainly caused by the steppe type. From southwest tonortheast in the Inner Mongolia steppe, the temperature de-creases but the precipitation increases gradually, and thesteppe type also changes from desert steppe to typical steppetomeadow steppe, which is mainly reflected in the variation indominant vegetation structures, soil types, and their properties(Feng et al. 2016; Niu 2000; Wang et al. 2016); these are themain differences between steppe types caused by climaticfactors (Alvarez and Lavado 1998; Feng et al. 2016). RDAproved that MAT and MAP could explain approximately49.3% and 40.1% of the variation in soil Po fractions, respec-tively (ESM, Table S4), which was consistent with the hy-pothesis. These results also support the view that the availabil-ity of Po depends primarily on seasonal patterns of precipita-tion and temperature, which affect microbial activity and min-eralization (Dormaar 1972; Eid et al. 1951;Magid and Nielsen1992; Westin 1978).

Plants access mineral P from deep soil, translocate it fromtheir roots to the shoots, and subsequently deposit the Po in thetopsoil as litter (Bol et al. 2016; Borie et al. 2019; Chadwicket al. 2007; Ippolito et al. 2010). Soil microorganisms associ-ated with vegetation release the available P into the soilthrough dissolution of P-containing minerals and mineraliza-tion of Po, but they also immobilize available P through mi-crobial uptake and anabolism (Achat et al. 2010; Obersonet al. 2001; Turner et al. 2013). Therefore, P transformationand distribution in unfertilized soils are largely controlled bythe vegetation during soil genesis and ecosystem succession.The low NDVI in the desert steppe (ESM, Table S1) led to asignificant decrease in organic inputs such as litter entering thesoil and photosynthetic carbon entering from root systems,which directly led to the decrease in SOM and the stark de-crease in Po content. The significant positive correlation of Pofractions with the NDVI and SOM (Table 3) supports thisidea. In addition, variations in soil Po fractions among vege-tation types can be attributed to changes in nutrient cyclingprocesses associated with vegetation conversion (Hooper andVitousek 1998). The content of NaHCO3+Po increased in theorder of desert steppe < meadow steppe < typical steppe (Fig.

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2c), while the typical steppe had higher contents of HCl-Po,NaOH-Po, and Phyt-P (Fig. 2d–f), which indirectly supportthe results of plants varying in their capacities of accessingdifferent Po forms in soils (Ahmad-Ramli et al. 2013;Ceulemans et al. 2017; Steidinger et al. 2015; Turner 2008).Thus, the clarification of mechanisms underlying the varia-tions in soil P fractions needs further quantification of P allo-cation and cycling processes in different vegetation types.

At the same time, the three soil types involved in this studywere formed through different degrees of humus and calciumaccumulation.With the soil type changes from Calcic Xerosolto Calcic Kastanozem to Calcic Chernozem, the process ofhumus accumulation is increasingly obvious, and the contentof SOM increases. Pearson correlation analysis showed thatPo fractions had a significant positive correlation with SOM(Table 3), which is consistent with previous results. Sales et al.(2017) used SEM to estimate the relationship between the soilP cycle and soil properties, and the results showed that therewas a strong correlation between the soil P pool and SOM.

The results of this study support the hypothesis that contin-uous accumulation of soil SOM could essentially lead to bind-ing of the P pool, thus reducing soil P availability and leadingto P limitations for plant growth (Huang et al. 2012;Schlesinger et al. 1998). Interestingly, RDA showed thatSOM explained only 2% of the variation in the Po fractionsin the conditional effects, which may be due to the climateeffects compensating for the SOM effects. SOM could explain43.7% of the variation in the Po fractions in the simple effectanalysis (p = 0.002) (ESM, Table S4). However, the aboveanalysis was based on the theory of humification. Wanget al. (2019) used one- and two-dimensional 31P-NMR tostudy the Po fractions in the 1500-year organic soil formationprocess of Bavarian alpine forest. They found that the long-term (1500 year) effect of SOM on Po fractions resulted fromthe continuous degradation of SOM and the continuous accu-mulation of stable small molecule monoesters, which eventu-ally occupied the Po pool. Therefore, 31P-NMR should beused in future studies, and the soil age should be considered.

The effect of pH on soil Po fractions is mainly reflected inthe change in solubility of Po fractions, the soil microbialcommunity, and enzyme activity (Zhao et al. 2008). Whensoil pH changes, the forms of P combined with iron, alumi-num, calcium, and other minerals in the soil and the Padsorbed with soil colloid will change due to the changes ofthe precipitation-dissolution balance and the adsorption-desorption balance of P (Javot et al. 2007). In acidic soils, Pcan be dominantly absorbed by Fe/Al oxides and hydroxidesas well as by clay minerals and form various complexes. Inalkaline soils, P retention is dominated by precipitation reac-tions, although P can also be adsorbed on the surface of Cacarbonate and clay minerals and become unavailable to plants(Ismat et al. 2018). As shown in the results of this study, pHhas a significant negative correlation with NaHCO3-Po and a

significant positive correlation with HCl-Po (Table 3), indicat-ing that the decline of soil pH would promote the transforma-tion of HCl-Po into NaHCO3-Po.

4.3 Relationships Between the Soil OrganicPhosphorus Fractions and Availability of Phosphorus

NaHCO3-Po and HCl-Po were the main Po fractions that great-ly contributed to AP in the InnerMongolia steppe soil. Amongthese, NaHCO3-Po was positively correlated with AP content(r = 0.86, p < 0.01) (Table 3), indicating that NaHCO3-Po isthe main source of soil AP and provided the P nutrient neededby plants, which is consistent with previous studies. Forexample, Grierson et al. (2004) showed that NaHCO3-Pohad a significant positive correlation with AP and was animportant source of soil AP. Sales et al. (2017) used SEM toestimate the relationship between the soil P cycle and soilproperties, which supported our results suggesting that thelabile soil P pool is an important source of soil AP. In addition,this study found that there was a significant negative correla-tion between HCl-Po and AP (r = − 0.56, p < 0.05) (Table 3).From desert steppe to meadow steppe, the vegetation coverageand aboveground biomass increased, and the content of HCl-Po may be transformed into NaHCO3-Po to meet plant de-mands as the SOM content increases (Cao et al. 2016).Correlation analysis also proved this point. There were nega-tive correlations of HCl-Po with NDVI and SOM (Table 3).Although NaOH-Po and Phyt-P were positively correlatedwith AP, the correlation was not significant (p > 0.05).Surprisingly, we found that NaOH-Po and Phyt-P were posi-tively correlated with NaHCO3-Pi (Table 3), and Phyt-P wasnegatively correlated with HCl-Pi (r = − 0.61, p < 0.05), whichsuggests these two fractions as a part of the stable pool areimportant to provide P to other P pools (i.e., this is a pool toreplenish the AP).

5 Conclusions

The organic phosphorus (Po) of steppe soil in Inner Mongoliaaccounted for 61.0% of the total phosphorus (TP) on averageand was dominated by NaOH-extractable Po (NaOH-Po)(mean 61.7 mg kg−1), while the H2O-extractable Po (H2O-Po) content was the lowest Po fraction (0.5–2.3 mg kg−1). Interms of H2O-Po and HCl-extractable Po (HCl-Po), there wereno significant differences among the three steppes. NaHCO3-extractable Po (NaHCO3-Po) showed an obvious increasingtrend of desert steppe < typical steppe <meadow steppe, whileNaOH-Po and phytate P (Phyt-P) showed an increasing trendmeadow steppe < typical steppe < desert steppe, which wasregulated by climatic conditions and was closely related to thesoil organic matter and pH. Po plays an indispensable role inthe supply of soil P in the semi-arid steppe of Inner Mongolia,

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among which NaHCO3-Po and HCl-Po greatly contributed toavailable phosphorus. NaOH-Po and Phyt-P as parts of thestable pool are important for providing P to NaHCO3-Pi andHCl-Pi. However, in order to better understand the process ofthe P cycle and the transformation mechanisms underlying thevariations in P fractions in steppe soils, further quantificationof P allocation and cycling processes in different vegetationtypes and 31P-NMR should be applied in future studies.

Funding Information This study was funded by the National NaturalScience Foundation of China (grant number 41877059).

Compliance with Ethical Standards

Conflict of Interest The authors declare that they have no conflict ofinterest.

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