Regulation of soil phosphorus cycling in grasslands by shrubs

Soil Biology and Biochemistry 133 (2019) 1–11

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Regulation of soil phosphorus cycling in grasslands by shrubs a

a,∗

a

Xiao-Li Gao , Xiao Gang Li , Ling Zhao , Yakov Kuzyakov a b c

T

a,b,c

State Key Laboratory of Grassland and Agro-ecosystems, School of Life Sciences, Lanzhou University, 222 South Tianshui Road, Lanzhou, 730000, China Department of Soil Science of Temperate Ecosystems, and Department of Agricultural Soil Science, University of Goettingen, Goettingen, Germany Institute of Physicochemical and Biological Problems in Soil Science, Russian Academy of Sciences, 142290 Pushchino, Russia

A R T I C LE I N FO

A B S T R A C T

Keywords: Fertile islands In situ soil phosphorus mineralization Microbial biomass phosphorus Organic phosphorus Shrub expansion Shrubby grasslands

The globally expanding colonization of grasslands by shrubs increases soil organic carbon and nitrogen, but the effects of shrubs on phosphorus (P) cycling have been rarely studied. We compared P contents in roots and soil fractions, phosphatase activity in the 1 m profile, and in situ net P mineralization between shrubby Potentilla fruticosa patches and grassy interspaces in grazed shrubby meadows at three representative sites on the eastern Tibetan Plateau. The P uptake of P. fruticosa exceeded 1 m soil depth, whereas grasses acquired P mainly within the upper 0.6 m. The P contents in shoots, aboveground litter and roots under P. fruticosa were greater than those under grasses. Litter P stock under the shrubs was 4–8 times higher than that under grasses and the root P stock doubled compared to that in grass areas. P. fruticosa generally increased the organic P (OP) content in the topsoil but decreased inorganic P (IP) in the subsoil. Phosphorus availability increased in the topsoil but decreased in the subsoil under the shrubs compared to grasses. Microbial biomass P (MBP), the activities of acid and alkaline phosphatases, and OP lability were all greater in the 1 m soil under P. fruticosa than grasses, leading to faster P mineralization and the P turnover under the shrubs. In the 1 m soil, P. fruticosa increased MBP and OP stocks but decreased IP and available P stocks. The larger and deeply distributed root system of P. fruticosa improved its P uptake ability especially from the subsoil. The subsequent greater organic matter input through litter fall and root turnover under P. fruticosa fed a larger microbial biomass that synthesized more microbial-derived OP in the topsoil. We concluded that shrubs increase the biological (plant and microbial) P transformation in the soil, the P uplift in the profile, and P cycling in shrubby grassland ecosystems. Such mechanisms structuring spatial heterogeneity of P content, transformation, turnover and fluxes are common in shrubby grasslands worldwide.

1. Introduction Phosphorus (P) is one of the most limiting nutrients for plants worldwide. The primary P source for ecosystems is from the weathering of P-containing minerals (Walker and Syers, 1976; Weihrauch and Opp, 2018). The biogeochemical cycle of P in natural ecosystems differs from that of carbon and nitrogen, which originate primarily from the atmosphere through photosynthesis, biotic fixation and abiotic deposition. During ecosystem succession, P is depleted through plant biomass removal, leaching and erosion (Walker and Syers, 1976; Izquierdo et al., 2013). In unfertilized soils, this loss of P cannot be compensated for. Thus, the P availability for primary productivity becomes increasingly restricted with ecosystem succession (Elser et al., 2007). Investigating P transformation and availability in soil is an important step forward in explaining the formation of communities and productivity in terrestrial ecosystems (Turner et al., 2007). Plants access mineral P from deep soil, translocate it from roots to

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shoots, and subsequently deposit the organic P in the topsoil as litter (Chadwick et al., 2007; Ippolito et al., 2010; Bol et al., 2016). Soil microorganisms associated with vegetation release available phosphates into soil through dissolution of P-containing minerals and mineralization of organic P, but also immobilize available P through microbial uptake and anabolism (Oberson et al., 2001; Achat et al., 2010a; Turner et al., 2013). Therefore, P transformation and distribution in unfertilized soils are largely controlled by the vegetation during soil genesis and ecosystem succession. Vegetation patterns comprising shrubby and grass patches are present in a wide variety of ecosystems, from savanna to tundra (Ravolainen et al., 2013; Becker et al., 2017; Stevens et al., 2017). Due to overgrazing, fire suppression, rising atmospheric CO2 concentration and increasing droughts, the distribution of woody plants in arid and semiarid ecosystems is expanding worldwide (Eldridge et al., 2011; Stevens et al., 2017). The biological characteristics of shrubby and grass plants differ with regard to life spans, photoassimilate allocation

Corresponding author. E-mail address: [email protected] (X.G. Li).

https://doi.org/10.1016/j.soilbio.2019.02.012 Received 4 September 2018; Received in revised form 15 February 2019; Accepted 19 February 2019 Available online 23 February 2019 0038-0717/ © 2019 Elsevier Ltd. All rights reserved.

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grasses (He and Li, 2016). Our overall objective was to investigate the mechanisms of P transformation, accumulation, spatial redistribution and cycling under shrubs compared to those under grasses in meadows.

patterns and tissue chemical composition, etc (Gavrichkova et al., 2018). These differences strongly affect ecosystem processes such as soil organic matter and nutrient dynamics (Hobbie, 1992; Eldridge et al., 2011; Holdo and Mack, 2014; Blok et al., 2018; Leitner et al., 2018). Consequently, the spatial mosaic of shrubs common in various arid, semiarid, and even in more mesic grasslands leads to significant nutrient heterogeneity (islands of fertility) (Garner and Steinberger, 1989; McCarron et al., 2003; Dossa et al., 2010). The mechanisms of nutrient redistribution and especially the increase of P availability in soil under shrubs are not clear. Previous studies investigated the effects of shrubby embedment in grass-dominated ecosystems on soil processes mostly within the topsoil layer (< 0.3 m). The resulting general perception is that shrubs redistribute P and accumulate it from the interspaces to the shrub-vegetated areas (Collins et al., 2014; Schlesinger and Pilmanis, 2010; Ochoa-Hueso et al., 2017). By sampling the soil down to 1–1.2 m, however, recent studies (He and Li, 2016; Zhou et al., 2018a, b) showed that woody patches within grasslands increased P in the upper layers due to P uplift by deep roots. Consequently, shallow soil sampling is unable to tell the complete story. On the Tibetan Plateau, the shrubby grasslands represent the most abundant vegetation types (Wang et al., 2006, 2012). The distribution of shrubs is currently also extending due to the on-going climate warming (Zhao et al., 2011; Gao et al., 2016; Carboni et al., 2018) and intensive grazing. Climate warming and the concurrent grazing intensification are accelerating the release of soil nutrients (Rui et al., 2012; Haynes et al., 2014; Liu et al., 2018a). Neglecting the shrub-induced nutrient heterogeneity may introduce large uncertainties and hamper the precise modeling of ecosystem processes. Characterizing soil nutrient cycling under shrubby and grass plants is crucial for understanding the mechanisms behind the formation of the communities and productivity of shrubby grasslands. Potentilla fruticosa L. (Rosaceae) is a key shrub species in meadows on the Tibetan Plateau. A distinct heterogeneity in soil organic C and nutrient availabilities characterizes P. fruticosa patches (He and Li, 2016). The increase in the total P content in the topsoil in such patches (relative to surrounding grass areas) occurs at the expense of lower P levels in the deeper soil layers under P. fruticosa. The mechanisms behind this finding remain to be explained in detail. Plant traits serve as a powerful tool for understanding the mechanisms behind plant–soil interactions and ecosystem functioning (Orwin et al., 2010). The effect of plants on the soil environment is positively correlated with plant size (Farley and Fitter, 1999; McClaran et al., 2008; Dossa et al., 2010). The soil P heterogeneity induced by P. fruticosa in meadows (He and Li, 2016) can be associated with its root morphological and physiological properties as well as soil microbial characteristics compared to grasses. In the present study, three independent winter-season grazed meadows were used to separate total P in the 1 m soil profile under compact P. fruticosa patches and grass areas. Total P was separated into organic (OP) and inorganic P (IP) pools to deduce differential effects of shrubs and grasses on soil P transformation (from inorganic to organic form) in meadows. Soil OP was further separated into sub-pools based on extractabilities to assess the effects of vegetation patches on OP lability. The plant root P stock, soil microbial biomass P (MBP) content and phosphatase activity in the 1 m profile, and in situ soil P mineralization, were determined to compare the effects of vegetation patches on biological P cycling. We hypothesized that (1) the shrub P. fruticosa has a greater ability to acquire P from deep soil than grasses because of its much deeper root system; (2) P. fruticosa has a greater capacity to transform soil P from inorganic to organic form because of its larger litter input; (3) OP is more labile in soil under P. fruticosa due to the accumulation of microbially derived OP and higher phosphatase activity, and consequently (4) P mineralization and turnover is faster in P. fruticosa soils than in those inhabited solely by grasses. These hypotheses were based on the findings that P. fruticosa has a larger and deeper root system and a greater aboveground litter accumulation than

2. Materials and methods 2.1. Site description The experiments were conducted at three sites: Maikecun (N33°40′, E101°52′, 3470 m above sea level), Nuoerlong (N33°50′, E101°51′, 3636 m a.s.l) and Yelong (N33°54′, E101°57′, 3474 m a.s.l.) in Maqu county, Gannan Tibetan Autonomous Prefecture, Gansu province, on the eastern edge of the Qinghai-Tibetan Plateau. The site Maikecun is very close to the Lanzhou University Research Station of Alpine Meadow and Wetland Ecosystems. The mean annual temperature at the station is 2.2 °C, the mean rainfall 672 mm. The distances from Maikecun to Nuoerlong and Yelong are 19.4 and 26.8 km, respectively, and from Nuoerlong to Yelong 10.3 km. The soils at all three sites are developed from loess-like materials, and are classified as alpine meadow soils according to the Chinese Soil Classification System (Institute of Soil Science, 1986), similar to Cryaquolls (Soil Survey Staff, 1975). Across all three sites, the soil organic carbon content in the 1 m soil profile decreased from 101 to 112 g kg−1 in the topsoil (0–0.2 m) to 10.3–12.0 g kg−1 in the lowest layer (0.8–1 m) in P. fruticosa patches. The corresponding values in grass patches were 94.0–98.8 g kg−1 to 7.9–10.9 g kg−1. The vegetation at the three sites was similarly composed of P. fruticosa (height about 0.5–0.7 m) and grass species including Kobresia spp., Elymus sp., Stipa spp., Poa sp., Saussurea spp., Roegneria sp. and some other species with minor abundance (Fig. 1). P. fruticosa formed compact patches (0.5–1 m diameter; or these merged to form larger areas) that were embedded into the grass matrix (Fig. 1). P. fruticosa is a long-living, slow-growing shrub; no mortalities were observed in the field. At all three sites, the meadows were used for grazing yaks (Bos grunniens) and sheep (Ovis aries) in the winter season (November–May). 2.2. Phosphorus fractions and phosphatase activity in the soil profile In August 2016, we established a 50 m × 50 m plot for plant and soil sampling in a flat, well-vegetated area at each of the three sites (Nuoerlong, Maikecun, Yelong). Within each plot, we randomly selected three circular areas (each about 8 m in diameter) with P. fruticosa as replicates. In P. fruticosa patches, soils were sampled from 5 points using an auger (38 mm inner diameter) at a 0.2 m interval down to the depth of 1 m, after removal of understory grasses and litter. Soil subsamples at the same depth were pooled to form a composite sample. Around the P. fruticosa patches, soils in the grass area (1.5 m away from

Fig. 1. Photograph shows shrub-embedded (Potentilla fruticosa) meadows in investigated areas. 2

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edges of P. fruticosa patches) were also sampled from 5 points using the auger, after removing plants and litter. Similarly, soil subsamples at the same depth were bulked to form a composite sample. Soil samples were paired between areas within P. fruticosa patches and around the P. fruticosa patches within the plot. At each site, under this sampling scheme, we formed an block-structured design of 2 types of vegetation patches (densely growing P. fruticosa patches and grass-only areas) × 5 soil depths × 3 replicates (blocks) (= 30 soil samples) to explore the distributions of total soil P and its fractions as well as the other related parameters in the soil profile. Soil samples were transported on ice to the laboratory. After removing the roots, all soil samples were sieved through a 2-mm aperture screen. One portion was stored in a refrigerator at 4 °C for analyses of soil MBP, acid and alkaline phosphatase activities and available P (AP) content at the field moisture level. These analyses were completed within 10 days after sampling. The other portion of each sample was air-dried at room temperature and used to determine soil pH (using a pH meter; soil:water = 1:2.5) and particle-size composition by the pipette method (Institute of Soil Science Academia Sinica, 1978). A small fraction of each air-dried soil sample was further ground to < 0.15 mm for analysis of total and IP contents. Soil MBP was determined using a chloroform fumigation-extraction method (Brookes et al., 1982; Morel et al., 1996). Briefly, 2 mL ethanolfree CHCl3 was added to each moist soil sample (equivalent to 5 g ovendried weight) in a 50 mL glass beaker. Beakers containing chloroformadded soils were evacuated with a high vacuum pump for 15 min in a desiccator containing a beaker with additional 50 mL CHCl3 and were then incubated for 1 h in the desiccator in the dark at 25 °C. After complete removal of residual CHCl3 from fumigated soils, the fumigated and non-fumigated samples were shaken for 30 min in the 0.03 M NH4F + 0.025 M HCl extractant (Bray-1) at a soil:solution ratio of 1:10 (Khan and Joergensen, 2012). Simultaneously, another portion of each moist soil sample was used to detect the recovery of MBP, with 50 mg P kg−1 (as KH2PO4) added. After filtration, IP in all Bray-1 extracts was determined with the ammonium molybdate spectrophotometric method at 700 nm (UV–1800, MAPADA, Shanghai, China). MBP was calculated based on the difference in the IP extracted from fumigated and non-fumigated samples divided by 0.4 and then by recovery (79–95% across all samples) (Khan and Joergensen, 2012). The activities of acid and alkaline phosphatases (phosphomonoesterases) were assayed by colorimetric determination of p-nitrophenol (PNP) released when soil was incubated with p-nitrophenyl phosphate in pH 6.5 or 11 buffers, respectively, for 1 h at 37 °C (Tabatabai, 1982; Hopkins et al., 2008). Moist soil equivalent to 1 g oven-dried weight was placed into 30-mL glass vials containing 4 mL of buffer and 1 mL of substrate solution, and incubated. After incubation, 1 mL of 0.5 M CaCl2 and 4 mL of 0.5 M NaOH were added to slurries to terminate enzymatic reactions. Immediately after filtration, the absorbance of enzyme extracts was measured at 410 nm (UV–1800, MAPADA, Shanghai, China). AP was extracted using 0.03 M NH4F + 0.025 M HCl (Bray-1) solution from moist soil samples at a soil weight to solution volume ratio of 1:5 (Lu, 2000). Total soil P was determined colorimetrically after the digestion of air-dried soil (< 0.15 mm) in an HClO4eH2SO4 mixture (Lu, 2000). IP was extracted by shaking 1 g air-dried sample (< 2 mm) for 16 h in 50 mL 0.5 M H2SO4 (Bünemann et al., 2016), followed by colorimetric measurement of phosphate ions in the filtrates. This method for extracting IP was suitable for our soils developed from loess-like materials because the contents of ferric and aluminum oxides is low due to weak weathering under cold climate. The soil OP was defined as the difference between the total and inorganic P. We fractionated soil OP into labile (L-OP), moderately labile (MLOP), moderately resistant (MR-OP) and highly resistant (HR-OP) fractions, basically following a procedure by Bowman and Cole (1978) with minor modifications. L-OP was P extractable from dead soil microbial biomass and organic matter by using Bray-1 solution, after CHCl3

fumigation (Hedley et al., 1982). One g air-dried soil sample (< 2 mm) was fumigated with ethanol-free CHCl3, similar to what was done in the MBP determination. After complete removal of residual CHCl3, each fumigated sample was shaken for 30 min in 50 mL Bray-1 solution and filtered. After a perchloric–sulphuric acid digestion (Bowman and Cole, 1978; Lu, 2000), total P in the filtrates was colorimetrically measured. The L-OP was calculated as the difference between the total P in the digested extracts and available P content (see above, extracted with Bray-1) in soil. ML-OP, MR-OP and HR-OP fractions were extracted sequentially from one soil sample (Bowman and Cole, 1978; Lu, 2000). Two g air-dried soil (passing 2 mm aperture) was first shaken for 3 h in 100 mL 1 M H2SO4. After filtration, the OP in the filtrates (H2SO4-extracted OP) was determined by the increase in the inorganic P after the perchloric–sulphuric acid digestion. The H2SO4-treated soil sample on the filter paper was then rinsed with ethanol (95%), air-dried and then shaken for 6 h in 100 mL 0.5 M NaOH to extract residual OP. The IP in the NaOH extracts was directly measured. The sum of this IP and the above H2SO4-extracted OP was defined as the ML-OP. 50 mL of the NaOH extracts was acidified to a pH range of 1.0–1.8, left standing overnight and then filtered. The OP in the acidified filtrates was determined by the increase in the IP after the perchloric–sulphuric acid digestion and defined as the MR-OP. The total P in the NaOH extracts was measured after the perchloric–sulphuric acid digestion. The difference between the total P and the sum of IP and MR-OP in the NaOH extracts was defined as the HR-OP. In this fractionation, by summing up the four sub-fractions, we recovered 92% of soil OP, across all samples. The total of sub-factions was closely correlated to the OP content in the soil (r = 0.98, p < 0.001). In late April (close to the end of grazing season) 2018, within the plots sampled in August 2016 at each site, we measured litter accumulation on the soil surface. On each of three circular areas (diameter 8 m each), litter was collected from three squares (each 0.5 m × 0.5 m) in P. fruticosa patches and three in grass areas. Litter was oven-dried at 65 °C to constant weight. Root biomass was sampled from 3 points under either P. fruticosa or grasses using a root sampler (inner diameter 70 mm) to 1 m depth at 0.2 m increments. Three root subsamples were pooled to form a composite sample for each depth. After the soil was washed off the roots on a screen (aperture 1 mm), the roots were oven dried at 65 °C to constant weight. Soil bulk density was measured using cutting rings (volume 100 cm3, inner diameter 50 mm) from three profiles dug under either P. fruticosa or grasses, at each site. Each 1 m profile was divided into 5 depths at the 0.2 m increment. Within each depth, 4 soil cores were sampled using cutting rings. Soils were dried at 105 °C to constant weight. A small portion of each aboveground litter or root biomass sample was ground to powder in a ball mill and used to colorimetrically measure P after digestion in sulphuric acid– H2O2 (Lu, 2000). 2.3. Measuring in situ phosphorus mineralization in the topsoil In situ net P mineralization in the top 0.2 m soil layer was measured from May to October 2016 by incubating soil samples at original positions where they were sampled at the Maikecun site. Each incubation period was 1 month. Within a flat area of 100 m × 50 m, nine plots (each about 8 m × 8 m) were randomly defined. Within each plot, at the beginning of every incubation period, five PVC tubes (inner diameter 40 mm; length 200 mm; there were 20 evenly distributed holes with a diameter of 1 mm on the wall of each) were randomly inserted down to 0.2 m at five points to take soil in dense P. fruticosa patches (after removing herbaceous plants and aboveground litter). Tubes containing soil were tightly capped at the bottom and were then placed back in the 0–0.2 m layer at their original locations for in situ incubation. In gap areas between P. fruticosa patches, soils were sampled (about 1.5 m away from patch edges) and incubated as within the patches, using another five PVC tubes. Simultaneously, soils within P. fruticosa patches or grass-only areas were sampled at 5 points (close to 3

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3. Results

the respective 5 tubes) using an auger (inner diameter 38 mm) down to the 0.2 m. These subsamples were pooled to form a composite sample for either P. fruticosa or grasses in each plot. This material was used to determine the initial inorganic P content in the soil before incubation. At the end of incubation, the incubated soils in the five tubes were bulked to form one composite sample, for either P. fruticosa or grasses. This was used to measure inorganic P contents after one month incubation. In every incubation period, we did not find any waterlogged or saturated situation in tubes. Leaves and twigs of P. fruticosa, and leaves and stems of grasses, were dynamically sampled to measure plant biomass P concentrations from May to October 2016. The sampling time of plant aboveground biomass paralleled that of soil incubation. Soil samples were transported on ice to the laboratory. After removing plant residues, each composite soil sample was sieved through a 2 mm screen, thoroughly mixed and stored in a refrigerator at 4 °C. MBP and phosphatase activities for non-incubated soils and IP content for either incubated or non-incubated soils were measured within one week after sampling at the field moisture level. MBP and AP contents and phosphatase activities were determined using the aforementioned methods. Soil IP was extracted by shaking 1 g moist soil for 30 min in 50 mL 0.5 M H2SO4 (Achat et al., 2010b); IP in the filtrates was measured colorimetrically. The net P mineralization rate during an incubation period was calculated by dividing the difference in the IP concentration between the end and beginning of the incubation period by the number of days. Cumulative P mineralized by the end of an incubation period was calculated by summing the mineralized P in all incubation periods before and including the incubation period. Generally, P mineralization is difficult to detect due to strong sorption of the released inorganic P onto solid surfaces (Achat et al., 2010b). In our case, however, measuring in situ soil P mineralization using the above protocol was feasible because of the low contents of Fee and Al-oxides versus the high organic P content in the soil. Soil water content was measured by weighing the sample as taken from the field and after drying to constant weight at 105 °C. We used the data measured for non-incubated samples (taken at the initial day of each incubation duration) to represent the dynamics of soil moisture in shrub and grass patches in the field. We measured the on-site soil temperature from May to October in 2015. Four button-type soil temperature recorders (WatchDog B100, Spectrum Technologies Inc. Aurora, IL, USA) were separately placed at 0.075 m soil depth in two P. fruticosa patches and two grass patches. The recorders were set to record every 1 h starting from midnight every day. The daily soil temperature was calculated by averaging the 24 readings.

3.1. Soil properties and phosphorus content in litter and plant biomass At all three sites (Nuoerlong, Maikecun, Yelong), the soil particle size distribution down to 1 m depth was similar between P. fruticosa and grass-only patches (p ≥ 0.05) (Table S1). Soil bulk density was lower under P. fruticosa than in grass areas between P. fruticosa canopies and increased with depth (p < 0.05) (Table S2). Soil pH was ∼0.1 units lower under P. fruticosa than under grasses (6.56 vs. 6.66 at Nuoerlong; 6.63 vs. 6.76 at Maikecun; 6.45 vs. 6.60 at Yelong, averaged over soil depths) and increased with soil depth (p < 0.05) (Table S3). Across the three sites, the litter accumulation under P. fruticosa canopies (150–191 g DW m−2) was more than four times higher than in grass areas (38–39 g m−2) (p < 0.001) (Table S4). The P content in litter was 12–51% greater under P. fruticosa (0.71–1.13 mg g−1) than under grasses (0.47–0.98 mg g−1) (p < 0.001) (Table S4). Consequently, the aboveground litter P return in P. fruticosa patches (136–206 mg m−2) was four to eight times higher than in grass areas (18–39 mg m−2) (p < 0.001) (Table S4). At all three sites, the roots in the soil profile extended down to depths below 1 m under P. fruticosa but only down to 0.6 m under grasses (Fig. S1). In the topsoil (upper 0.4 m), root P concentrations were 10–37% greater under P. fruticosa than under grasses (p < 0.05) (Fig. 2a). In the 1 m soil profile, the root P stock under P. fruticosa doubled compared with areas beyond such patches (Fig. 3a). At the Maikecun site, the P content in leaves was 34% greater for P. fruticosa (leaves and twigs) than for grasses (leaves and stems), averaged over sampling dates (Fig. 2b). 3.2. Phosphorus fractions and phosphatase activity in the 1 m soil profile At each site, the effects of vegetation patch type on the measured parameters generally changed with soil depth (interaction between vegetation patch type and soil depth; Figs. 4–6). Total P concentration in the top 0.4 or 0.6 m under P. fruticosa increased compared to that under grasses (p < 0.05; Fig. 4). P. fruticosa increased OP generally in the topsoil and decreased IP in the subsoil compared to grasses (p < 0.05; Fig. 4). The AP content in the topsoil was greater (but in the subsoil smaller) under P. fruticosa versus grasses (p < 0.05; Fig. 4). The MBP content in the topsoil and its proportion in the OP in the whole profile were generally greater under P. fruticosa (p < 0.05; Fig. 5). Both acid and alkaline phosphatase activities in the whole 1 m soil profile were generally greater under P. fruticosa than under grasses (p < 0.05) (Fig. 5). Across vegetation types, OP, AP and MBP all decreased with soil depth, whereas the IP content increased with depth (Fig. 4; Fig. 5). In the top 0.4 m, more than 80% of total soil P was present as OP at all three sites (Fig. 4). Total P stock in the 1 m soil was similar between vegetation patch types at Nuoerlong and Yelong but was marginally smaller under shrubs than under grasses at Maikecun (Fig. 3b). Across the sites, the stock of OP was generally 4–8% higher in shrubby patches; in contrast, stocks of IP and AP were lower by 7–15% and 21–36%, respectively, under shrub compared to grasses (Fig. 3c, d, e). The MBP stock was increased by 26–55% and its proportion in the OP by 40–47%, in shrub versus grass areas (Fig. 3f).

2.4. Statistical analysis At each site, two-way analysis of variance (ANOVA) was conducted to test the effects of vegetation type and soil depth (fixed factors) on the investigated parameters, with a consideration of a block-structured sampling design. One-way ANOVA was used to compare means of the stocks of litter, root and P fractions between vegetation patch types within each site. At the Maikecun site, where we additionally measured P mineralization, vegetation type effects on parameters in the top 0.2 m soil layer were assessed using repeated measure ANOVA, with sampling date as the repeated factor. Prior to conducting all ANOVAs, data were checked for their normality of distribution. If not, a log10(x) or log10(constant + x) transformation was made. The significance of the differences between means in all ANOVAs was identified using the least significance difference (LSD). The significance of linear correlations between parameters was expressed as the Pearson's product moment correlation coefficient. All the data processing was performed using SPSS version 13.0 (SPSS Inc., USA).

3.3. Sub-fractions of organic phosphorus At all sites, generally, labile OP (L-OP) and moderately labile OP (ML-OP) concentrations in the profile were higher under P. fruticosa than under grasses (p < 0.05) (Fig. 6). Moderately and highly resistant OP (MR-OP and HR-OP) concentrations were both lower in P. fruticosa patches than in grass areas (p < 0.05) (Fig. 6). Across all soil samples of three sites, correlations of soil MBP to various OP fractions increased according to the order: HR-OP (r = 0.76) < MR-OP (0.87) < ML-OP 4

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Fig. 2. (a) Root P contents in the 1 m soil profile in Potentilla fruticosa patches and grassy areas in meadows at the three sites Nuoerlong, Maikecun and Yelong sampled in late April 2018. Bars are ± one standard errors of the means (n = 3). Root distribution under grasses was limited to a depth of 0.4–0.6 m. (b) Dynamics of P contents in shoots of grasses (stems and leaves) and the shrub Potentilla fruticosa (newly growing leaves and twigs) in the 2016 growing season at Maikecun. Bars are ± one standard errors of the means (n = 9). Averaging sampling dates, the P content differed between the two vegetation patch types at p < 0.001 (repeated measure's analysis of variance).

topsoil, synthesizing more microbially derived OP from AP in upper depths (Turner et al., 2013; Weihrauch and Opp, 2018). Carbon availability is a major driver of the synthesis of microbially derived OP in soil (Khan and Joergensen, 2012; Spohn and Kuzyakov, 2013; Sorkau et al., 2018). Thus, the discrepancy in the profile distribution between OP and IP reflected a more intensive coupling among root P acquisition, plant P uplift, litter P input and microbial OP synthesis in the topsoil than in the subsoil. The higher AP concentrations in the upper soil depths reflected faster P mineralization in the upper than in the lower profile (see below).

(0.94) < L-OP (0.99) (n = 30 and p < 0.001 in all correlations; Fig. S2). 3.4. Soil phosphorus mineralization in the topsoil The phosphorus mineralization rate in the top 0.2 m soil layer at Maikecun was greater in soil under P. fruticosa than under grasses throughout the incubation duration (p < 0.005) (Fig. 7a). Cumulative P mineralized by the end of incubation (5 months) was 54% larger under P. fruticosa (103 mg kg−1) than under grasses (67 mg kg−1) (p < 0.001) (Fig. 7b). This corresponds to higher MBP and AP contents and phosphatase activities under P. fruticosa (p < 0.001 for all parameters) (Fig. 8a, b, c, d). Averaged over the growing season, the daily soil temperature at 7.5 cm was 1.1 °C lower under P. fruticosa (12.6 °C) than under grasses (13.7 °C) (p < 0.001), whereas soil moisture in the top 0.2 m was higher under P. fruticosa (66.0%) than under grasses (59.2%) (p < 0.001) (Fig. S3).

4.2. Phosphorus uptake ability of plants We hypothesized that the shrub P. fruticosa had a greater ability to acquire P from soil than grasses, based on the higher P concentrations in its shoots and roots and the greater P storage in its roots. The shrub's greater ability to acquire P could be facilitated by several mechanisms. First, P. fruticosa has a larger and deeper root system than grasses, thus being capable of mining P from a larger soil volume. In particular, P. fruticosa rooted to depths below 1 m, whereas grass roots were distributed in the upper 0.6 m. This root architecture extended P. fruticosa's P-uplift depth and helped it outcompete for P by spatial niche differentiation (Yoder and Nowak, 2000). Consequently, AP and IP were depleted in the subsoil under P. fruticosa compared to areas beyond the P. fruticosa canopy. Second, P. fruticosa roots are potentially colonized more by arbuscular mycorrhizal fungi than roots of gramineous plants (Bao and Yan, 2004), whereby sedge plant roots are seldom mycorrhizal (Brundrett, 2009). Gramineous and sedge plants were two dominant groups in the grass areas. Arbuscular mycorrhizal hyphae increase the volume of soil from which plants can acquire P and produce phosphatases and phytases in the rhizosphere (Joner et al., 2000; Koide and Kabir, 2000; Javot et al., 2007). Phosphatases catalyze the release of phosphate anions from phosphate esters (Joner et al., 2000; Koide and Kabir, 2000; Turner, 2008), whereas phytases specialize in disintegrating inositol phosphates (Li et al., 1997). Both acid and alkaline phosphatase activities in soil were greater under P. fruticosa than under grasses (Fig. 5). Third, the pH was lower in soils where P. fruticosa grew, than in grass-only soils. Possibly, P. fruticosa secreted more acidic substances into the rhizosphere than grasses. The decreased soil pH under shrubs increased the solubility of P-containing compounds in soil compared to that under grasses, by competing with phosphate ions for cation-binding partners (Javot et al., 2007). Fourth, shrub roots have a greater longevity than grass roots (Gill et al., 2002), leading to a

4. Discussion 4.1. General distribution patterns of P fractions in the soil profile The uniform soil particle-size composition throughout the 1 m profile indicated the identical origin of the parent materials between the shrubby and grassy patches at all three sites. Accordingly, the relative increase in the total soil P content in the topsoil compared to the lower depths reflected P uplift by vegetation during ecosystem development and soil genesis. Plants take up P from the range of root system extension, whereas they return P in organic form largely into the surface soil via litterfall and root turnover (Walker and Syers, 1976). The OP content was higher while IP content was lower in the topsoil relative to the subsoil. These different distribution patterns between OP and IP in the profile are apparently related to the root distribution in soil. Roots were more abundant in the topsoil, and thus took up more P in the upper depths and recycled it mainly in the upper soil layer. Plants acquire P from both organic (after depolymerization) and inorganic sources (after weathering and dissolution). Nonetheless, the input of OP came more from aboveground litterfall and root turnover in the topthan in the subsoil. In contrast, the IP pool could not be replenished substantially due to limited concentrations of phosphate anions and polyvalent cations in the profile. In addition, the larger litter input into the upper versus lower depths fed a larger microbial community in the 5

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to transform P from the inorganic to organic form. This was demonstrated by the fact that the shrub increased the OP content in the topsoil but decreased the IP content in the subsoil, compared to grasses (Fig. 4; Fig. 9); the OP stock increased but the IP stock decreased in the 1 m profile under P. fruticosa compared to grasses (Fig. 3c and d). The depleted IP in the lower depths under shrubs was sequestered in the topsoil as the OP through plant uplift. The higher OP content in soils inhabited by P. fruticosa was consistent with higher organic C accumulation under shrub patches versus grass-only areas (He and Li, 2016). Grazing livestock consumes less shoot biomass of P. fruticosa than grasses due to its poor palatability (Li et al., 2014). Dense P. fruticosa branches also prevent animals from grazing the understory grass plants. These two factors led to a greater accumulation of aboveground litter in than around shrub patches. P. fruticosa also has a larger root biomass, returning more high-P-content, root-derived litter to the soil through root turnover. More abundant plant input to soils under the shrub than under grasses supported a larger microbial biomass there, promoting accumulation of more microbially derived OP compounds through the uptake of AP (released from mineralization of OP and dissolution of mineral P). This was reflected in the greater MBP content in the 1 m soil profile under P. fruticosa than under grasses (Fig. 5). Soil MBP is closely related to C availability in grasslands (Joergensen and Scheu, 1999; Khan and Joergensen, 2012; Sorkau et al., 2018). Under P. fruticosa, therefore, the greater P uptake by plants and microbes jointly increased soil P transformation from inorganic to organic forms. We confirmed that OP was more labile in soils inhabited by P. fruticosa than solely by grasses. The OP composition revealed by sequential fractionation showed that relatively labile OP fractions (L- and ML-OP) were represented in larger proportions throughout the soil profile, whereas the contents of resistant OP fractions (MR- and HR-OP) were smaller, under P. fruticosa versus grasses (Fig. 6). The sequential fractionation of OP based on its susceptibility or resistance to chemical agents provided a means for examining mineralization, microbial turnover and plant-utilization dynamics of OP in soil (Bowmanm and Cole, 1978). Microbial biomass contains P mainly in the form of nucleic acids, P-esters and phospholipids, whereas inositol phosphates are mainly synthesized in plants (Stewart and Tiessen, 1987; Jung and Tamai, 2013; Nash et al., 2014). Phosphorus compounds of microbial origin are easily extractable from soil using lukewarm salt or acid solutions. The extraction of inositol phosphates and humified P-containing compounds requires alkaline extractants (Bowman and Cole, 1978; Jarosch et al., 2015). Closer correlations of L- and ML-OP to MBP than MR- or HR-OP (Fig. S2) strongly imply that labile OP sub-pools contained more microbially derived P compounds; accordingly, relatively resistant OP sub-fractions were rich in more plant-derived and humified P compounds. The evidence that OP under P. fruticosa contained more microbial-derived compounds than under grasses was further supported by a greater proportion of OP present as MBP throughout the profile under the shrub (Fig. 5). The greater microbial activity under shrubs increased the decomposition of plant-derived OP and synthesized more microbially derived OP compounds. Another explanation for the decreased concentrations of relatively resistant OP fractions under P. fruticosa is that this shrubby plant might have a greater capacity to depolymerize the resistant OP fractions than grasses. Competing plants vary in their capacities to access different OP forms in soils (Turner, 2008; Ahmad-Ramli et al., 2013; Steidinger et al., 2015; Ceulemans et al., 2017; Liu et al., 2018b). For example, despite their recalcitrance in soil, the resistant inositol phosphates are differently available for plants (Li et al., 1997; Turner et al., 2005; Turner, 2008).

Fig. 3. Root P stocks (a) and total (b), organic (c), inorganic (d), available (e) and microbial biomass P (MBP) stocks (f) in the 1 m soil profile under shrubby Potentilla fruticosa and grasses at Nuoerlong, Maikecun and Yelong. Different lowercase letters (a and b) show means are different within each site at p < 0.05.

longer residence time of P in root biomass. 4.4. Organic phosphorus mineralization 4.3. Organic phosphorus in soil We confirmed that OP mineralization was faster under P. fruticosa than under grasses, causing more AP under the shrubs. The faster soil P

We confirmed our hypothesis that P. fruticosa had a greater capacity 6

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Fig. 4. Contents of inorganic, available and organic P in the 1 m soil profile (vertical axis shows soil depth, m) under the shrub Potentilla fruticosa and grassy areas in meadows at the three sites Nuoerlong, Maikecun and Yelong. Bars are ± one standard errors of the means (n = 3).

Fig. 5. Soil microbial biomass P (MBP) and acid (AcPME) and alkline phosphatase (AlPME) activities in the profile under the shrub Potentilla fruticosa and grassy areas in meadows at the three sites Nuoerlong, Maikecun and Yelong. Bars are ± one standard errors of the means (n = 3). OP: organic phosphorus; PNP: pnitrophenol. 7

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Fig. 6. Labile organic P (L-OP), moderately labile organic P (ML-OP), moderately resistant organic P (MR-OP) and highly resistant organic P (HR-OP) in the soil profile under the shrub Potentilla fruticosa and grass areas in meadows at the three sites Nuoerlong, Maikecun and Yelong. Bars are ± one standard errors of the means (n = 3).

mineralization was facilitated by the higher content and lability of OP under P. fruticosa. Easily extractable OP substances mineralize first (Weihrauch and Opp, 2018). The faster P mineralization under shrubs than under grasses was associated with greater phosphatase activities, microbial biomass (MBP) and root biomass in shrub inhabited soils. Larger root biomass generally corresponds to greater root activity (e.g. secretion of enzymes and exudates) as well as to greater microbial activity in the rhizosphere (Pii et al., 2015; Razavi et al., 2016). Microbes serve as a source and sink of AP in soil and are directly involved in P mineralization (Turner et al., 2013; Sorkau et al., 2018; Spohn and Kuzyakov, 2013). Besides mycorrhiza and roots, soil microbes also synthesize phosphatases and phytases (Joner et al., 2000; Koide and Kabir, 2000; Turner, 2008). The higher soil moisture under P. fruticosa than under grasses might have an insignificant effect on the increased P mineralization. This is because the slightly higher soil water content under the shrub reflected a greater water holding capacity of matrix. The higher soil organic matter content (He and Li, 2016) increases the soil water holding capacity (Li et al., 2007). Faster OP mineralization in the topsoil under P. fruticosa was also unrelated to soil temperature, which was lower under P. fruticosa than under grasses, because of better shading. 4.5. Synthesis The deep rooting shrubs used a greater amount of IP from the subsoil than shallow-rooted grasses. Greater plant input through litterfall and root turnover under shrubs fed a larger microbial biomass that accumulated more microbially-derived OP in soil than that under grasses. Thus, shrubs had a greater capacity to uplift P in the profile and to transform P from inorganic to organic forms (Fig. 9). Soil OP under shrubs was more labile than in adjoining grassy areas. Greater content and lability of OP as well as greater root and soil microbial activities under shrubs increased P mineralization compared to those under grasses. Overall, biological (plant and microbial) P cycling was fast in shrub patches (Fig. 9). We concluded shrubs increased the biological P transformation in the soil, the P uplift in the profile and P cycling in the ecosystem. Such mechanisms structuring spatial heterogeneity of P

Fig. 7. Dynamics of P mineralization rate (a) and cumulative P mineralized (b) in the top 0.2 m soil under the shrub Potentilla fruticosa and grass areas in meadows in 2016 at Maikecun. Bars are ± one standard error of the mean (n = 9). Averaging sampling dates, the P mineralization rate differs between two vegetation patch types at p < 0.01 (repeated measures analysis of variance). By the end of the 5-month incubation, cumulative P mineralized (per either soil mass or area) differed between vegetation patch types at p < 0.001 (one-way analysis of variance).

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Fig. 8. Dynamics of soil microbial biomass P content (a), acid and alkaline phosphatase activities (b, c) and available P content (d) in the top 0.2 m soil under shrub Potentilla fruticosa patches and grass areas in meadows at Maikecun. Bars are ± one standard errors of the means (n = 9). PNP refers to pnitrophenol. Averaging sampling dates, all parameters differ between two vegetation patch types at p < 0.001.

the Russian Science Foundation (project No. 18-14-00362). Authors highly appreciate anonymous reviewers and editor for their very constructive comments on the previous version, which greatly contribute to the improvement of manuscript quality. We thank Lin Wang, Gaobo Jing, Xiao-Ming Mou, Bin Jia and Qiu-Jin Ma for their assistances in soil and plant sampling and data drafting. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.soilbio.2019.02.012. References Achat, D.L., Morel, C., Bakker, M.R., Augusto, L., Pellerin, S., 2010a. Assessing turnover of microbial biomass phosphorus: combination of an isotopic dilution method with a mass balance model. Soil Biology and Biochemistry 42, 2231–2240. Achat, D.L., Bakker, M.R., Zeller, B., Pellerin, S., Bienaimé, S., Morel, C., 2010b. Longterm organic phosphorus mineralization in Spodosols under forests and its relation to carbon and nitrogen mineralization. Soil Biology and Biochemistry 42, 1479–1490. Ahmad-Ramli, M.F., Cornulier, T., Johnson, D., 2013. Partitioning of soil phosphorus regulates competition between Vaccinium vitis-idaea and Deschampsia cespitosa. Ecology and Evolution 3, 4243–4252. Bao, Y.Y., Yan, W., 2004. Arbuscular mycorrhizae and their structural types on common plants in grasslands of mid-western Inner Mongolia. Biodiversity Science 12, 501–508. Becker, J., Gütlein, A., Sierra Cornejo, N., Kiese, R., Hertel, D., Kuzyakov, Y., 2017. Savanna vegetation structure controls soil nutrient availability and carbon sequestration potential. Ecosystems 20, 989–999. Blok, D., Faucherre, S., Banyasz, I., Rinnan, R., Michelsen, A., Elberling, B., 2018. Contrasting above- and belowground organic matter decomposition and carbon and nitrogen dynamics in response to warming in High Arctic tundra. Global Change Biology 24, 2660–2672. Bol, R., Julich, D., Brödlin, D., Siemens, J., Kaiser, K., Dippold, M.A., Spielvogel, S., Zilla, T., Mewes, D., von Blanckenburg, F., Puhlmann, H., Holzmann, S., Weiler, M., Amelung, W., Lang, F., Kuzyakov, Y., Feger, K.H., Gottselig, N., Klumpp, E., Missong, A., Winkelmann, C., Uhlig, D., Sohrt, J., von Wilpert, K., Wu, B., Hagedorn, F., 2016. Dissolved and colloidal phosphorus fluxes in forest ecosystems - an almost blind spot in ecosystem research. Journal of Plant Nutrition and Soil Science 179, 425–438. Bowmanm, R.A., Cole, C.V., 1978. An exploratory method for fractionation of organic phosphorus from grassland soils. Soil Science 125, 95–101. Brookes, P.C., Powlson, D.S., Jenkinson, D.S., 1982. Measurement of microbial biomass phosphorus in soil. Soil Biology and Biochemistry 14, 319–329. Brundrett, M.C., 2009. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant and Soil 320, 37–77. Bünemann, E.K., Augstburger, S., Frossard, E., 2016. Dominance of either physicochemical or biological phosphorus cycling processes in temperate forest soils of contrasting phosphate availability. Soil Biology and Biochemistry 101, 85–95. Carboni, M., Guéguen, M., Barros, C., Georges, D., Boulangeat, I., Douzet, R., Dullinger, S., Klonner, G., van Kleunen, M., Essl, F., Bossdorf, O., Haeuser, E., Talluto, M.V., Moser, D., Block, S., Conti, L., Dullinger, I., Münkemüller, T., Thuiller, W., 2018.

Fig. 9. Mechanisms of the effects of shrubby Potentilla fruticosa on biological P cycling and P distribution pattern in the soil profile in shrubby meadows. Compared to grasses, P. fruticosa, with its larger and deep penetrating root system, acquired P more from the subsoil (mainly from inorganic P: IP) and returned more plant-derived organic P (OP) to the topsoil through litterfall and root turnover. P. fruticosa had larger microbial biomass and thus synthesized more microbially derived organic P (MBP) in the topsoil under its canopy compared to grasses. The greater abundance and lability of organic P and integrated biological activity in soil under P. fruticosa increased P mineralization and so, the P turnover (presented as circle arrows at the topsoil).

content, transformation, turnover and fluxes are common in shrubby grasslands worldwide. Acknowledgements This study was supported by the National Natural Science Foundation of China (41571279). Contribution of YK was supported by 9

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