Forest conversion to pasture affects soil phosphorus dynamics and nutritional status in Brazilian Amazon

Soil & Tillage Research 194 (2019) 104330

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Forest conversion to pasture affects soil phosphorus dynamics and nutritional status in Brazilian Amazon

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Amin Soltangheisia,1, , Moacir Tuzzin de Moraesa,1, Maurício Roberto Cherubinb, Dasiel Obregón Alvarezc, Leandro Fonseca de Souzac, Wanderlei Bieluczykc, Deisi Navroskic, Ana Paula Bettoni Telesb, Paulo Sérgio Pavinatob, Luiz Antonio Martinellia, Siu Mui Tsaic, Plínio Barbosa de Camargoa a

Departamento de Ecologia Isotópica, Centro de Energia Nuclear na Agricultura (CENA), Universidade de São Paulo (USP), Av. Centenário, 303 - São Dimas, CEP 13416000, Piracicaba, SP, Brazil Departamento de Ciência do Solo, Escola Superior de Agricultura Luiz de Queiroz, Universidade de São Paulo – ESALQ/USP, Av. Pádua Dias, 11, CEP 13418-900, Piracicaba, SP, Brazil c Cell and Molecular Biology Laboratory, Centro de Energia Nuclear na Agricultura (CENA), Universidade de São Paulo (USP), Av. Centenário, 303 - São Dimas, CEP 13416-000, Piracicaba, SP, Brazil b

A R T I C LE I N FO

A B S T R A C T

Keywords: Path analysis Acid phosphatase C:Po ratio Soil P transformation Hedley P fractionation

Understanding the pathways of soil phosphorus (P) transformations and determining the factors related to P nutritional status of soils when land use changes is critical for a better management, especially in Amazon region. We investigated different P fractions and their transformations in different land uses (primary forest and pasture) and soil textures (clayey and sandy) in Amazonian Oxisols using path analysis. Besides P fractionation, phosphatase activity and its correlation with soil carbon (C):organic P (Po) ratio was evaluated to correlate it with soil P nutritional status. After 15 years from forest slashing and burning, total P in pasture reaches to the forest levels in Amazonian soils, regardless of soil texture. Path analysis showed that land use conversion from forest to pasture decreased the diversity of the contribution of P pools to buffer P extracted by anion exchange resin. However, Po accounted for one-fourth of total P in our sites, it plays an important role as source of plant available P and contributed more in pasture compared to forest. Our results from P fractionation and C:Po ratio revealed that Amazonian pastures and forests are not P deficient. We also showed that with increasing C:Po ratio, plant-available P content became more dependent on P mineralization. Soil acid phosphatase activity can be used as an indicator for evaluating soil P nutritional status; however, its range changes according to the land use.

1. Introduction Phosphorus (P) is the major limiting macronutrient for plant growth in highly weathered tropical soils (Elser et al., 2007; Hamer et al., 2013). These soils have high quantities of iron (Fe) and aluminum (Al) sesquioxides which geochemically bind P and make it unavailable for plant uptake (Gama-Rodrigues et al., 2014). It is estimated that 90% of Amazonian upland soils are P limited for annual crop production (Tiessen et al., 1994; McGrath et al., 2000) and some studies showed that even native forest productivity is limited by P in this region (Cuevas and Medina, 1988; Luizão et al., 2009). The primary source of P for terrestrial ecosystems is the weathering of parent material, and hence P is considered as the ultimate limiting soil nutrient in nature

(Walker and Syers, 1976). Phosphorus is found in inorganic, organic, and microbial forms in soils and its dynamics may be controlled by a combination of chemical and biological properties (Frossard et al., 2000). Since P is highly limited in tropical soils, turnover of organic P and the rapid recycling of P from litterfall are the main processes for providing P to plants in natural ecosystems (Johnson et al., 2003). Land use change from forest to pasture or intensive agriculture for feeding the expected world population of 9 billion in 2050 (Tilman et al., 2011) has been the largest global change of the last two centuries (Guillaume et al., 2015). Brazil is a key player in the global food production (FAOSTAT, 2017) which part of it comes from the deforestation of major Brazilian biomes (Lapola et al., 2014). In 2004, 25,396 km2 of Brazilian Legal Amazon was cleared, and after that time, the rate of

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Corresponding author. E-mail address: [email protected] (A. Soltangheisi). 1 Amin Soltangheisi and Moacir Tuzzin de Moraes are joint first authors. https://doi.org/10.1016/j.still.2019.104330 Received 30 April 2019; Received in revised form 1 July 2019; Accepted 6 July 2019 0167-1987/ © 2019 Published by Elsevier B.V.

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deforestation fortunately decreased, reached 7900 km2 in 2018 (INPE, 2018). The conversion of forest to pasturelands by forest slashing and burning is the main driver in Brazilian Amazon (Dias et al., 2016). Land use changes, especially those which disturb the soil and alter redox reactions, affect directly the P dynamics and lability for plant uptake in the soil through changes in P losses via runoff or leaching and by changing the proportions of P accumulated in more recalcitrant pools (Wright, 2009). Forest clearing by slash and burn releases P from forest biomass and redistributes it between living plants and microorganisms at different P pools in the soil (Garcia-Montiel et al., 2000; Wright, 2009; Hamer et al., 2013). Some techniques to explore the distinct P pools in the soil are very helpful for a better understanding of P dynamics over the time with land use change. The direct analysis of different organic (nuclear magnetic resonance spectroscopy- 31P-NMR) and inorganic (X-ray absorption near edge structure spectroscopy- XANES) P species are some powerful techniques but difficult to use due to their financial, practical, and socially acceptable limitations (Zheng et al., 2004). Hedley chemical sequential P fractionation (Hedley et al., 1982) is an alternative technique that quantify labile Pi (inorganic P), Ca-associated Pi, Fe + Al-associated Pi, as well as labile and more stable forms of Po (organic P). This fractionation procedure can also estimate the potential of different P pools to contribute to plant available P (Yang and Post, 2011) and differentiate P pools related to their degree of recalcitrance, influenced by land use change (Wright, 2009) and soil texture. However, very few Hedley-P data in tropical forests is an issue which was pointed out by some researchers (Johnson et al., 2003; Dieter et al., 2010) and the data related to P fractions in sub-surface horizon of these ecosystems are even more scarce. Understanding P behavior in soils by revealing the transformations between P fractions with distinct bioavailability is still a missing information nowadays, and these transformations are influenced by soil mineralogical, chemical, and biological processes (Frossard et al., 2000). Path analysis has been used to shed light on these mechanisms by constructing conceptual models of cause-and-effect relationships among different P fractions and reveal the roles of P pools as sources and sinks in the process of transformation (e.g., Beck and Sanchez, 1994; Tiecher et al., 2018; Jiménez et al., 2019). Path analysis can also decompose the observed correlation into direct and indirect effects which operate indirectly through subsequent variables. The objectives of this study were to shed light on the pathways of soil P transformations in Amazonian forest and pasture Oxisols with different textures by path analysis and determining the sources and sinks of anion exchange resin P, which is the most available P fraction for plant uptake. In addition, we investigated soil phosphatase activity in these land uses to establish its relationship with Po and C:Po ratio in Amazonian soils. Based on a previous study (Garcia-Montiel et al., 2000), we hypothesized that conversion of forest to pasture in Amazon changes the dynamics of P and patterns of P cycling in the soil. In addition, this land use change modifies microbial community leading to the changes in phosphatase activity and consequently Po mineralization.

years) are presented in Fig. 2 (Alvares et al., 2013). In each site, the primary land use change sequence undergoing in that region, pristine forest to pasture, was evaluated. Forest-to-pasture conversion occurred 15 years ago through a process of selective logging of valuable timber, followed by slash-and-burn deforestation of the remaining vegetation, and finally mechanical seeding of non-native, fast growing grass Urochloa sp. (former Brachiaria). Pasturelands in both sites had been managed with the same practices. In each site, for soil sampling, a square plot of 100 × 100 m (1 ha) was selected and five sampling points were chosen within this square (Fig. 1C). In each point, a 40 cm deep trench (50 × 50 cm) was dug and soil samples were collected from 0 to 10, 10–20, 20–30, and 30–40 cm depth layers (Fig. 1C). Samples were collected in March 2018, which is considered as the end of rainy season. Selected soil physical and chemical properties of each site are described in Table 1. 2.2. Soil analysis For chemical analysis, soil samples were air-dried, and then passed through 2 mm sieve. The soil P fractionation was performed according to the methodology proposed by Hedley et al. (1982), with modifications made by Condron et al. (1985) changing the original sonication step by 0.5 M NaOH extraction. Different extractors were added to 0.5 g of soil in sequential order: anion exchange resin (PAER); NaHCO3 0.5 mol L−1 (labile inorganic (PiBIC) and organic (PoBIC) P); NaOH 0.1 mol L−1; HCl 1.0 mol L−1 (moderately labile inorganic (PiHID-0.1 + PHCl) and organic (PoHID-0.1) P), and NaOH 0.5 mol L−1 (non-labile inorganic (PiHID-0.5) and organic (PoHID-0.5) P). In all the five steps, the suspension was stirred for 16 h in an end-over-end shaker (33 rpm). At the end of the sequential extraction, the remaining residual soil was dried in 50 °C, ground to homogenize and digested by concentrated H2SO4, 30% H2O2, and saturated magnesium chloride to extract residual P (Presidual) (Brookes et al., 1982). Phosphorus concentration in the extracts were measured by colorimetric method of Murphy and Riley (1962) for acid extracts and Dick and Tabatabai (1977) for alkaline extracts, using spectrophotometer (Femto 600 plus) at 882 and 700 nm wavelengths, respectively. The inorganic fractions were determined directly in the extract. The organic P fractions were estimated as the difference between total P fractions, determined after digestion of the alkaline extracts with 7.5% (w/v) ammonium persulfate [(NH4)2S2O8] solution and 50% H2SO4 in an autoclave (103 kPa, 121 °C) for 2 h (Kopp and McKee, 1979), and the respective inorganic fractions. Soil samples for phosphatase analyses were collected from each soil layer (0–10, 10–20, 20–30, and 30–40 cm depths), homogenized and kept in a falcon tube (15 ml) at 4 °C. In the lab, these soil samples were used to measure acid phosphatase activity by the method proposed by Tabatabai and Bremner (1969) using p-nitrophenyl phosphate (PNP). One gram of soil, 4 mL of modified universal buffer (MUB), 0.25 mL of toluene and 1 mL of PNP solution were placed in a 50-mL Erlenmeyer flask and swirled to mix the contents. Then the flask was stoppered and placed in an incubator at 37 °C for 1 h. In the next step, 1 mL of CaCl2 and 4 mL of 0.5 M NaOH was added and the solution was filtered with quantitative filter paper (blue spot, diameter 12.5 cm, and basis weight of 85 g m−2, similar to Whatman nº 42). The yellow color intensity of the filtrate was measured with a Klett-Summerson photoelectric colorimeter fitted with a blue filter. Then the p-nitrophenyl content of the filtrate was calculated according to a calibration graph plotted by standards containing 0, 10, 20, 30, 40, and 50 μg of p-nitrophenyl. For soil total C, prior to analysis, soil samples were air dried, ground and sieved through a 2-mm mesh. Then a 50-g subsample was handpicked to remove roots and charcoal. These soil samples were passed through a 100 mesh (0.149 mm sieve), sealed in thin capsules to analyze the C concentration by dry combustion in an elemental analyzer (Carlo-Erba, CH-110, Milan, Italy) coupled with an isotope ratio mass spectrometer (IRMS) (Thermo Scientific Delta Plus,Bremen, Germany).

2. Materials and methods 2.1. Site description and soil sampling The study was conducted in the Tapajós National Forest, centraleastern region of Amazon rainforest, Santarem, Pará, Brazil. Four paired sites were selected, being two sites with clayey and two sites with sandy soil texture (Fig. 1A and B). This region is characterized as a hotspot of change and intensification of land use, with important expansion of livestock and agriculture in the last decades (Lees et al., 2013). The climate is tropical monsoon, ‘Am’ according to Köppen classification, with rainfalls in 7–9 hottest months of the year (Alvares et al., 2013). Rainfall distribution and temperature (average of 23 2

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Fig. 1. Geographical location of study sites (A), picture showing the distance between pasture and forest sites (B), and soil sampling points in 1 ha area and trench for soil sampling from different depths (C).

Fig. 2. Monthly precipitation (mm) (gray bars) and mean temperature (°C) (black circles) averaged of 23 years.

Index and Bentler-Bonett NFI were chosen as criteria to determine how well the conceptual model represents graphic interpretations of P transformations in soils in the present study. Soil depths of 0–10, 0–30, and 0–40 cm were analyzed by path analysis model. Phosphorus transformations in both land uses and soil textures of 0–40 cm depth passed these criteria and are presented in this research.

2.3. Statistical and path analysis Variance homogeneity and normality of data were tested for each parameter before conducting analysis of variance (ANOVA). Data were transformed using Box-Cox techniques (Box and Cox, 1964) and outliers were removed when needed, and then the data were submitted to oneway ANOVA models to test the effect of land use on different parameters. All the statistical analysis were performed by Statistical Analysis System - SAS v.9.4 (SAS Inc., Cary, NC, USA). Plots and bar graphs were generated using the software SigmaPlot 14.0. Simple equation analysis was performed with raw data of P fractionation, and regression coefficients were used as the initial coefficients of linear structure equations, which were subjected to optimization in the path analysis. PAER, PiBIC, PoBIC, PiHID-0.1, PoHID-0.1, and Presidual were considered as endogenous (dependent) variables, while PiHID-0.5, PoHID-0.5, and PHCl were considered as exogenous (independent) variables in the general path analysis model (Tiecher et al., 2018). The PROC CALIS procedure in SAS v.9.4 was used to drive the path coefficients between the source and the recipient P pools in the conceptual model. The optimized coefficients from these equations are taken as path coefficients (β) which are essentially linear regression coefficients. The Chi-Square test, along with Bentler Comparative Fit

3. Results 3.1. Changes in phosphorus fractions The PAER content in both soil textures was higher in forest compared to pasture in 0–10 and 0–30 cm depths (Table 2). It can be stated that in clayey forest, PAER tended to concentrate in 0–10 cm depth as its content in 0–30 cm depth was 61% lower than 0–10 cm depth, while in clayey pasture and sandy forest and pasture this difference between 0–10 and 0–30 cm depths was not observed. The PiBIC content was higher in forest compared to pasture only in sandy soil in both depths intervals (Table 2). In clayey soil, PiHID-0.1 in forest was higher than pasture in both 0–10 and 0–30 cm depths, while in sandy soil the reverse trend was observed (Table 2). Considering 0–10 cm soil depth, PoHID-0.5 which is non-labile organic P fraction was not influenced by 3

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and total P contents were not influenced by land use change in both soil textures (clayey and sandy) and soil depths (0–10 and 0–30 cm) (Table 2). The proportion of total P in PHCl was negligible (< 0.3%) in both soil textures. Total P contents in 0–30 cm depth were 613 and 432 mg kg−1 in clayey and sandy soils (averaged among forest and pasture), respectively (Table 2). Land use change did not influence total P in both soil textures. In terms of soil P lability, moderately labile (mod-labile) P (sum of PiHID-0.1, PoHID-0.1, and PHCl) was affected by land use change in both soil textures in 0–10 cm depth and in clayey soil in 0–30 cm depth (Table 2). In clayey soil, mod-labile P in forest was higher than pasture, while in sandy soil, the inverse trend was observed. Organic P accounted for 21, 19, 22, and 24% of total P in clayey forest, clayey pasture, sandy forest, and sandy pasture, respectively, in both soil depths of 0–10 and 0–30 cm (Table 2). The amount of organic P (sum of PoBIC, PoHID-0.1, and PoHID-0.5) was not affected by land use change in both soil textures considering 0–10 cm depth, while it was higher in clayey forest in comparison with clayey pasture in 0–30 cm depth.

Table 1 Soil physical and chemical properties at 0–40 cm depth of study sites. Site

Sandy forest

Sandy pasture

Clayey forest

Clayey pasture

Soil texture

Loamy sand 858 64 79 1.49 3.7 11.1 1.16 0.10 6.7 0.9 1.1 0.8 9.2 18.1 18.7 0.4 0.1 115 0.5 0.2

Sandy clay loam 627 50 323 1.53 4.1 15.0 1.26 0.10 9.0 1.0 2.1 2.0 9.0 23.3 26.6 0.4 0.2 108 1.6 0.2

Clay

Clay

15 128 858 1.04 3.8 17.8 1.36 0.11 16.9 0.9 1.2 1.0 17.4 34.9 36.1 0.6 0.2 64 1.0 0.2

321 63 617 1.31 4.2 14.8 1.21 0.10 15.4 0.9 3.1 2.1 7.2 19.0 23.5 0.4 0.1 66 1.3 0.3

Sand (g kg−1) Silt (g kg−1) Clay (g kg−1) Bulk density (Mg m−3) pH (CaCl2) OM (g kg−1) Total C (%) Total N (%) S (mg kg−1) K (cmol(+) kg−1) Ca (cmol(+) kg−1) Mg (cmol(+) kg−1) Al (cmol(+) kg−1) H + Al (cmol(+) kg−1) CEC (cmol(+) kg−1) B (mg kg−1) Cu (mg kg−1) Fe (mg kg−1) Mn (mg kg−1) Zn (mg kg−1)

3.2. Path analysis In forest, all P fractions except Presidual in sandy soil (Fig. 3A) and Presidual and PHCl in clayey soil (Fig. 3B) acted as sources of PAER. In sandy forest soil, organic P contributed 53% to buffer PAER, while it was increased to 64% in clayey forest soil. In clayey forest, PiHID-0.5, PoBIC, and PoHID-0.5 were sources of Presidual (Fig. 3B). In sandy forest, these three P fractions besides PiHID-0.1 were sources of Presidual (Fig. 3A). In this soil, PiHID-0.1 also acted as source of PiBIC. In sandy pasture, PiHID-0.1, PHCl, and PoBIC (Fig. 3C), and in clayey pasture, PoBIC and PoHID-0.1 (Fig. 3D) contributed to buffer PAER. Compared to forest, the contribution of organic P to buffer PAER increased in pasture in both soil textures from 53% to 63% in sandy soil and from 64% to 100% in clayey soil. In clayey pasture, PiBIC, PiHID-0.1, and all the organic P fractions were sources of Presidual (Fig. 3D). In this soil, PoHID-0.5 was also source of PoHID-0.1. In sandy pasture, PiBIC and PHID-0.5 (organic and inorganic) were sources of Presidual (Fig. 3C). In both land uses and soil textures, PiHID-0.5 and PoHID-0.1 were not sources of PiHID-0.1 and PoBIC, respectively, while in our model they were considered as sources of these P fractions. PoHID-0.5 was the only P fraction which was the source of Presidual in all land uses and soil textures.

Table 2 Soil P fractions in 0–10 and 0–30 cm depths in different land uses (primary forest and pasture) and different soil textures (clayey and sandy). 0-10 cm Clayey −1

P fractions (mg kg PAER PiBIC PoBIC PiHID-0.1 PoHID-0.1 PHCl PiHID-0.5 PoHID-0.5 Presidual Plabile Pmod-labile Pnon-labile Porganic Pinorganic Ptotal 0-30 cm PAER PiBIC PoBIC PiHID-0.1 PoHID-0.1 PHCl PiHID-0.5 PoHID-0.5 Presidual Plabile Pmod-labile Pnon-labile Porganic Pinorganic Ptotal

)

Sandy

Forest

Pasture

Forest

Pasture

6.1A 8.3 43.2 37.3A 48.8A 0.97 16.4 41.2 405.5 57.6 87.1A 463.0 133.2 474.6 607.8

3.7B 7.4 45.8 31.3B 35.7B 1.14 16.6 35.3 440.4 56.9 68.1B 492.3 116.8 500.5 617.3

4.3A 12.8A 40.3 19.1B 32.0 1.07 16.3 25.8 287.5 57.4 52.2B 329.6 98.1 341.1 439.2

3.1B 9.1B 47.0 28.1A 34.2 1.37 21.3 25.0 256.1 59.2 63.7A 302.4 106.2 319.1 425.3

3.8A 6.3 45.4 30.2A 44.2 1.01 16.2 38.5A 412.3 55.5 75.4A 467.0 128.1A 469.8 597.9

3.0B 6.3 45.4 22.1B 38.3 1.02 15.4 32.5B 434.9 54.7 61.4B 482.8 116.2B 482.7 598.9

3.5A 10.8A 41.4 18.6B 34.8 0.99 15.6B 26.6 312.1 55.7 54.4 354.3 102.8 361.6 464.4

2.7B 7.1B 43.7 23.7A 32.9 1.08 20.4A 25.8 264.1 53.5 57.7 310.3 102.4 319.1 421.5

3.3. C:Po ratio and phosphatase activity C:Po ratio was influenced by land use in all depths except in the soil surface layer (0–10 cm) in clayey soil (Fig. 4A). In this soil, C:Po ratio was higher in forest compared to pasture. In sandy soil, C:Po ratio was affected by land use change in 0–10 and 10–20 cm soil depths (Fig. 4B). In this soil, C:Po ratio in forest was higher than pasture in 0–10 and 10–20 cm depths, while in 20–30 and 30–40 cm depths, this ratio was not changed. In both soil textures and both land uses, C:Po ratio decreased with depth, except in sandy forest which it was not changed with depth. Averaged among soil depths (0–40 cm), C:Po ratios were 107, 143, 101, and 76 in clayey pasture, clayey forest, sandy pasture, and sandy forest, respectively. In both soil textures, with enhancing C:Po ratio, the correlation between inorganic labile P and C content increased (Fig. 5) meaning that in clayey soil, C:Po ratio in forest was higher than pasture and inorganic labile P had higher correlation with C content in forest (Fig. 5A), while in sandy soil, C:Po ratio in pasture was higher than forest and consequently higher correlation between inorganic labile P and C content was observed in pasture (Fig. 5B). Phosphatase activity was influenced by land use change only in 10–20 cm soil depth in clayey soil (Fig. 6A), while in sandy soil, land use change affected phosphatase activity in all soil depths (Fig. 6B). In both soil textures, phosphatase activity in pasture was higher than

Within each depth, soil texture, and P fraction, means followed by different capital letters were not significantly different at p < 0.05 by one-way ANOVA test. Where there is no letter, it means that the difference was not significant.

land use change in both soil textures, while considering 0–30 cm depth, it was higher in forest compared to pasture in clayey soil (Table 2). The PoBIC, PoHID-0.1, PHCl, Presidual, labile P, non-labile P, inorganic P, 4

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Fig. 3. Relationship among soil P pools and relative contribution of each P fraction to PAER in sandy forest (A), clayey forest (B), sandy pasture (C), and clayey pasture (D) by path analysis. Black arrows indicate significant paths.

same trend as C:Po ratio in both soil textures meaning that it was decreased with depth, except in sandy forest which it was not changed with depth. Correlations between phosphatase activity and C:Po ratio in

forest in soil depths where the effect of land use change was significant. In sandy soil, phosphatase activity in pasture was four times higher than forest in 0–10 cm soil depth but this difference became smaller with depth. Changes in phosphatase activity with depth followed the 5

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Fig. 4. C:Po ratio in clayey (A) and sandy (B) soil in 0–40 cm depth. Horizontal bars show the standard error for the mean comparisons.

Fig. 5. Relationship between inorganic labile P (PAER + PiBIC) and C content in clayey (A) and sandy (B) soil. Green and brown regression lines represent forest and pasture, respectively. 6

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Fig. 6. Phosphatase activity in clayey (A) and sandy (B) soils in 0–40 cm depth. Horizontal bars show the standard error for the mean comparisons.

Fig. 7. Relationship between phosphatase activity and C:Po ratio. Green and brown regression lines represent forest and pasture, respectively.

burning forest in Rodonia, Brazil, but after 6 years without P addition, total P levels reached the levels of adjacent forest soil (Kauffman et al., 1995). Immediately after forest burning, forest biomass P was released to the soil and hence soil total P increased (Garcia-Montiel et al., 2000). Forest sites in our study were burned more than 15 years ago and hence the levels of total P in pasture reached the same levels as forest. Reduced P stocks with pasture aging was previously observed by Townsend et al. (2002) and Numata et al. (2007) in strongly weathered tropical soils. Other studies showed that the contents of nutrients released to the soil after forest slashing and burning declined rapidly in the first years of conversion to pasture (Fearnside, 1980; Buschbacher, 1984). More than 15 years after land use change, it can be stated that soil total P in both land uses is inherited from parent material, considered as a primary property of the soil, and as Amazonian soils are highly weathered, total P is not affected by land use change. Total P in 0–30 cm depth of forest sites were 598 and 464 mg kg−1 in clayey and sandy soils, respectively, which is higher than the forested Oxisols in other studies except Hawaiian forested Oxisols (Table 3). As resin does not chemically change the soil solution, PAER can be considered as freely exchangeable and the most plant available (Tiessen and Moir, 1993) inorganic P. PAER declined with depth in clayey and sandy forest. It is related to “nutrient pumping” meaning that forest

different land uses were investigated (Fig. 7). Phosphatase activity had a significant positive correlation with C:Po ratio in pasture (R2 = 0.68) and forest (R2 = 0.66). 4. Discussion 4.1. Effect of land use change on soil P dynamics While in our study, forest to pasture conversion did not change total P in both soil textures, Hamer et al. (2013) observed enhanced amount of total P due to this land use change in Cambisols of Southern Ecuador for 20 years and it reached to the forest levels afterwards. Groppo et al. (2015) also recorded higher P stocks in pasture related to the native vegetation in several Brazilian regions. On the contrary, Wright (2009) detected the lower total P in pasture compared to forest system in organic soils of Florida. He stated that a dense canopy cover in forest reduces soil temperature and consequently decreases microbial activity and P mineralization leading to the reduced P loss potential via runoff or leaching. Lilienfein et al. (2000) observed 12 and 15% less P in degraded pasture and productive pasture, respectively, in comparison with native savannah and they attributed this reduction to P removal by grazing. Total P concentrations increased by 40% immediately after 7

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proportions of PoBIC in monoculture in comparison with different crop rotation systems due to lower total soil C content in monoculture. PiHID-0.1 constitutes 4.4 and 4.8% of total P in Amazonian clayey and sandy soils (considering 0–30 cm depth), respectively, which is within the range of 4–17% proposed by Yang and Post (2011) for different soil orders. Lower %PiHID-0.1 in clayey pasture compared to clayey forest can be related to plant species capable of acquiring P from this modlabile inorganic P fraction in pasture via different mechanisms like mycorrhizal association or P-solubilizing rhizosphere exudates (Bolan, 1991). Fernandes and Sanford (1995) related the lower amount of PiHID-0.1 in peach palm monocultures compared to adjacent secondary forest and cacao plantations to the ability of the palm to deplete this P fraction faster than the other plants in their trial. Decrease of PiHID-0.1 proportions with depth which was observed in both land uses and soil textures was previously reported by Wright (2009). This P pool, together with inorganic labile P fractions represent least recalcitrant pools derived from mineralization of Po or rainfall and hence tend to accumulate in soil surface. Higher contents of PoHID-0.1 in pastures compared to forest, which was observed in clayey soil in 0–10 cm depth of our study, was previously observed in Brazilian Oxisols, in the central Brazilian Amazon (Garcia-Montiel et al., 2000), and in southwestern Costa Rica (Townsend et al., 2002). The authors related these higher proportions to the changes in the structure and quality of soil organic matter. Orthophosphate monoesters constitute the major proportion of PoHID-0.1; however, readily mineralizable diester P and teichoic acids were also found in this fraction (Guggenberger et al., 1996). PoHID-0.1 in pasture declines with time to reach to forest level which can be considered as one of the factors inducing pasture degradation (Townsend et al., 2002). PHCl is defined as inorganic calcium bound P (Hedley et al., 1982; Cross and Schlesinger, 1995) as P associated with Fe and Al which is possibly not extracted with NaOH is insoluble in acid and HCl 1.0 mol L−1 is not strong enough to extract organic C from soil and hence it does not extract organic P (Tiessen and Moir, 1993). As our soils are strongly weathered, apatite P (PHCl) is a very negligible proportion of total P (< 0.3%). These amounts are even lower than about 3% of total P stated by Yang and Post (2011) for strongly weathered Oxisols and in accordance with Tiessen and Moir (1993) who stated that PHCl is absent in many strongly weathered soils. Presidual constitutes 71 and 65% of total P in clayey and sandy soils, respectively (considering 0–30 cm depth), which is higher than the proportions recorded by Yang and Post (2011) for highly weathered Oxisols (59%), in accordance with Garcia-Montiel et al. (2000) in Brazilian Amazon (64–65%), and within the range of 40–70% measured by Tiessen et al. (1994) for the upper Rio Negro region of Amazon Basin. Presidual is enhanced with increasing the weathering of soils and these proportions show that Amazonian soils investigated here are at the late stage of development and extensively weathered based on Walker and Syers model (Walker and Syers, 1976). The Presidual contents was not changed with land use change in both soil textures indicating that plants in forests and pastures sites could not utilize this P pool as it is considered as stable, recalcitrant, and non-labile P (Turner et al., 2005). Our results are in contrast to Chen et al. (2000) who recorded lower Presidual in forest soils compared to adjacent grassland and GarciaMontiel et al. (2000) who found lower proportions of Presidual in 20 year old pasture (41–55% of total P) compared to the original forest (63–65% of total P) in the Brazilian Amazon. Hedley et al. (1982) related 50% depletion of total P to the depletion of Presidual under 65 years of cropping without P addition. The bioavailability of Presidual not only observed over the long term, but also observed over only 14 days in the rhizosphere of rape (Brassica napus) (Magid et al., 1996), what we did not observe here. Averaged among land uses, labile P content was 55 mg kg−1 in clayey and sandy soils in 0–30 cm depth. This is almost 3 times higher than the amounts of labile P for highly weathered soils (20 mg kg−1)

Table 3 Total P contents in different Oxisols of the world. Total P (mg kg−1)

Location

Study

78 152

Maraca Island, Roraima, Brazil Averaged among different Oxisols of the world San Carlos de Rio Negro, Venezuela Eeastern Amazonia, Brazil Amazonian forests, Rio Negro basin, Venezuela Bragantina Region, Brazil Eastern Amazonia, Brazil Puerto Rico Averaged among different Oxisols of the world Rio Negro, Venezuela Sandy forest, Amazonia, Brazil Clayey forest, Amazonia, Brazil Hawaii, USA

Scott et al. (1992) Cross and Schlesinger (1995) Uhl and Jordan (1984)

183 208 210-250 269 317 387 429 439 463 558 716

Buschbacher et al. (1988) Medina and Cuevas (1989) Frizano et al. (2003) Johnson et al. (2001) Frizano (1999) Sharpley et al. (1985) Tiessen et al. (1994) Current study Current study Crews et al. (1995)

trees take up available P from lower depths and redistribute it to the soil surface via litterfall and throughfall (Kautz et al., 2013). Chemical changes induced by 0.5 M NaHCO3 addition are slight and resembled root action (Tiessen and Moir, 1993); hence, Bowman and Cole (1978) considered PiBIC as readily plant available. Decrease of this P fraction with depth in both soil textures and land uses can be attributed to the higher turnover of it in the soil surface layer from litterfall in forest and grasses in pasture. Higher inorganic labile P (PAER + PiBIC) in forest compared to pasture in sandy soil can be related to the annual release of P through microbial biomass. Chen et al. (2008) showed that annual release of P via microbial biomass and the turnover rate were higher in forest related to pasture. 60% of P accumulated in microbial pool is bound in nucleic acids and 10% is cytoplasmic organic P (Bünemann et al., 2011) which are plant available in short term and can act as the sources of PAER and PiBIC. Labile P in both soil textures was dominated by PoBIC (82 and 78% in clayey and sandy soil, respectively, considering 0–30 cm depth) which shows the importance of soil organic matter on the P nutrition of plants in Amazonian tropical forests and unfertilized pastures regardless of soil texture. Johnson et al. (2003) stated that PoBIC accounted for 53 and 33% of labile P in highly and slightly weathered soils, respectively. Cross and Schlesinger (1995) observed that 30–60% of labile P accumulates in PoBIC and Sharpley et al. (1987) reported this proportion as slightly more than 50%. Cross and Schlesinger (1995) showed that the proportion of PoBIC increased along the weathering gradient. Proportions of PoBIC show that Amazonian soils in our study are more highly weathered as this proportion is much higher than the previous studies. Although Bowman and Cole (1978) considered PoBIC easily mineralizable which can contribute to available P, these high proportions in our study should be considered with caution as first, bicarbonate extraction occurs at pH 8.5 which mobilizes organic P compounds not soluble under the field condition with acidic pH (Dieter et al., 2010). Second, only a fraction of PoBIC can be considered as plant available as Turner et al. (2003) showed that 37–87% of PoBIC was hydrolyzed by phosphatase enzymes in semi-arid arable soils in USA, while 3–8% was hydrolyzed in Podzolic soils in Canada under permanent pasture (Hayes et al., 2000). Third, air-drying of soil samples in our procedure may increase PoBIC compared to fresh soil (Turner and Haygarth, 2003). The PoBIC contents was not influenced by land use change in our study, while Lessa et al. (1996) observed higher PoBIC contents in pasture in comparison with forest in an Oxisol after burning forest in Savanna and conversion to pasture. They related this increase to higher total soil C content and organic matter decomposition in pasture soils of their study. Zheng et al. (2001) observed lower 8

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more. One possible reason is the changes in soil microbial community with land use change which needs more investigations.

reported by Yang and Post (2011) and even higher than the median sum of the labile P from 39 highly weathered soils (43 mg kg−1) stated by Johnson et al. (2003). Labile P derived from Hedley P fractionation is several times higher than the annual litterfall P (Yang and Post, 2011) and forest P demand (Johnson et al., 2003; Yang and Post, 2011) in tropical soils nevertheless many tropical forests are regarded as P limited (Cuevas and Medina, 1988; Vitousek et al., 2010). Sharpley et al. (1987) and Tiessen et al. (1994) stated that labile P contents in Ultisols and Oxisols are similar to the other soil orders. Johnson et al. (2003) calculated that 10–15% of labile P in forests of humid tropics is derived from annual mineralization of forest floor which will be 5.5–8.3 mg kg−1 in the Amazonian forest sites studied here. Although it can be stated that labile P in pasture is sufficient for optimum plant growth, it should be checked after some more years as P limitation in pasture results in pasture degradation which can be avoided by moderate P fertilization (Hamer et al., 2013). Higher labile P contents in sandy forest compared to sandy pasture was previously observed by Garcia-Montiel et al. (2000) five years after forest clearing in Brazilian Amazon. Mod-labile P fractions are considered unavailable for plant uptake in short term (Cross and Schlesinger, 1995), while they replenish labile P over longer periods of time (Frizano et al., 2002). Mod-labile P fractions accounted for 11 and 13% of total P in clayey and sandy soil, respectively, in 0–30 cm depth, which is not high but important as they can be sources or drains of plant available P in longer period of time (Soltangheisi et al., 2018). The turnover of Po is a fundamental source of available P for plants in tropical soils (Hedley et al., 1982; Beck and Sanchez, 1994; Tiessen et al., 1994; Condron and Tiessen, 2005; Cherubin et al., 2016), especially when Pi reserves are limited (Chimdi et al., 2014). Land use change can modify the chemical nature of Po due to the changes in vegetation (Chen et al., 2008), hence different organic P species should be investigated by 31P-NMR analysis even in sandy soil, where the amount of Po was not changed by land use conversion from forest to pasture. McDowell and Stewart (2006) detected higher levels of orthophosphate monoesters in pasture soils compared to forest soils of five paired sites. Like the clayey soil in our study, Graham et al. (2005) observed higher proportions of Po in natural areas compared to disturbed Histosols. It seems that land use change in clayey soil enhanced mineralization of Po leading to the lower contents of Po in pasture compared to forest. Contrary to our results, some studies showed 13–38% decrease in Po due to the land use change from grassland to plantation forest (Condron et al., 1996; Chen et al., 2000). From 53–100% of the variability in PAER was accounted for by Po which emphasizes the importance of the mineralization of organic P for plant nutrition in tropical weathered Oxisols, even when Po is accounted for only a quarter of total P. Tiessen et al. (1984) observed that 80% of labile P originated from Po in weathered Ultisols. The contribution of Po to PAER was higher in pasture (81% averaged among sandy and clayey soil) compared to forest (59% averaged among sandy and clayey soil) and in clayey soil (82% averaged among forest and pasture) in comparison with sandy soil (58% averaged among forest and pasture). Among different Po fractions, PoBIC was the only fraction which acted as sink of PAER in all land uses and soil textures and it can be considered as the most important P fraction, while Tiessen et al. (1984) and Beck and Sanchez (1994) considered this role for PoHID in highly weathered Ultisols. In forest soils with clayey and sandy textures, six and seven different P fractions acted as a source for PAER, respectively, while in sandy and clayey pasture only three and two different P fractions buffered PAER, respectively. PiBIC and PHID-0.5 (inorganic and organic) could not help to replenish PAER when land use changed from forest to pasture and the diversity of the contribution of different P pools to buffer PAER was reduced. While Hedley et al. (1982) and Tiessen et al. (1984) stated that PHID-0.5 buffers PAER in highly weathered acid soils, we observed that this statement is true in undisturbed forest and when land use changed, PHID-0.5 did not play this role any

4.2. Soil P nutritional status For P nutritional status of soils, many indicators can be used; however, Yang and Post (2011) stated that C:Po ratio is a better indicator of nutrient status of a site rather than considering total P. Po mineralization is independent of C mineralization and occurs by phosphatase enzymes excreted by plant roots and microbes in response to P deficiency (McGill and Cole, 1981). When there is sufficient available P in the soil, phosphatase activity is repressed because Po mineralization is not necessary and hence Po accumulates in the soil. Therefore, when C:Po ratio is < 100, the soil is considered P sufficient (Dieter et al., 2010). In contrast, when soil P is deficient for plant growth, Po should be mineralized to prepare inorganic phosphate for plant uptake. In this situation, Po mineralization exceeds C mineralization and C:Po ratio is > 200 (McGill and Cole, 1981; Dieter et al., 2010; Spohn and Kuzyakov, 2013). Among the sites investigated, sandy forest was the only site with C:Po < 100 and it can be stated that P was not limited for plant growth in this site. C:Po ratio in sandy pasture (101) and clayey pasture (107) were also near to the limit of P sufficiency (100) and these sites can be also considered as P sufficient. Clayey forest had the C:Po ratio of 143, categorized as a site with intermediate P status. Since P mineralization did not contribute to the available P content, there was not any correlation between soil C content and inorganic labile P (R2 = 0.01, Fig. 5B) in sandy forest. In both soil textures, with increasing C:Po ratio, the correlation between soil C content and inorganic labile P increased (Fig. 5), showing that when C:Po ratio enhanced, available P content for plant uptake became more dependent on P mineralization. Higher phosphatase activity in pasture compared to forest in both soil textures was observed in the sites investigated here. The higher activity of phosphomonoesterase and phosphodiesterase under grassland related to the adjacent forest was previously observed (Chen et al., 2000). As phosphatase activity is one of the major biological indicators of soil fertility (Guangming et al., 2017), it can be stated that soil biological fertility in pasture was better than forest in both soil textures. This change can be related to the changes in soil bacterial community (Nüsslein and Tiedje, 1999) or even soil microbial community (Cookson et al., 2007). Higher phosphatase activity in pasture compared to forest means higher Po mineralization and lower Po content. A lower Po content in pasture related to forest was observed in clayey soil, while in sandy soil, Po was not influenced by land use change. The relationships between phosphatase activity and Po mineralization is poorly understood (Chen et al., 2008) despite investigations (Condron and Tiessen, 2005) but it can be stated that this relationship is affected by soil texture. While in clayey soil, Po contents in pasture was lower than forest due to higher phosphatase activity, no relationships were observed in sandy soil. Some studies showed a decrease in PoHID in the rhizosphere of radiata pine due to higher phosphatase activity (Chen et al., 2002; Liu et al., 2004), while Adams (1992) did not see any correlation between Po mineralization and phosphatase activity. Considering the correlations between phosphatase activity and C:Po ratio, it can be stated that when phosphatase activity is higher than 549 and 711 mg kg−1 soil hr−1 (C:P > 200) in Amazonian forest and pasture, respectively, the soil is P deficient, while when phosphatase activity is less than 249 and 437 mg kg−1 soil hr−1 (C:P < 100) in forest and pasture, respectively, the soil is rich in P. Unlike C:Po ratio, we cannot define a unique limit of phosphatase activity related to soil P nutritional status for all land uses and it should be defined for each land use. 5. Conclusion After 15 years from forest slashing and burning, total P in pasture 9

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reaches to the forest levels in Amazonian soils, regardless of soil texture. These soils are more highly weathered and they are at the late stage of development considering higher proportions of PoBIC and Presidual compared to other tropical weathered soils based on Walker and Syers model. Total P and labile P contents in our study sites were also higher than other studies which can be an indication of P sufficiency for plant growth in both land uses and soil textures. In both soil textures, with increasing C:Po ratio, the correlation between soil C content and inorganic labile P increased, showing that when C:Po ratio enhanced, available P content for plant uptake became more dependent on P mineralization. The relationships between phosphatase activity and Po mineralization is affected by soil texture. While in clayey soil, Po contents in pasture was lower than forest due to higher phosphatase activity, no relationships were observed in sandy soil. Phosphatase activity can be used as a factor to evaluate soil P status for plant nutrition but it should be determined for each land use regardless of soil texture. The contribution of Po to PAER was higher in pasture compared to forest and in clayey soil in comparison with sandy soil which shows the importance of organic P in plant nutrition especially in pasture. Land use conversion from forest to pasture decreases the diversity of the contribution of different P pools to buffer PAER. Acknowledgements The authors are grateful to the National Science Foundation (NSF) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), which supported the research (Grant no. 2014/50320-4), and FAPESP for providing scholarships to A.S (Grant no. 2017/11332-5), M.T.M. (Grant no. 2017/18327-7), and D.O.A. (Grant no. 2016/24695-6). References Adams, M.A., 1992. Phosphatase activity and phosphorus fractions in Karri (Eucalyptus diversicolor F. Muell.) forest soils. Biol. Fertil. Soils 14 (3), 200–204. Alvares, C.A., Stape, J.L., Sentelhas, P.C., de Moraes Gonçalves, J.L., Sparovek, G., 2013. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22, 711–728. Beck, M.A., Sanchez, P.A., 1994. Soil phosphorus fraction dynamics during 18 years of cultivation on a Typic Paleudult. Soil Sci. Soc. Am. J. 58 (5), 1424–1431. Bolan, N.S., 1991. A critical review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant Soil 134 (2), 189–207. Bowman, R.A., Cole, C.V., 1978. Transformations of organic phosphorus substances in soil as evaluated by NaHCO: extraction. Soil Sci. 125, 49–54. Box, G.E., Cox, D.R., 1964. An analysis of transformations. J. R. Stat. Soc. Ser. B 211–252. Brookes, P.C., Powlson, D.S., Jenkinson, D.S., 1982. Measurement of microbial biomass phosphorus in soil. Soil Biol. Biochem. 14 (4), 319–329. Bünemann, E.K., Prusisz, B., Ehlers, K., 2011. Characterization of phosphorus forms in soil microorganisms. Phosphorus in Action. Springer, Berlin, Heidelberg, pp. 37–57. Buschbacher, R.J., 1984. Changes in Productivity and Nutrient Cycling Following Conversion of Amazon Rainforest to Pasture. Doctoral dissertation. University of Georgia. Buschbacher, R., Uhl, C., Serrao, E.A.S., 1988. Abandoned pastures in eastern Amazonia. II. Nutrient stocks in the soil and vegetation. J. Ecol. 682–699. Chen, C.R., Condron, L.M., Xu, Z.H., 2008. Impacts of grassland afforestation with coniferous trees on soil phosphorus dynamics and associated microbial processes: a review. For. Ecol. Manage. 255 (3-4), 396–409. Chen, C.R., Condron, L.M., Davis, M.R., Sherlock, R.R., 2000. Effects of afforestation on phosphorus dynamics and biological properties in a New Zealand grassland soil. Plant Soil 220 (1-2), 151–163. Chen, C.R., Condron, L.M., Davis, M.R., Sherlock, R.R., 2002. Phosphorus dynamics in the rhizosphere of perennial ryegrass (Lolium perenne L.) and radiata pine (Pinus radiata D. Don.). Soil Biol. Biochem. 34 (4), 487–499. Cherubin, M.R., Karlen, D.L., Franco, A.L., Tormena, C.A., Cerri, C.E., Davies, C.A., Cerri, C.C., 2016. Soil physical quality response to sugarcane expansion in Brazil. Geoderma 267, 156–168. Chimdi, A., Esala, M., Ylivainio, K., 2014. Sequential fractionation patterns of soil phosphorus collected from different land use systems of Dire Inchine District, West Shawa Zone, Ethiopia. American-Eurasian J. Sci. Res. 9 (3), 51–57. Condron, L.M., Tiessen, H., 2005. Interactions of organic phosphorus in terrestrial ecosystems. Organic Phosphorus in the Environment. pp. 295–307. Condron, L.M., Cornforth, I.S., Davis, M.R., Newman, R.H., 1996. Influence of conifers on the forms of phosphorus in selected New Zealand grassland soils. Biol. Fertil. Soils 21 (1-2), 37–42. Condron, L.M., Goh, K.M., Newman, R.H., 1985. Nature and distribution of soil

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