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Organic and inorganic phosphorus in Mollisol soil under different tillage practices
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Soil & Tillage Research 99 (2008) 131–138 www.elsevier.com/locate/still
Organic and inorganic phosphorus in Mollisol soil under different tillage practices E.C. Zamuner *, L.I. Picone, H.E. Echeverria Unidad Integrada EEA INTA Balcarce – Facultad de Ciencias Agrarias (UNMP), CC 276, 7620 Balcarce, Argentina Received 27 February 2007; received in revised form 28 November 2007; accepted 11 December 2007
Abstract The distribution of soil phosphorus (P) between different organic and inorganic forms depends on, among other factors, the tillage systems. The evaluation of soil P fractions is essential to determine if they are related to available P. The objective was to characterize the P forms from a soil under no tillage (NT) and conventional tillage (CT). Soil samples were taken at 0–5, 5–10 and 10–20 cm depth from a fine, mixed, thermic Petrocalcic Paleoudoll, after 8 years under NT and CT. Inorganic and organic P was measured in the anion exchange membrane (AEM), NaHCO3, NaOH, NaOH after sonication, HCl and residual fractions extracted sequentially. Microbial P was determined by fumigating with chloroform after P extraction with AEM. The tillage systems did not affect the total P content but the distribution of P among fractions changed between NT and CT. No tillage system had significantly higher microbial P at all soil depths and ranged from 34 mg P kg1 at 0–5 cm to 10 mg P kg1 at 10–20 cm. In the upper 10 cm of soil, NT tended to have higher AEM-Pi and NaHCO3-Pi comparing to CT system. The increase in AEM-Pi was closely related to organic carbon increases and pH decreases. The was a consistently higher concentration of NaOH-Po but the increase was significant al 5–10 and 10–20 cm, and represented on average about 35% of total P. The residual P which was considered mostly organic was also an important pool in both NT and CT, and accounted for about 30% of total P. Therefore, P availability is mainly controlled by organic P which makes up a larger proportion of total P. # 2008 Published by Elsevier B.V. Keywords: Phosphorus fractions; No tillage; Tiessen fractionation
1. Introduction Soil phosphorus (P) is described kinetically as soluble, labile, and non-labile P, where the equilibrium between labile and non-labile P is slower than the equilibrium between soluble and labile P (Larsen, 1967). This suggests that there is a continuum among different forms of soil P; however the fractionation procedures that use chemical sequential extractions can separate the continuum in different P fractions but
* Corresponding author. E-mail address: [email protected] (E.C. Zamuner). 0167-1987/$ – see front matter # 2008 Published by Elsevier B.V. doi:10.1016/j.still.2007.12.006
without identifying the type of P compounds. The fractionation method developed by Hedley et al. (1982) has been widely used to characterize the organic and inorganic forms of P that differ in availability to plants and microorganisms. The fractionation procedure allows examining the P fractions that participate in short and long-term transformations in soil. This procedure also helps to carry out a complete balance of different forms of P and to evaluate the availability of organic P for plant used. The distribution of P between inorganic and organic fractions depends in part, among other factors, on tillage systems (Selles et al., 1999; Essington and Howard, 2000; Daroub et al., 2000). The widespread adoption of
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conservation tillage, particularly no tillage, have not only been affecting certain soil physical properties (Beare et al., 1994; Sauer et al., 1996; Thompson, 2001), but also causes a decrease in the residues decomposition rate (Paustian et al., 1997), and qualitative and quantitative changes in microbial biomass (Mccarty et al., 1995), Selles et al. (1999) observed that the conversion from the original cultivator, tilled fallow-wheat to zero-tilled continuous wheat system caused a significant increase in total soil P in the surface 6 cm of the soil. According to Selles et al. (1999), the increase in total P in their study was a result of accumulation of labile and moderately labile organic forms of P. Similarly, Essington and Howard (2000) reported that plots under no tillage management had significantly greater values of organic P than those under conventional tillage. However, in experiments carried out by Weil et al. (1988) and Urioste et al. (1996) it was demonstrated that the organic P concentration at the soil surface was not affected by tillage practices. Previous studies (Weil et al., 1988; Urioste et al., 1996; Selles et al., 1999; Essington and Howard, 2000) related to the effect of different management practices, especially tillage, showed contradictory results on soil P transformations especially in organic P form. In the mean time, there is a lack of information about the effect of different cropping practices on the distribution of P within inorganic and organic fractions. Such information is essential to understand soil P dynamics and to determine if transformations between inorganic and organic fractions are related to P availability. Therefore, the objective of this study was to determine the quantity and the distribution of soil organic and inorganic P at different depths with no tillage or conventional tillage practices. 2. Materials and methods 2.1. Site description and experimental design A field experiment was conducted from 1992 to 2000 at the Balcarce Experimental Station of the National Institute of Agricultural Technology (INTA) located in the southeastern area of Buenos Aires province, Argentina (378450 S latitude, 588180 W longitude). The soil was a complex of fine, mixed, thermic Typic Argiudolls and fine, mixed, thermic Petrocalcic Paleudoll (USA soil classification). It has a mollic epipedon that is thick (0–23 cm), very dark in color due to its high organic matter content (6.93–7.06%), and an argilic horizon with textural class is clay loam due to accumulation of clay (31–33%). In this soil, both A and B horizons show a high
base saturation (70–99%) and cation exchange capacity (18.2–30.3 cmol kg1). Accumulation of calcium carbonate is found below 70 cm in the Petrocalcic Paleudoll soil while, and in general, there is no accumulation of carbonate in the profile of the Typic Argiudoll soil. http:// olavarria.coopenet.com.ar/sallies/serie.htm [Consulted 27/11/07]. The region is used for agriculture production and soil had developed under grass vegetation, being loess, an eolic sediment of the quaternary period and rich in calcareous material, the parent material. The soil is located in an area with low ondulations (30–600 m over sea level) and slight slopes (0.5–2.5%). The pH at the surface layer ranged from 5.6 to 6.1. The experiment was established in 1992 on field that had been under continuous conventional tillage for the last 25 year, with a soil bulk density of 1.45 Mg m3 (Ferreras et al., 2000). The climate of the region is to between humid sub humid mesothermal with an annual average temperature of 13 8C and an annual average precipitation of 928 mm, 80% of rainfall occurs in the spring–summer period. The experiment design was randomized complete block with three replications. The treatments consisted on two tillage systems, conventional tillage (CT) and no tillage (NT) with the same crop rotation: spring wheat [Triticum aestivum L.] (1992/1993), soybean [Glycine max (L.) Merr] (1993/1994), spring wheat (1994), corn [Zea mays L.] (1995/1996 and 1996/1997), sunflower [Heliantus annus sp.] (1997/1998), corn (1998/1999), soybean (1999/2000) and pea [Pisum sativum L.] (2000/ 2001). The CT treatment consisted of one moldboard plow tillage operation at 0–20 cm depth, and one to three disking to a depth of 8–10 cm every year for seed bed preparation. The NT treatment consisted of chemical weed control during the fallow period with Glyphosate and 2,4-D, and seeding directly into the standing residues of the previous crop. For weed control was applied in pre-emergence Atrazine plus Metolachlor in corn and Fluorchloridone plus Metolachlor in sunflower; and in post-emergence Metsulfuron plus Dicamba in wheat. Nitrogen fertilizer, urea, was broadcast each year at the rate of 120 kg N ha1 prior to seeding. Phosphorus fertilizer, monocalcic superphosphate, was applied by banding into the soil on average rate of 30 kg P ha1 all years. The size of plots was 120 m2 (3 m wide 40 m long). 2.2. Soil sampling Soil samples were collected in October of 2000, before planting pea crop and after tillage operations. Soil cores were taken with an auger (20 cm long and
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2.5 cm diameter) to a depth of 20 cm and segmented into 0–5, 5–10 and 10–20 cm. Each soil sample was composed at least of 30 sub-samples. The soil samples were homogenized, air-dried and sieved to <2 mm. A sub-sample (50 g) was ground in a roller mill, sieved to <0.5 mm (Selles et al., 1999) and stored at room temperature until analysis. 2.3. Analytical procedures Soil samples were subjected to the sequential fractionation procedure as described by Tiessen and Moir (1993) (Fig. 1), with three modifications: (1) P
Fig. 1. Diagram of the sequential phosphorus procedure modified from Tiessen and Moir (1993).
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held by the anion-exchange membrane (type 204-PZL386. Ionics, Watertown, MA) was extracted by shaking the membrane with 1 M NaCl for 1 h (Cooperband and Logan, 1994) instead of 16 h with 0.5 M HCl, (2) a sonification step was included using 0.1 M NaOH after ultrasonification for 2 min at a power of 100 W (Aweep Zone, Quantrex S 200), and (3) P extraction with hot concentrated HCl was omitted. Briefly, 0.5 g of air dry soil was placed into a 50-mL centrifuge tube and sequentially extracted with 30 mL distilled H2O and two anion- exchange membrane strips (6 cm 1 cm), with 30 mL 0.5 M NaHCO3 (pH 8.5), with 30 mL 0.1 M NaOH, with 30 mL 0.1 M NaOH after ultrasonification, and with 30 mL 1 M HCl to remove soluble P, weakly adsorbed P, Fe/Al-P, Fe/Al-P within aggregates and Ca-P; respectively. After shaking for 16 h, samples were centrifuged at 25,000 g for 10 min at 0 8C, and inorganic P (Pi) was determined in the supernatant. In the last step, residual P was determined by digestion of soil residue with concentrated H2SO4 and H2O2 at 360 8C, and then analyzed for Pi. Total P was also quantified in the NaHCO3 and NaOH extracts, after oxidizing the organic P (Po) with ammonium persulfate and 0.9 M H2SO4 in an autoclave at 121 8C. The Po concentration was estimated as the difference between total P and Pi in these fractions. In soil samples not subjected to P fractionation, microbial P was determined by fumigating the soil with chloroform after P extraction with anion-exchange membrane (Hedley and Stewart, 1982). Two sets of airdried, <0.5 mm sieved soil samples, were shaken with 30 mL of H2O and two anion-exchange membranes for 16 h at 24 8C. After shaking, the membranes were removed, the soil was centrifuged at 25,000 g for 10 min at 0 8C, and the supernatant was discarded. One set of soil samples was fumigated with 1 mL of chloroform (ethanol free) overnight at room temperature, and the other set was kept under the same conditions without chloroform, unfumigated. The Pi released in fumigated and unfumigated samples was extracted by shaking with 30 mL 0.5 M NaHCO3 (adjusted to a pH of 8.5) for 16 h, and centrifuging at 25,000 g for 10 min at 0 8C. The supernatant was analyzed for Pi. Microbial P was calculated as the difference in NaHCO3-Pi between fumigated and unfumigated soil samples and using a recovery factor of 0.4 (Brookes et al., 1982). The Pi concentration was measured colorimetrically according to the method described by Murphy and Riley (1962) previous pH adjustment between 5.4 and 6.6 with H2SO4 or NaOH, using p-nitrophenol as an
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indicator. All laboratory analyses were conducted in duplicate, and P concentration was expressed in mg P kg1 on soil oven dried bases. In order to make easy the interpretation of the results, the P fractions were classified in three groups according to the criteria given by Bowman and Cole (1978) and Tiessen et al. (1984): (1) labile P included Pi extracted with anion-exchange membranes (AEM-Pi), NaHCO3Pi, NaHCO3-Po and microbial-P; (2) moderately labile P included the NaOH-Pi, NaOH-Po, NaOH-Pi and NaOH-Po after applying ultrasound, and HCl-Pi fractions; and (3) non-labile P included the residual P fraction extracted with H2SO4–H2O2. Soil pH was measured in distilled water with a soil:H2O ratio of 1:2.5. Organic carbon content was determined by wet oxidation with K2Cr2O7 and H2SO4 (Walkley and Black, 1934). Bray P was extracted as described by Bray and Kurtz (1945). Total Pi was determined sequentially with concentrated HCl at room temperature, followed by an extraction with 0.5N NaOH at room temperature and 0.5N NaOH at 90 8C (Mehta et al., 1954). 2.4. Statistical analyses The effects of tillage system on soil P fractions were evaluated for each depth, with analysis of variance using the General Linear Model Procedure (PROC GLM) of SAS program (SAS Institute, 1996), and the least significant difference test (LSD) to separate means between treatments. All tests of significance were made at p < 0.05 unless stated otherwise. Correlation analyses were performed to determine the relationships between AEM-Pi with Bray 1-P, organic carbon, pH and microbial P. Pearson coefficients were calculated using the PROC CORR procedure of SAS program (SAS Institute, 1996). 3. Results and discussion 3.1. General soil characteristics After 8 years under NT, the organic carbon concentration increased significantly in the surface 10 cm of soil, not being observed significant differences due to tillage systems below the 10 cm soil depth (Table 1). The carbon contribution through crop residues, from 1992 to 1998, was estimated taking into account the harvest index and assuming that residues have in average 45% of C. According to the calculation, the amount of carbon that returns to the soil was similar with both tillage systems (Table 2). Therefore, the higher organic carbon concentration
Table 1 Soil organic carbon content and pH in no tillage (NT) and conventional tillage (CT) in the 0–20 cm depth Organic carbon (g kg1)
pH
0–5 cm NT CT
34.06a 28.38b
5.6a 6.1b
5–10 cm NT CT
29.86a 27.72b
5.6a 5.8a
10–20 cm NT CT
28.38a 27.19a
5.8a 5.8a
Treatment
Means values followed by the same letter within the same depth are not significantly different ( p < 0.05) according to LSD test.
observed in NT could be attributed to the lower residues decomposition rate and stable fractions of soil organic matter (Paustian et al., 1997). The NT system caused a significant reduction in soil pH by 0.5 units in the upper 5 cm depth; but no significant differences in soil pH was detected in deeper depths between NT and CT practices (Table 1). The reduction in soil pH at the surface NT could be due to the combination of surface urea broadcast (Rothon, 2000) and the higher amount of organic carbon on mineralization results in additional production of organic acids (Stevenson and Cole, 1999). 3.2. Soil phosphorus fractionation 3.2.1. Labile phosphorus In the three soil depths, the labile Pi tended to increase in the soil under NT compared with CT, but none of the increase was statistically significant (Table 3). O’Halloran (1993) reported a higher concentration of labile Pi at the surface layer in NT compared with CT as result of the accumulation of P fertilizer and crop residues. The AEM-Pi represented a small fraction of the total P, on average, 7%; and because AEM-Pi is a source of P for plants and microorganisms in a short period of time (Cross and Schlesinger, 1995) it plays a significant role in crop production which is corroborated with the high and significant correlation between AEM-Pi and Bray 1-P (r = 0.99; p < 0.05) (data are not shown). In addition, the AEM-Pi was positively and significantly correlated with organic carbon (r = 0.79), and negatively correlated with soil pH (r = 0.49) (Fig. 2). It seems that the decreases in soil pH stimulated the development of positive charges (Barrow, 1984) and the
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Table 2 Annual carbon input to soil with crop residues in no tillage (NT) and conventional tillage (CT) Year
1992 1993 1994 1995 1996 1997 1998 1999
Crop
Harvest index (%)
Yield grain (Mg ha1)
Wheat Soybean Wheat Corn Corn Sunflower Corn Soybean
Residue (Mg ha1)
C added to soil (Mg ha1)
NT
CT
NT
CT
NT
CT
NT
CT
5.5 4.4 5.5 7.3 8.6 3.3 8.0 #
6.2 4.4 6.5 6.3 10.2 3.4 4.3 #
45 40 45 45 45 35 45 #
45 40 45 45 45 35 45 #
8.2 6.6 8.2 10.9 3.9 6.1 12 #
9.3 6.6 9.7 9.4 15.3 6.3 8.0 #
3.7 3.0 3.7 4.9 1.7 2.8 5.4 #
4.2 3.0 4.4 4.2 6.9 2.8 3.6 #
(#) Data no available. Based on the assumption that carbon content in residues was 45%. Harvest index was the ratio between grain yield and dried matter.
increases in organic carbon promoted P retention (Sanyal and de Datta, 1991) which could explain the trend to increase the AEM-Pi in NT, especially in the soil surface. In contrast to labile Pi fractions, the labile Po fraction such as NaHCO3-Po significantly decreased, at 0–5 cm depth, in NT compared with CT (Table 3). Under NT, the increase in AEM-Pi and NaHCO3-Pi was parallel with the decrease in NaHCO3-Po suggesting a linkage among these fractions and a potential contribution of mineralizable labile Po to labile Pi fraction. According to Bowman and Cole (1978), the Po extracted with NaHCO3 has been considered to be an active fraction of soil Po, because it represents compounds such as glycerophosphate and ribonucleic acid which are readily exchangeable from the soil. Significant differences in microbial P concentration were observed between tillage systems. Microbial P in NT was higher than CT at all sampling depths (Table 4)
probably due to more favorable soil conditions under NT. In fact, soil organic carbon content, which is an important source of energy for the heterotrophic microorganisms, was higher under NT comparing to CT. In addition, the decrease of microbial P concentration with increasing soil depth coincided with the decrease of soil organic matter. Aslam et al. (1999) and Daroub et al. (2000) found higher microbial P and organic matter content in the top layer of NT than in ploughed soils. The microbial P was closely related to AEM-Pi (r = 0.97) emphasizing on the importance of available P in controlling the microbial P (Fig. 2). Similarly, Chauhan et al. (1981) observed a positive relationship between concentration of Pi in solution and P assimilation by microbial biomass. 3.2.2. Moderately labile phosphorus No significant changes in HCl-Pi occurred as a result of the different tillage systems. However the HCl-Pi
Table 3 Phosphorus concentration in inorganic (Pi) and organic (Po) fractions in no tillage (NT) and conventional tillage (CT), at three soil depths Treatment
Phosphorus fractions (mg kg1) Ultrasonic-NaOH
HCl
Pi
Po
Pi
Po
Pi
Po
Pi
52.46a 28.69a
36.52a 23.30a
43.00b 50.00a
50.07a 39.40a
202.07a 180.90a
10.35a 8.00a
23.34b 29.76a
5–10 cm depth NT 35.10a CT 23.09a
29.65a 19.72a
41.37a 48.24a
39.67a 35.64a
212.48a 166.06b
7.73a 7.69a
10–20 cm depth NT 12.75a CT 18.02a
15.59a 18.33a
41.24a 50.16a
22.46a 32.50a
188.45a 162.63b
6.26a 7.80a
AEM-Pi
0–5 cm depth NT CT
NaOH
NaHCO3
Residual (Pi, Po)
Total P (sum)
53.96a 45.13a
164.37a 153.41a
636.62a 558.62a
22.88a 28.71a
50.44a 44.77a
150.55a 145.37a
589.65a 519.28a
22.80b 28.33a
43.11a 42.44a
157.06a 163.64a
509.75a 523.84a
Means values followed by the same letter within the same depth are not significantly different ( p < 0.05) according to LSD test.
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Fig. 2. Relationships between anion-exchange membrane extractable P (AEM-Pi) and total organic carbon (a), pH (b), and microbial biomass P (c).
represented the highest concentration of Pi, accounting for 8% of the total P in both systems, followed by NaOH-Pi (Table 3). These values for HCl-Pi were expected since this soil was characterized by having a high bases saturation percentage with Ca2+ as a main exchangeable cation (Fabrizzi et al., 1998). The NT system had consistently higher fraction of NaOH-Po and NaOH-Pi than the CT system, where the increase was significant at 5–10 and 10–20 cm depths for NaOH-Po (Table 3). Cabria et al. (2005) reported that continuous agriculture under CT caused a reduction in macroaggregate mass and decrease in Fe concentration associated with organic compound. According to Schoenau et al. (1989) NaOH-Po and NaOH-Pi are associated with humic compounds and adsorbed to Al and Fe. Therefore, as the soil organic matter and Fe concentration reduced with CT, the soil capacity to retain P in form of NaOH-Po and NaOH-Pi diminished. The NaOH-Po and NaOH-Pi constituted Table 4 Size of soil microbial biomass phosphorus according to the Hedley and Stewart (1982) method in no tillage (NT) and conventional tillage (CT), at three soil depths Treatment
Microbial biomass P (mg P kg1)
0–5 cm depth NT CT
13.54a 3.88b
33.75a 9.75b
5–10 cm depth NT CT
14.50a 0.43b
36.25a 1.00b
10–20 cm depth NT CT
3.97a 0.10b
10.00a 0.25b
Means values followed by the same letter within the same depth are not significantly different ( p < 0.05) according to LSD test. Microbial biomass calculated from chloroform-released 0.5N NaHCO3-P (first column) and using a recovery factor of 0.4 (second column).
the majority of the total P in the surface and subsurface layers, where NaOH-Po and NaOH-Pi were almost 40% of total P. Physically protected P (ultrasonic NaOH-Pi and NaOH-Po) was not affected by tillage practices, with the exception of NT that showed a significant decrease in ultrasonic NaOH-Po at 0–5 and 10–20 cm depths (Table 3). In the three sampling depths and both tillage systems, the Po concentration exceeded by a factor of two or three the Pi concentration indicating that an important proportion of Po is sequestered within aggregates and can be susceptible to decomposition after physical disruption of aggregates. 3.2.3. Non-labile phosphorus Residual P was not affected by tillage systems, possibly because this fraction includes the chemically more stable and insoluble forms of P which changes over a long period of time (Cross and Schlesinger, 1995). The residual P fraction was the second largest fraction after NaOH-Po plus NaOH-Pi, and represented up to 31% of the total P (Table 3). Residual P was quantified without partitioning in residual-Po and Pi; however it can infer its composition by comparing the total Pi, determined according to Metha method, with the sum of Pi fractions extracted by the sequential procedure. The total Pi and the sum of AEM-Pi, NaHCO3-Pi, NaOH-Pi and HCl-Pi fractions, average of tillage systems and soil depths, were 157 and 143 mg P kg1, respectively. The sum of these four fractions accounted for about 91% of the total Pi. These values demonstrated that most of the total Pi was recovery in the labile and moderately labile Pi fractions while a small proportion was related to residual Pi, therefore residual P was considered entirely organic. This observation agrees with Tiessen et al. (1983) who reported that the residual P in Mollisols contains a large proportion of organically bound P.
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4. Conclusion In this study the tillage systems did not affect the total P content, however the distribution of inorganic and organic fractions changed between NT and CT management systems. No tillage system had significantly higher microbial P, and a trend to have higher AEM-Pi and NaHCO3-Pi comparing to CT system. The increase in AEM-Pi was closely related to organic carbon content and pH. The greater concentration of labile P in NT soil would lead to a greater availability of this nutrient for plants. Therefore more research is required to investigate the relationships between organic and inorganic P fractions and P plant uptake in these systems. The Po extracted with NaOH increased under NT and represented on average about 35% of total P. The residual P which was considered mostly organic was also an important pool in both NT and CT, and accounted for about 30% of total P. Therefore, P availability is mainly controlled by organic P which makes up a larger proportion of total P. Acknowledgments The authors acknowledge Facultad de Ciencias Agrarias (UNMdP) and EEA-INTA Balcarce for financial support. References Aslam, T., Choudhry, M.A., Saggar, S., 1999. Tillage impacts on soil microbial biomass C, N and P, earthworms and agronomy after two years of cropping following permanent pasture in New Zealand. Soil Till. Res. 51, 103–111. Barrow, N.J., 1984. Modeling effects of pH on phosphate sorption by soils. J. Soil Sci. 35, 283–297. Beare, M.H., Hendrix, P.F., Coleman, D.C., 1994. Water-stable aggregates and organic matter fractions in conventional and no tillage soils. Soil Sci. Am. J. 58, 787–795. Bowman, R.A., Cole, C.V., 1978. An exploratory method for fractionation of organic phosphorus from grassland soils. Soil Sci. 125, 95–101. Bray, R.H., Kurtz, L.T., 1945. Determination of total, organic, and available forms of phosphorus in soils. Soil Sci. 59, 39–45. Brookes, P.C., Powlson, D.S., Jenkinson, D.S., 1982. Measurement of microbial biomass phosphorus in soil. Soil Biol. Biochem. 14, 319–329. ´ xidos de Fe Cabria, F.N., Bianchini, M.R., Mediavilla, M.C., 2005. O libre asociados a carbono orga´nico en agregados de suelos del partido de Balcarce. Free iron oxides associated to organic carbon in soil aggregates in Balcarce county. Ciencia del Suelo. 23, 23– 29. Chauhan, B.S., Stewart, J.W.B., Paul, E.A., 1981. Effect of labile inorganic phosphate status and organic carbon additions on the microbial uptake of phosphorus in soils. Can. J. Soil Sci. 61, 373– 385.
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Thompson, C.A., 2001. Winter wheat and grain sorghum production as influenced by depth of soil water, tillage and cropping system. J. Soil Water Conserv. 56, 56–63. Tiessen, H., Stewart, J.W.B., Moir, J.O., 1983. Changes in organic and inorganic phosphorus composition of two grassland soils and their particle fractions during 60–70 years of cultivation. J. Soil Sci. 34, 815–823. Tiessen, H., Stewart, J.W.B., Cole, C.V., 1984. Pathways of phosphorus transformations in soil of differing pedogenesis. Soil Sci. Soc. Am. J. 48, 853–858. Tiessen, H., Moir, J.O., 1993. Characterization of available P by sequential extraction. In: Carter, M.R. (Ed.), Soil Sampling and
Methods of Analysis. Canadian Soc. Soil Sci. Lewis Publ., Boca Raton, FL, pp. 75–86. Urioste, A.M., Bono, A.A., Buschiazzo, D.E., Hevia, G.G., Hepper, E.N., 1996. Fracciones de fo´sforo en suelos agrı´colas y pastoriles de la regio´n semia´rida pampeana central (Argentina). Ciencia del Suelo 14, 92–95. Walkley, A., Black, I.A., 1934. An examination of the Degtjareff method for determining soil organic matter and a proposed modification of the chromic acid titration method. Soil Sci. 37, 29–38. Weil, R.R., Benedetto, P.W., Sikora, L.J., Bandel, V.A., 1988. Influence of tillage practices on phosphorus distribution and forms in three Ultisols. Agron. J. 80, 503–509.
Soil & Tillage Research 99 (2008) 131–138 www.elsevier.com/locate/still
Organic and inorganic phosphorus in Mollisol soil under different tillage practices E.C. Zamuner *, L.I. Picone, H.E. Echeverria Unidad Integrada EEA INTA Balcarce – Facultad de Ciencias Agrarias (UNMP), CC 276, 7620 Balcarce, Argentina Received 27 February 2007; received in revised form 28 November 2007; accepted 11 December 2007
Abstract The distribution of soil phosphorus (P) between different organic and inorganic forms depends on, among other factors, the tillage systems. The evaluation of soil P fractions is essential to determine if they are related to available P. The objective was to characterize the P forms from a soil under no tillage (NT) and conventional tillage (CT). Soil samples were taken at 0–5, 5–10 and 10–20 cm depth from a fine, mixed, thermic Petrocalcic Paleoudoll, after 8 years under NT and CT. Inorganic and organic P was measured in the anion exchange membrane (AEM), NaHCO3, NaOH, NaOH after sonication, HCl and residual fractions extracted sequentially. Microbial P was determined by fumigating with chloroform after P extraction with AEM. The tillage systems did not affect the total P content but the distribution of P among fractions changed between NT and CT. No tillage system had significantly higher microbial P at all soil depths and ranged from 34 mg P kg1 at 0–5 cm to 10 mg P kg1 at 10–20 cm. In the upper 10 cm of soil, NT tended to have higher AEM-Pi and NaHCO3-Pi comparing to CT system. The increase in AEM-Pi was closely related to organic carbon increases and pH decreases. The was a consistently higher concentration of NaOH-Po but the increase was significant al 5–10 and 10–20 cm, and represented on average about 35% of total P. The residual P which was considered mostly organic was also an important pool in both NT and CT, and accounted for about 30% of total P. Therefore, P availability is mainly controlled by organic P which makes up a larger proportion of total P. # 2008 Published by Elsevier B.V. Keywords: Phosphorus fractions; No tillage; Tiessen fractionation
1. Introduction Soil phosphorus (P) is described kinetically as soluble, labile, and non-labile P, where the equilibrium between labile and non-labile P is slower than the equilibrium between soluble and labile P (Larsen, 1967). This suggests that there is a continuum among different forms of soil P; however the fractionation procedures that use chemical sequential extractions can separate the continuum in different P fractions but
* Corresponding author. E-mail address: [email protected] (E.C. Zamuner). 0167-1987/$ – see front matter # 2008 Published by Elsevier B.V. doi:10.1016/j.still.2007.12.006
without identifying the type of P compounds. The fractionation method developed by Hedley et al. (1982) has been widely used to characterize the organic and inorganic forms of P that differ in availability to plants and microorganisms. The fractionation procedure allows examining the P fractions that participate in short and long-term transformations in soil. This procedure also helps to carry out a complete balance of different forms of P and to evaluate the availability of organic P for plant used. The distribution of P between inorganic and organic fractions depends in part, among other factors, on tillage systems (Selles et al., 1999; Essington and Howard, 2000; Daroub et al., 2000). The widespread adoption of
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conservation tillage, particularly no tillage, have not only been affecting certain soil physical properties (Beare et al., 1994; Sauer et al., 1996; Thompson, 2001), but also causes a decrease in the residues decomposition rate (Paustian et al., 1997), and qualitative and quantitative changes in microbial biomass (Mccarty et al., 1995), Selles et al. (1999) observed that the conversion from the original cultivator, tilled fallow-wheat to zero-tilled continuous wheat system caused a significant increase in total soil P in the surface 6 cm of the soil. According to Selles et al. (1999), the increase in total P in their study was a result of accumulation of labile and moderately labile organic forms of P. Similarly, Essington and Howard (2000) reported that plots under no tillage management had significantly greater values of organic P than those under conventional tillage. However, in experiments carried out by Weil et al. (1988) and Urioste et al. (1996) it was demonstrated that the organic P concentration at the soil surface was not affected by tillage practices. Previous studies (Weil et al., 1988; Urioste et al., 1996; Selles et al., 1999; Essington and Howard, 2000) related to the effect of different management practices, especially tillage, showed contradictory results on soil P transformations especially in organic P form. In the mean time, there is a lack of information about the effect of different cropping practices on the distribution of P within inorganic and organic fractions. Such information is essential to understand soil P dynamics and to determine if transformations between inorganic and organic fractions are related to P availability. Therefore, the objective of this study was to determine the quantity and the distribution of soil organic and inorganic P at different depths with no tillage or conventional tillage practices. 2. Materials and methods 2.1. Site description and experimental design A field experiment was conducted from 1992 to 2000 at the Balcarce Experimental Station of the National Institute of Agricultural Technology (INTA) located in the southeastern area of Buenos Aires province, Argentina (378450 S latitude, 588180 W longitude). The soil was a complex of fine, mixed, thermic Typic Argiudolls and fine, mixed, thermic Petrocalcic Paleudoll (USA soil classification). It has a mollic epipedon that is thick (0–23 cm), very dark in color due to its high organic matter content (6.93–7.06%), and an argilic horizon with textural class is clay loam due to accumulation of clay (31–33%). In this soil, both A and B horizons show a high
base saturation (70–99%) and cation exchange capacity (18.2–30.3 cmol kg1). Accumulation of calcium carbonate is found below 70 cm in the Petrocalcic Paleudoll soil while, and in general, there is no accumulation of carbonate in the profile of the Typic Argiudoll soil. http:// olavarria.coopenet.com.ar/sallies/serie.htm [Consulted 27/11/07]. The region is used for agriculture production and soil had developed under grass vegetation, being loess, an eolic sediment of the quaternary period and rich in calcareous material, the parent material. The soil is located in an area with low ondulations (30–600 m over sea level) and slight slopes (0.5–2.5%). The pH at the surface layer ranged from 5.6 to 6.1. The experiment was established in 1992 on field that had been under continuous conventional tillage for the last 25 year, with a soil bulk density of 1.45 Mg m3 (Ferreras et al., 2000). The climate of the region is to between humid sub humid mesothermal with an annual average temperature of 13 8C and an annual average precipitation of 928 mm, 80% of rainfall occurs in the spring–summer period. The experiment design was randomized complete block with three replications. The treatments consisted on two tillage systems, conventional tillage (CT) and no tillage (NT) with the same crop rotation: spring wheat [Triticum aestivum L.] (1992/1993), soybean [Glycine max (L.) Merr] (1993/1994), spring wheat (1994), corn [Zea mays L.] (1995/1996 and 1996/1997), sunflower [Heliantus annus sp.] (1997/1998), corn (1998/1999), soybean (1999/2000) and pea [Pisum sativum L.] (2000/ 2001). The CT treatment consisted of one moldboard plow tillage operation at 0–20 cm depth, and one to three disking to a depth of 8–10 cm every year for seed bed preparation. The NT treatment consisted of chemical weed control during the fallow period with Glyphosate and 2,4-D, and seeding directly into the standing residues of the previous crop. For weed control was applied in pre-emergence Atrazine plus Metolachlor in corn and Fluorchloridone plus Metolachlor in sunflower; and in post-emergence Metsulfuron plus Dicamba in wheat. Nitrogen fertilizer, urea, was broadcast each year at the rate of 120 kg N ha1 prior to seeding. Phosphorus fertilizer, monocalcic superphosphate, was applied by banding into the soil on average rate of 30 kg P ha1 all years. The size of plots was 120 m2 (3 m wide 40 m long). 2.2. Soil sampling Soil samples were collected in October of 2000, before planting pea crop and after tillage operations. Soil cores were taken with an auger (20 cm long and
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2.5 cm diameter) to a depth of 20 cm and segmented into 0–5, 5–10 and 10–20 cm. Each soil sample was composed at least of 30 sub-samples. The soil samples were homogenized, air-dried and sieved to <2 mm. A sub-sample (50 g) was ground in a roller mill, sieved to <0.5 mm (Selles et al., 1999) and stored at room temperature until analysis. 2.3. Analytical procedures Soil samples were subjected to the sequential fractionation procedure as described by Tiessen and Moir (1993) (Fig. 1), with three modifications: (1) P
Fig. 1. Diagram of the sequential phosphorus procedure modified from Tiessen and Moir (1993).
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held by the anion-exchange membrane (type 204-PZL386. Ionics, Watertown, MA) was extracted by shaking the membrane with 1 M NaCl for 1 h (Cooperband and Logan, 1994) instead of 16 h with 0.5 M HCl, (2) a sonification step was included using 0.1 M NaOH after ultrasonification for 2 min at a power of 100 W (Aweep Zone, Quantrex S 200), and (3) P extraction with hot concentrated HCl was omitted. Briefly, 0.5 g of air dry soil was placed into a 50-mL centrifuge tube and sequentially extracted with 30 mL distilled H2O and two anion- exchange membrane strips (6 cm 1 cm), with 30 mL 0.5 M NaHCO3 (pH 8.5), with 30 mL 0.1 M NaOH, with 30 mL 0.1 M NaOH after ultrasonification, and with 30 mL 1 M HCl to remove soluble P, weakly adsorbed P, Fe/Al-P, Fe/Al-P within aggregates and Ca-P; respectively. After shaking for 16 h, samples were centrifuged at 25,000 g for 10 min at 0 8C, and inorganic P (Pi) was determined in the supernatant. In the last step, residual P was determined by digestion of soil residue with concentrated H2SO4 and H2O2 at 360 8C, and then analyzed for Pi. Total P was also quantified in the NaHCO3 and NaOH extracts, after oxidizing the organic P (Po) with ammonium persulfate and 0.9 M H2SO4 in an autoclave at 121 8C. The Po concentration was estimated as the difference between total P and Pi in these fractions. In soil samples not subjected to P fractionation, microbial P was determined by fumigating the soil with chloroform after P extraction with anion-exchange membrane (Hedley and Stewart, 1982). Two sets of airdried, <0.5 mm sieved soil samples, were shaken with 30 mL of H2O and two anion-exchange membranes for 16 h at 24 8C. After shaking, the membranes were removed, the soil was centrifuged at 25,000 g for 10 min at 0 8C, and the supernatant was discarded. One set of soil samples was fumigated with 1 mL of chloroform (ethanol free) overnight at room temperature, and the other set was kept under the same conditions without chloroform, unfumigated. The Pi released in fumigated and unfumigated samples was extracted by shaking with 30 mL 0.5 M NaHCO3 (adjusted to a pH of 8.5) for 16 h, and centrifuging at 25,000 g for 10 min at 0 8C. The supernatant was analyzed for Pi. Microbial P was calculated as the difference in NaHCO3-Pi between fumigated and unfumigated soil samples and using a recovery factor of 0.4 (Brookes et al., 1982). The Pi concentration was measured colorimetrically according to the method described by Murphy and Riley (1962) previous pH adjustment between 5.4 and 6.6 with H2SO4 or NaOH, using p-nitrophenol as an
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indicator. All laboratory analyses were conducted in duplicate, and P concentration was expressed in mg P kg1 on soil oven dried bases. In order to make easy the interpretation of the results, the P fractions were classified in three groups according to the criteria given by Bowman and Cole (1978) and Tiessen et al. (1984): (1) labile P included Pi extracted with anion-exchange membranes (AEM-Pi), NaHCO3Pi, NaHCO3-Po and microbial-P; (2) moderately labile P included the NaOH-Pi, NaOH-Po, NaOH-Pi and NaOH-Po after applying ultrasound, and HCl-Pi fractions; and (3) non-labile P included the residual P fraction extracted with H2SO4–H2O2. Soil pH was measured in distilled water with a soil:H2O ratio of 1:2.5. Organic carbon content was determined by wet oxidation with K2Cr2O7 and H2SO4 (Walkley and Black, 1934). Bray P was extracted as described by Bray and Kurtz (1945). Total Pi was determined sequentially with concentrated HCl at room temperature, followed by an extraction with 0.5N NaOH at room temperature and 0.5N NaOH at 90 8C (Mehta et al., 1954). 2.4. Statistical analyses The effects of tillage system on soil P fractions were evaluated for each depth, with analysis of variance using the General Linear Model Procedure (PROC GLM) of SAS program (SAS Institute, 1996), and the least significant difference test (LSD) to separate means between treatments. All tests of significance were made at p < 0.05 unless stated otherwise. Correlation analyses were performed to determine the relationships between AEM-Pi with Bray 1-P, organic carbon, pH and microbial P. Pearson coefficients were calculated using the PROC CORR procedure of SAS program (SAS Institute, 1996). 3. Results and discussion 3.1. General soil characteristics After 8 years under NT, the organic carbon concentration increased significantly in the surface 10 cm of soil, not being observed significant differences due to tillage systems below the 10 cm soil depth (Table 1). The carbon contribution through crop residues, from 1992 to 1998, was estimated taking into account the harvest index and assuming that residues have in average 45% of C. According to the calculation, the amount of carbon that returns to the soil was similar with both tillage systems (Table 2). Therefore, the higher organic carbon concentration
Table 1 Soil organic carbon content and pH in no tillage (NT) and conventional tillage (CT) in the 0–20 cm depth Organic carbon (g kg1)
pH
0–5 cm NT CT
34.06a 28.38b
5.6a 6.1b
5–10 cm NT CT
29.86a 27.72b
5.6a 5.8a
10–20 cm NT CT
28.38a 27.19a
5.8a 5.8a
Treatment
Means values followed by the same letter within the same depth are not significantly different ( p < 0.05) according to LSD test.
observed in NT could be attributed to the lower residues decomposition rate and stable fractions of soil organic matter (Paustian et al., 1997). The NT system caused a significant reduction in soil pH by 0.5 units in the upper 5 cm depth; but no significant differences in soil pH was detected in deeper depths between NT and CT practices (Table 1). The reduction in soil pH at the surface NT could be due to the combination of surface urea broadcast (Rothon, 2000) and the higher amount of organic carbon on mineralization results in additional production of organic acids (Stevenson and Cole, 1999). 3.2. Soil phosphorus fractionation 3.2.1. Labile phosphorus In the three soil depths, the labile Pi tended to increase in the soil under NT compared with CT, but none of the increase was statistically significant (Table 3). O’Halloran (1993) reported a higher concentration of labile Pi at the surface layer in NT compared with CT as result of the accumulation of P fertilizer and crop residues. The AEM-Pi represented a small fraction of the total P, on average, 7%; and because AEM-Pi is a source of P for plants and microorganisms in a short period of time (Cross and Schlesinger, 1995) it plays a significant role in crop production which is corroborated with the high and significant correlation between AEM-Pi and Bray 1-P (r = 0.99; p < 0.05) (data are not shown). In addition, the AEM-Pi was positively and significantly correlated with organic carbon (r = 0.79), and negatively correlated with soil pH (r = 0.49) (Fig. 2). It seems that the decreases in soil pH stimulated the development of positive charges (Barrow, 1984) and the
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Table 2 Annual carbon input to soil with crop residues in no tillage (NT) and conventional tillage (CT) Year
1992 1993 1994 1995 1996 1997 1998 1999
Crop
Harvest index (%)
Yield grain (Mg ha1)
Wheat Soybean Wheat Corn Corn Sunflower Corn Soybean
Residue (Mg ha1)
C added to soil (Mg ha1)
NT
CT
NT
CT
NT
CT
NT
CT
5.5 4.4 5.5 7.3 8.6 3.3 8.0 #
6.2 4.4 6.5 6.3 10.2 3.4 4.3 #
45 40 45 45 45 35 45 #
45 40 45 45 45 35 45 #
8.2 6.6 8.2 10.9 3.9 6.1 12 #
9.3 6.6 9.7 9.4 15.3 6.3 8.0 #
3.7 3.0 3.7 4.9 1.7 2.8 5.4 #
4.2 3.0 4.4 4.2 6.9 2.8 3.6 #
(#) Data no available. Based on the assumption that carbon content in residues was 45%. Harvest index was the ratio between grain yield and dried matter.
increases in organic carbon promoted P retention (Sanyal and de Datta, 1991) which could explain the trend to increase the AEM-Pi in NT, especially in the soil surface. In contrast to labile Pi fractions, the labile Po fraction such as NaHCO3-Po significantly decreased, at 0–5 cm depth, in NT compared with CT (Table 3). Under NT, the increase in AEM-Pi and NaHCO3-Pi was parallel with the decrease in NaHCO3-Po suggesting a linkage among these fractions and a potential contribution of mineralizable labile Po to labile Pi fraction. According to Bowman and Cole (1978), the Po extracted with NaHCO3 has been considered to be an active fraction of soil Po, because it represents compounds such as glycerophosphate and ribonucleic acid which are readily exchangeable from the soil. Significant differences in microbial P concentration were observed between tillage systems. Microbial P in NT was higher than CT at all sampling depths (Table 4)
probably due to more favorable soil conditions under NT. In fact, soil organic carbon content, which is an important source of energy for the heterotrophic microorganisms, was higher under NT comparing to CT. In addition, the decrease of microbial P concentration with increasing soil depth coincided with the decrease of soil organic matter. Aslam et al. (1999) and Daroub et al. (2000) found higher microbial P and organic matter content in the top layer of NT than in ploughed soils. The microbial P was closely related to AEM-Pi (r = 0.97) emphasizing on the importance of available P in controlling the microbial P (Fig. 2). Similarly, Chauhan et al. (1981) observed a positive relationship between concentration of Pi in solution and P assimilation by microbial biomass. 3.2.2. Moderately labile phosphorus No significant changes in HCl-Pi occurred as a result of the different tillage systems. However the HCl-Pi
Table 3 Phosphorus concentration in inorganic (Pi) and organic (Po) fractions in no tillage (NT) and conventional tillage (CT), at three soil depths Treatment
Phosphorus fractions (mg kg1) Ultrasonic-NaOH
HCl
Pi
Po
Pi
Po
Pi
Po
Pi
52.46a 28.69a
36.52a 23.30a
43.00b 50.00a
50.07a 39.40a
202.07a 180.90a
10.35a 8.00a
23.34b 29.76a
5–10 cm depth NT 35.10a CT 23.09a
29.65a 19.72a
41.37a 48.24a
39.67a 35.64a
212.48a 166.06b
7.73a 7.69a
10–20 cm depth NT 12.75a CT 18.02a
15.59a 18.33a
41.24a 50.16a
22.46a 32.50a
188.45a 162.63b
6.26a 7.80a
AEM-Pi
0–5 cm depth NT CT
NaOH
NaHCO3
Residual (Pi, Po)
Total P (sum)
53.96a 45.13a
164.37a 153.41a
636.62a 558.62a
22.88a 28.71a
50.44a 44.77a
150.55a 145.37a
589.65a 519.28a
22.80b 28.33a
43.11a 42.44a
157.06a 163.64a
509.75a 523.84a
Means values followed by the same letter within the same depth are not significantly different ( p < 0.05) according to LSD test.
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Fig. 2. Relationships between anion-exchange membrane extractable P (AEM-Pi) and total organic carbon (a), pH (b), and microbial biomass P (c).
represented the highest concentration of Pi, accounting for 8% of the total P in both systems, followed by NaOH-Pi (Table 3). These values for HCl-Pi were expected since this soil was characterized by having a high bases saturation percentage with Ca2+ as a main exchangeable cation (Fabrizzi et al., 1998). The NT system had consistently higher fraction of NaOH-Po and NaOH-Pi than the CT system, where the increase was significant at 5–10 and 10–20 cm depths for NaOH-Po (Table 3). Cabria et al. (2005) reported that continuous agriculture under CT caused a reduction in macroaggregate mass and decrease in Fe concentration associated with organic compound. According to Schoenau et al. (1989) NaOH-Po and NaOH-Pi are associated with humic compounds and adsorbed to Al and Fe. Therefore, as the soil organic matter and Fe concentration reduced with CT, the soil capacity to retain P in form of NaOH-Po and NaOH-Pi diminished. The NaOH-Po and NaOH-Pi constituted Table 4 Size of soil microbial biomass phosphorus according to the Hedley and Stewart (1982) method in no tillage (NT) and conventional tillage (CT), at three soil depths Treatment
Microbial biomass P (mg P kg1)
0–5 cm depth NT CT
13.54a 3.88b
33.75a 9.75b
5–10 cm depth NT CT
14.50a 0.43b
36.25a 1.00b
10–20 cm depth NT CT
3.97a 0.10b
10.00a 0.25b
Means values followed by the same letter within the same depth are not significantly different ( p < 0.05) according to LSD test. Microbial biomass calculated from chloroform-released 0.5N NaHCO3-P (first column) and using a recovery factor of 0.4 (second column).
the majority of the total P in the surface and subsurface layers, where NaOH-Po and NaOH-Pi were almost 40% of total P. Physically protected P (ultrasonic NaOH-Pi and NaOH-Po) was not affected by tillage practices, with the exception of NT that showed a significant decrease in ultrasonic NaOH-Po at 0–5 and 10–20 cm depths (Table 3). In the three sampling depths and both tillage systems, the Po concentration exceeded by a factor of two or three the Pi concentration indicating that an important proportion of Po is sequestered within aggregates and can be susceptible to decomposition after physical disruption of aggregates. 3.2.3. Non-labile phosphorus Residual P was not affected by tillage systems, possibly because this fraction includes the chemically more stable and insoluble forms of P which changes over a long period of time (Cross and Schlesinger, 1995). The residual P fraction was the second largest fraction after NaOH-Po plus NaOH-Pi, and represented up to 31% of the total P (Table 3). Residual P was quantified without partitioning in residual-Po and Pi; however it can infer its composition by comparing the total Pi, determined according to Metha method, with the sum of Pi fractions extracted by the sequential procedure. The total Pi and the sum of AEM-Pi, NaHCO3-Pi, NaOH-Pi and HCl-Pi fractions, average of tillage systems and soil depths, were 157 and 143 mg P kg1, respectively. The sum of these four fractions accounted for about 91% of the total Pi. These values demonstrated that most of the total Pi was recovery in the labile and moderately labile Pi fractions while a small proportion was related to residual Pi, therefore residual P was considered entirely organic. This observation agrees with Tiessen et al. (1983) who reported that the residual P in Mollisols contains a large proportion of organically bound P.
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4. Conclusion In this study the tillage systems did not affect the total P content, however the distribution of inorganic and organic fractions changed between NT and CT management systems. No tillage system had significantly higher microbial P, and a trend to have higher AEM-Pi and NaHCO3-Pi comparing to CT system. The increase in AEM-Pi was closely related to organic carbon content and pH. The greater concentration of labile P in NT soil would lead to a greater availability of this nutrient for plants. Therefore more research is required to investigate the relationships between organic and inorganic P fractions and P plant uptake in these systems. The Po extracted with NaOH increased under NT and represented on average about 35% of total P. The residual P which was considered mostly organic was also an important pool in both NT and CT, and accounted for about 30% of total P. Therefore, P availability is mainly controlled by organic P which makes up a larger proportion of total P. Acknowledgments The authors acknowledge Facultad de Ciencias Agrarias (UNMdP) and EEA-INTA Balcarce for financial support. References Aslam, T., Choudhry, M.A., Saggar, S., 1999. Tillage impacts on soil microbial biomass C, N and P, earthworms and agronomy after two years of cropping following permanent pasture in New Zealand. Soil Till. Res. 51, 103–111. Barrow, N.J., 1984. Modeling effects of pH on phosphate sorption by soils. J. Soil Sci. 35, 283–297. Beare, M.H., Hendrix, P.F., Coleman, D.C., 1994. Water-stable aggregates and organic matter fractions in conventional and no tillage soils. Soil Sci. Am. J. 58, 787–795. Bowman, R.A., Cole, C.V., 1978. An exploratory method for fractionation of organic phosphorus from grassland soils. Soil Sci. 125, 95–101. Bray, R.H., Kurtz, L.T., 1945. Determination of total, organic, and available forms of phosphorus in soils. Soil Sci. 59, 39–45. Brookes, P.C., Powlson, D.S., Jenkinson, D.S., 1982. Measurement of microbial biomass phosphorus in soil. Soil Biol. Biochem. 14, 319–329. ´ xidos de Fe Cabria, F.N., Bianchini, M.R., Mediavilla, M.C., 2005. O libre asociados a carbono orga´nico en agregados de suelos del partido de Balcarce. Free iron oxides associated to organic carbon in soil aggregates in Balcarce county. Ciencia del Suelo. 23, 23– 29. Chauhan, B.S., Stewart, J.W.B., Paul, E.A., 1981. Effect of labile inorganic phosphate status and organic carbon additions on the microbial uptake of phosphorus in soils. Can. J. Soil Sci. 61, 373– 385.
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