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Published online 9 January 2007
Published in J Environ Qual 36:305-315 (2007)
DOI: 10.2134/jeq2006.0131
© 2007 American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America
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TECHNICAL REPORTS

Waste Management

Phosphorus Movement and Speciation in a Sandy Soil Profile after Long-Term Animal Manure Applications

G. F. Koopmansa,*, W. J. Chardonb and R. W. McDowellc

a Dep. of Soil Quality, Wageningen Univ., Wageningen Univ. and Research Centre (WUR), P.O. Box 8005, 6700 EC, Wageningen, the Netherlands
b Alterra, WUR, P.O. Box 47, 6700 AA, Wageningen, the Netherlands
c AgResearch, Invermay Agricultural Centre, Private Bag 50034, Mosgiel, New Zealand

* Corresponding author (gerwin.koopmans{at}wur.nl)

Received for publication April 5, 2006.

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Long-term application of phosphorus (P) with animal manure in amounts exceeding removal with crops leads to buildup of P in soil and to increasing risk of P loss to surface water and eutrophication. In most manures, the majority of P is held within inorganic forms, but in soil leachates organic P forms often dominate. We investigated the mobility of both inorganic and organic P in profile samples from a noncalcareous sandy soil treated for 11 yr with excessive amounts of pig slurry, poultry manure, or poultry manure mixed with litter. Solution 31P nuclear magnetic resonance spectroscopy was used to characterize NaOH-EDTA-extractable forms of P, corresponding to 64 to 93% of the total P concentration in soil. Orthophosphate and orthophosphate monoesters were the main P forms detected in the NaOH-EDTA extracts. A strong accumulation of orthophosphate monoesters was found in the upper layers of the manure-treated soils. For orthophosphate, however, increased concentrations were found down to the 40- to 50-cm soil layers, indicating a strong downward movement of this P form. This was ascribed to the strong retention of orthophosphate monoesters by the solid phase of the soil, preventing orthophosphate sorption and facilitating downward movement of orthophosphate. Alternatively, mineralization of organic P in the upper layers of the manure-treated soils may have generated orthophosphate, which could have contributed to the downward movement of the latter. Leaching of inorganic P should thus be considered for the assessment and the future management of the long-term risk of P loss from soils receiving large amounts of manure.

Abbreviations: {alpha}, molar ratio of P to the sum of Al and Fe extractable by acid ammonium oxalate • EDTA, ethylenediaminetetraacetic acid • MDP, methylenediphosphonic acid trisodium salt tetrahydrate • NMR, nuclear magnetic resonance • PM, poultry manure • PML, poultry manure mixed with litter • PS, pig slurry • Pw, water-extractable phosphorus


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
LONG-TERM APPLICATION OF PHOSPHORUS (P) with animal manure in amounts exceeding removal with crops leads to buildup of P in topsoil (Sharpley, 1996; Lehmann et al., 2005) and to increasing risk of P loss to ground and surface water when sorption capacity approaches P saturation (Novak et al., 2000; Schoumans and Groenendijk, 2000). Phosphorus is mainly present in inorganic forms in pig slurry (Gerritse, 1981) and in swine and cattle manures (Turner, 2004). However, in soil leachates, organic P was often found to dominate (e.g., Chardon et al., 1997; Toor et al., 2003; McDowell and Koopmans, 2006). Therefore, studying the mobility in the soil profile of organic forms of P present in animal manures is needed. Sequential fractionation methods are most often used for studying different pools of P in soil profiles (e.g., Condron et al., 1985; Hansen et al., 2004; Lehmann et al., 2005). However, these methods only give a rough indication of the presence of inorganic and organic P but not of specific P forms (McDowell and Stewart, 2005b). For this purpose, solution 31P nuclear magnetic resonance (NMR) spectroscopy can be used. In many 31P NMR studies, the NaOH-EDTA extraction procedure of Bowman and Moir (1993) has been employed allowing for the characterization of up to 96% of the total P concentration in soil (Cade-Menun and Preston, 1996; Koopmans et al., 2003; Turner et al., 2003c, 2004; McDowell et al., 2006). Hansen et al. (2004) applied 31P NMR to NaOH-EDTA extracts from soil samples taken from different depths of a heavily fertilized calcareous loamy fine sand. However, no such applications are known to exist on profile samples from noncalcareous soils. In the Netherlands, soil samples taken down to 50-cm depth were available from a long-term field experiment on a noncalcareous sandy soil to which excessive rates of different types of manure had been applied for 11 yr. The objective of our study was to take advantage of the unique opportunity to assess movement of P through the soil profile presented by these samples, via measurements of water-extractable P and P saturation, and characterization of P forms extracted by NaOH-EDTA with solution 31P NMR spectroscopy.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Field Experiment
In the present study, we used soil profile samples taken down to 50-cm depth of four fertilization regimes (control, pig slurry [PS], poultry manure [PM], and poultry manure mixed with litter [PML]) from a long-term field experiment (1970 through 1980) (van der Veen, 1985). After sampling, soil samples were dried at 40°C, sieved through a 2-mm sieve, and stored in closed cardboard boxes at constant temperature and humidity in TAGA (de Willigen et al., 2001). TAGA is an extensive archive for technical information and soil samples containing the data of about 20 000 field experiments performed in the period between 1879 and 1998 in the Netherlands, and about 250 000 soil samples from selected experiments (de Willigen et al., 2001). The setup of the field experiment was previously described by Koopmans et al. (2003). In short, grassland sites were located in a single field on a noncalcareous sandy soil (mesic Typic Haplorthod). The average annual rainfall during the experimental period was 733 ± 114 mm (± standard deviation), with on average 36% falling from November through February (i.e., the period outside the growing season). Each site exhibited a size of 2 by 2 m. The sites were separated by 5-cm-wide and 3-cm-deep trenches preventing horizontal transport of the applied manures between sites. The field experiment had a completely randomized design without replications. From 1970 onward, PM and PML were applied at a rate of 25 Mg ha–1 yr–1. Pig slurry was applied from 1971 onward at the same rate. From 1971 onward, the same amount of manures was split and applied at two occasions each year: at the start of the growing season (April or March) and 1 to 9 d after the second harvest of grass in June or July. In most growing seasons, four or five grass harvests were obtained, but in 1970 and 1971 only three harvests were obtained. The manures were applied on the soil surface without mechanical incorporation. For measuring the composition of the applied manures, fresh manure samples were taken before each field application and analyzed promptly after sampling. In March 1981, soil samples were taken from six layers (0- to 5-, 5- to 10-, 10- to 20-, 20- to 30-, 30- to 40-, and 40- to 50-cm layers). No tillage was applied during the field experiment. Irrigation was only applied at a few occasions in 1970 and 1976 (20 mm in 1970 and 85 mm in 1976).

Chemical Analyses
For the soil samples, we used the following results from van der Veen (1985): pH (KCl), organic matter (estimated from loss-on-ignition), Pw (water-extractable P at a soil/solution ratio of 1:60 [v/v]), and total Ca, N, and P concentrations. The method of Sissingh (1971) was used to determine Pw. In the Netherlands, Pw is used for P fertilizer recommendations for arable land. Normally, Pw is expressed in mg P2O5 L–1 of soil but in this study is expressed in mg P kg–1 of soil. For converting Pw, we calculated the density of the soil samples using organic matter. For the manure samples, the following results were taken from van der Veen (1985): pH (H2O), dry matter, organic matter, CaCO3, N, P, Cl, Ca, K, Mg, Na, and S. These results were averaged over the whole experimental period. Moreover, the dry matter yield of grass and the cumulative P balance were taken from van der Veen (1985). The cumulative P balance was calculated as the difference between P applied with manure and P removed with the harvested grass. For calculating the P balance, the P concentration of the grass and the dry matter yield of grass were determined. All analytical methods used are described in Vierveijzer et al. (1979). In the present study, we determined acid ammonium oxalate-extractable P, Al, and Fe in soil (Schwertmann, 1964). Phosphorus, Al, and Fe were measured by inductively coupled plasma–atomic emission spectroscopy (ICP–AES). Based on these results, the degree of P saturation of a soil with respect to its content of amorphous Al and Fe oxides (van der Zee and van Riemsdijk, 1988) can be calculated:

Formula 1[1]
where Pox and [Al+Fe]ox are expressed in mmol kg–1. This parameter {alpha} was developed for noncalcareous sandy soils where sorption of orthophosphate is dominated by metal oxides (van der Zee and van Riemsdijk, 1988).

NaOH-EDTA Extracts
We used the 0.25 M NaOH-0.05 M Na2EDTA extraction method proposed by Cade-Menun and Preston (1996) to characterize P in soil by solution 31P NMR spectroscopy. This method was originally developed by Bowman and Moir (1993) as an extractant for total organic soil P. The alkaline extractant NaOH solubilizes organic matter and EDTA increases the effectiveness of organic P extraction by breaking P-containing Al and Fe complexes from soil. For most soil samples, duplicate 2.5-g portions of each soil were suspended in 50 mL of NaOH-EDTA in a centrifuge tube and shaken reciprocatively for 16 h at 85 strokes min–1 and 20°C. The suspensions were centrifuged at 2100 x g for 10 min and combined before filtration through a Schleicher & Schuell (Dassel, Germany) 589/5 filter (pore size 2 to 4 µm). An aliquot of 80 mL of the filtrate was frozen and freeze-dried. The freeze-dried material was stored at 4°C until analysis by 31P NMR. Before analysis, the freeze-dried extract was redissolved in 2 mL of 1 M NaOH and 0.2 mL of D2O (for signal lock), vortexed for 2 min, and transferred to a NMR tube. The addition of NaOH ensured a solution pH > 12 and comparative chemical shifts (Turner et al., 2003c; McDowell and Stewart, 2005a). The remaining filtrate was used to determine the concentrations of Fe, Mn, and P by ICP–AES. However, for the soil samples taken from the two upper layers (0- to 5- and 5- to 10-cm layers) of the PM and PML treatments, 3 g of soil were suspended in 60 mL of NaOH-EDTA. The same shaking, filtration, and ICP–AES analysis procedures were used as for soil samples from other layers. However, for freeze-drying, a smaller aliquot (30 mL) was used to prevent precipitation of inorganic P in the redissolved NaOH-EDTA extracts. Precipitation was thought possible due to abundant inorganic P in NaOH-EDTA extracts of the top 5 cm of the PM and PML treatments (Koopmans et al., 2003). The freeze-dried material was redissolved in 4 mL of 1 M NaOH and 0.4 mL of D2O.

The 31P NMR spectra were obtained on a Bruker (Rheinstetten, Germany) DPX 300 spectrometer, operating at 121.49 MHz and room temperature. Conditions used for 31P NMR analysis were a pulse angle of 90°, a pulse delay of 1 s, and an acquisition time of 0.82 s. This exceeded the spin-lattice relaxation time (T1) of most spectra as estimated from the ratio of P to the paramagnetic cations Fe and Mn (McDowell et al., 2006). For each sample, 1024 scans were accumulated which was sufficient to obtain good recognizable signals with a signal/noise ratio of the orthophosphate peak commonly >50. Chemical shifts ({delta}) of the peaks were measured according to 0.98 mM methylenediphosphonic acid trisodium salt tetrahydrate (MDP; 98%) standard, contained in a capillary tube measured simultaneously with each sample. In most other 31P NMR studies, orthophosphoric acid is used as an external standard. For comparison of our results with these studies, MDP was set at {delta} = 18.1 ppm. Peaks representing different P forms within 31P NMR spectra were integrated using Mestre-C software (Gómez and López, 2004) and made quantitative using the peak assignments of Cade-Menun and Preston (1996) and McDowell and Stewart (2005a), the percentage spectral area occupied by each P form, and the total P concentration in the corresponding NaOH-EDTA extract. Within the 31P NMR spectra, the orthophosphate peak was separated from the orthophosphate monoesters peaks using deconvolution.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS
 REFERENCES
 
Soils
In the present study, we used archived soil samples for the characterization of P forms extracted by NaOH-EDTA with solution 31P NMR spectroscopy. However, storage of dried soil samples is known to have an effect on the speciation of soil-extractable P (e.g., Turner, 2005). Nevertheless, chemical analysis of soil samples after finishing a long-term field experiment without having to store soil samples in an archive is in most cases impossible. Moreover, we used dried soil samples whereas drying has been shown to have an effect on the release of P to soil water extracts (e.g., Turner and Haygarth, 2001; Turner et al., 2003a; Koopmans et al., 2006), and on the extraction of P from marine sediments by 0.25 M NaOH-0.05 M Na2EDTA (Cade-Menun et al., 2005). In addition, drying of marine sediments induced changes in the speciation of P in NaOH-EDTA extracts (Cade-Menun et al., 2005). However, these effects were relatively small (<10%) compared to differences between P forms observed among sediment samples from different locations. Drying of fresh soil samples is common practice for most routine soil analyses and in most 31P NMR studies, because storage of dried soil samples is less complicated and subsampling is much easier.

Table 1 shows the cumulative P balance of the four fertilization regimes and selected characteristics of the soil samples from the field experiment after 11 yr of treatment. Comparison of pH at each depth of the control soil and manure-treated soils indicated a clear pH increase resulting from long-term manure application. In the top 5 cm of the manure-treated soils, pH increased by 1.5 to 2.6 units and remained higher than in the control treatment down to the 40- to 50-cm soil layer. A clear pH increase has been found before in the field experiments of Mugiwra (1976) and Kingery et al. (1994) after application of 22 to 267 Mg dairy cattle manure ha–1 yr–1 and 6 to 22 Mg broiler litter ha–1 yr–1, respectively. The presence of CaCO3 in the applied manures (Table 2) can raise the pH of naturally acidic soils due to the consumption of protons by CaCO3 dissolution. In general, a higher pH has the effect of decreasing sorption strength of P in noncalcareous sandy soils, increasing the potential for P desorption and favoring the microbial degradation of organic P (Beek and van Riemsdijk, 1982). Organic matter and total concentrations of Ca and N were clearly increased in the upper layers of the manure-treated soils (Table 1), which was also found by Mugiwra (1976) and Kingery et al. (1994). Our results can be explained by the abundant presence of organic matter, Ca, and N in the applied manures (Table 2). However, buildup of plant residues resulting from the greater dry matter yield of grass (Table 1) may have contributed to the elevated organic matter concentration in the upper layers of the manure-treated soils. Long-term manure application caused the C/N ratio in the upper soil layers to decrease (Table 1) due to the relatively low C/N ratio of the manures (Table 2) in comparison with the C/N ratio of the control soil (Table 1). A higher pH and an increased mineralization of organic matter as stimulated by the addition of fresh organic C may have contributed to the lowering of the C/N ratio. Although our results are based on manures which were applied in a field experiment dating from more than 25 yr ago and animal diets have changed during this period (Jongbloed and Lenis, 1998; Maguire et al., 2005), the general composition of the applied manures (Table 2) is reasonably comparable with more recent data on manure composition (Mooij, 1996).


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  		Table 1. Cumulative P balance, average annual dry matter yield of the grass, and selected characteristics of the soils from the field experiment.

 

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  		Table 2. Average composition of the manures over the whole experimental period of 11 yr.{dagger}

 
Depth distribution of Pox, the total P concentration (Table 1), and Pw (Fig. 1) indicated both a very clear accumulation and downward movement of P through the soil profiles of the manure treatments. Increase of soil-extractable P in the soil profile following the long-term application of animal manures in the field has been reported many times before (e.g., Mugiwra, 1976; Lehmann et al., 2005; Nelson et al., 2005). Obviously, downward movement of P in our soils is the result of the positive P balances (Table 1), varying from 100 kg P ha–1 yr–1 for the PS treatment to 322 kg P ha–1 yr–1 for the PM treatment. On arable fields with maize in the middle, east, and south of the Netherlands where intensive livestock systems on noncalcareous sandy soils dominate, the P surplus varied from 48 to 108 kg P ha–1 yr–1 in the period between 1950 and 1990 (Reijerink and Breeuwsma, 1992). Locally, however, the P surplus may have been >300 kg P ha–1 yr–1 (van Eekeren and Iepema, 2004). In some areas of the USA, excessive P application rates for different types of animal manure as high as 310 kg P ha–1 yr–1 (Lehmann et al., 2005) or 806 kg P ha–1 yr–1 (Sharpley, 1996) have been reported. In our field experiment, long-term manure application caused the total P concentration in the top 5 cm to increase 2.8 to 5.5 times (Table 1). The total P concentration decreased with depth in all treatments but remained higher than in the control treatment down to the 30- to 40-cm layer of the PS-treated soil, the 20- to 30-cm layer of the PM-treated soil, and the 40- to 50-cm layer of the PML-treated soil. The Pw in the top 5 cm of the manure-treated soils increased 7.5 to 13.6 times (Fig. 1) so the relative increase of Pw was much greater than the increase of the total P concentration. With depth, Pw decreased but remained higher than in the control treatment down to the 40- to 50-cm layer of the manure-treated soils. Compared to the control, the sum of oxalate-extractable Al and Fe showed only a small increase in the top 5 cm of the manure-treated soils. Long-term manure application caused Pox in the top 5 cm to increase 3.1 to 5.4 times (Table 1). Oxalate-extractable P decreased with depth but remained higher than in the control treatment down to the 30- to 40-cm layer of the PS-treated soil, the 20- to 30-cm layer of the PM-treated soil, and the 40- to 50-cm layer of the PML-treated soil. In the PML-treated soil, clearly more P moved to lower depths than in the other treatments (Table 1 and Fig. 1). This can easily be explained by the greater P surplus of the PML treatment (Table 1). Moreover, the litter mixed with the poultry manure caused an increase in the organic matter concentration of PML (Table 2). This may have contributed to the increased downward movement of P via the formation of dissolved organic P species or colloids containing orthophosphate associated with dissolved organic carbon via cation bridges (Gerke, 1992; Dolfing et al., 1999; Ilg et al., 2005). Also, dissolved organic anion concentrations in PML may have been higher than in the other manures, causing displacement of orthophosphate bound to the soil solid phase further increasing downward P movement (Geelhoed et al., 1998).


Figure 1
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  		Fig. 1. Concentration of water-extractable P at a soil/solution ratio of 1:60 (v/v) (Pw) with depth in the soil profiles of the control, pig slurry, poultry manure, and poultry manure mixed with litter treatments.

 
The increase in Pox caused the molar ratio of Pox/[Al+Fe]ox (i.e., {alpha}) in the profiles of our manure-treated soils to increase. As the solid phase of the soil becomes increasingly saturated with P, any additional soluble P applied via manure remains as readily soluble P in soil causing a large increase in Pw and risk of downward movement of P (Koopmans et al., 2003; Ilg et al., 2005; Nelson et al., 2005). In the 0- to 5- and 5- to 10-cm layers of the soils treated with PM and PML, {alpha} is, however, much higher than expected based on the theoretical maximum (Table 1). Values of {alpha} in these soil layers varied from 0.76 to 1.00, whereas {alpha}max values of 0.4 to 0.6 have been found in several P sorption studies (van der Zee and van Riemsdijk, 1988; van der Zee et al., 1988; Freese et al., 1992; Maguire et al., 2001). Plotting {alpha} against Pw leads to the construction of a desorption isotherm (Fig. 2), because Pox is often considered as an estimate for the total pool of sorbed inorganic P (van der Zee and van Riemsdijk, 1988; Koopmans et al., 2004, 2006) and Pw represents the readily soluble P pool in soil (Schoumans and Groenendijk, 2000). Since the soil samples taken from the 0- to 5- and 5- to 10-cm soil layers of the PM and PML treatments had {alpha} values far above the theoretical maximum, they were not included in the calculation of the isotherm. The isotherm could be described reasonably well with the Langmuir equation (R2adj = 79.1%***). The estimated {alpha}max is 0.50 ± 0.04 (± standard error), and is in very good agreement with the range found for {alpha}max in the aforementioned P sorption studies. The data points representing the soil samples taken from the 0- to 5- and 5- to 10-cm layers of the PM and PML treatments clearly lie above the desorption isotherm. This can be explained by dissolution of Ca-P precipitates in the acid ammonium oxalate, leading to overestimation of the total pool of sorbed inorganic P. These Ca-P minerals possibly control the P concentration in the Pw extracts at a constant concentration. This idea agrees with the elevated pH levels and molar Ca/P ratios varying from 1.3 to 1.9 in the PM- and PML-treated soils (Table 1), supporting the presence of Ca-P precipitates. For example, at a Ca/P ratio of 1.3, P may reside in soil within octacalcium phosphate, at a Ca/P ratio of 1.5, tricalcium phosphate may be present, and at a Ca/P ratio of 1.7 and above, hydroxyapatite (HA) may be the stable phase. These Ca-P minerals may have been added to the PM- and PML-treated soils with the manures or they may have formed in soil after manure application. In PM and PML, the Ca/P ratios were 2.1 and 1.4, respectively, possibly facilitating precipitation of Ca/P minerals (Table 2). Using near-edge X-ray spectroscopy (XANES), Toor et al. (2005) identified dicalcium phosphate (DCP) in broiler litter and turkey manure at a Ca/P ratio less than 2.0 whereas both DCP and HA were present at a Ca/P ratio greater than 2.0. In acidic to neutral soils enriched with Ca and P, Ca-P minerals may exist as metastable solid phases. Based on the soil solution composition of noncalcareous sandy soils treated with large amounts of pig manure, de Haan and van Riemsdijk (1986) found indications for the existence of brushite. Obviously, this information does not provide conclusive evidence for the presence of specific Ca-P minerals in our manure-treated soils. Solution 31P NMR spectroscopy can, however, not be used for this purpose, because P associated with different minerals dissolved in NaOH-EDTA appears as one orthophosphate peak within 31P NMR spectra. For the identification of Ca-P precipitates in soil, mineralogical techniques such as XANES and solid-state 31P NMR spectroscopy should be used, because the application of these techniques has generated direct evidence for the presence of Ca-P minerals in heavily manured soils (e.g., Lookman et al., 1997; McDowell et al., 2002; Beauchemin et al., 2003; Sato et al., 2005).


Figure 2
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  		Fig. 2. The molar ratio of Pox/[Al+Fe]ox (i.e., {alpha} plotted against Pw of the soil samples taken from various depths of the control, pig slurry, poultry manure, and poultry manure mixed with litter treatments. The data points represented by the filled symbols (i.e., the samples from the 0- to 5- and 5- to 10-cm soil layers of the poultry manure and poultry manure mixed with litter treatments) were not included in calculating the Langmuir equation, because {alpha} of these soil samples exceeded the theoretical maximum of 0.4 to 0.6.

 
Characterization of Phosphorus Extracted with NaOH-EDTA
Total P in the NaOH–EDTA extracts represented 64 to 93% of the total P concentration in soil (Table 3). This range compares well with those extracted in other studies where 0.25 M NaOH-0.05 M Na2EDTA was used as an extractant; 45 to 96% of total P was recovered by Cade-Menun and Preston (1996), Turner et al. (2003c, 2004), and McDowell et al. (2006). However, lower percentages of the total P concentration (12 to 45%) were found by Turner et al. (2003b) and Hansen et al. (2004) in calcareous soils with a high pH. This may be attributed to poor dissolution of Ca-P minerals in these soils by NaOH-EDTA (McDowell et al., 2006). Figure 3 shows 31P NMR spectra obtained from soil profile samples of two contrasting fertilization regimes: the control and the PML treatments. In Table 3, data are presented on the concentrations and the relative proportions of different P forms detected by 31P NMR in the redissolved NaOH-EDTA extracts. Investigation of the P speciation by 31P NMR revealed the presence of four functional classes of P: orthophosphate, orthophosphate monoesters, orthophosphate diesters, and pyrophosphate. Trace amounts of phosphonate were detected in only two soils. However, signals from other phosphonate forms occurring in the region where our MDP standard resonates may have been obscured by the large MDP peak, resulting in an uncertain analysis of phosphonate. Since phosphonate typically represents a very small percentage of the total P concentration in soil (Tate and Newman, 1982; Turner et al., 2003b, 2003c, 2004; McDowell and Stewart, 2006), this may not affect the outcome of our study. Aromatic orthophosphate diesters and polyphosphates were not detected in any soil. Orthophosphate was the dominant P form in the top 5 cm of the manure-treated soils, constituting between 68 and 76% of total P extracted by NaOH-EDTA. Long-term field experiments generally indicate a tendency for heavily manured soils to contain a higher percentage of inorganic P rather than organic P (e.g., Sharpley et al., 1984; Lehmann et al., 2005), reflecting the abundant presence of inorganic P in the applied manures. In animal manures, inorganic P has been found to vary from 75 to 95% of total P (Gerritse, 1981; Dou et al., 2000; Sharpley and Moyer, 2000; McDowell and Stewart, 2005b). With depth, the relative importance of orthophosphate in the soil profiles of the manure treatments clearly decreased. Orthophosphate monoesters were the main organic P form in all soils. This agrees well with the results of many other studies where P speciation has been determined by 31P NMR in alkaline extracts from various soil types with a different land use and under varying climates (Tate and Newman, 1982; Condron et al., 1985, 1990; Turner et al., 2003b, 2003c, 2004; Lehmann et al., 2005; McDowell and Stewart, 2006). In the top 5 cm of the control soil, the relative importance of orthophosphate monoesters was, however, much greater (54% of total P) than in the manure-treated soils (24 to 32% of total P). In nonagricultural soils without P input, organic P tends to be more important (e.g., Condron et al., 1990; Cade-Menun and Preston, 1996; Turner et al., 2004). In the soil profiles of the manure treatments, the relative importance of orthophosphate monoesters increased with depth. Orthophosphate monoesters in soil consist mainly of inositol phosphates, at times >50% of total organic P in soil (Anderson, 1967). The dominant form of inositol phosphates in soil is myo-inositol hexakisphosphate (IHP), an inositol with six P anion groups (Harrison, 1987). Inositol phosphates are stabilized in soil via strong sorption reactions with Al and Fe oxides (Ognalaga et al., 1994) and as a result, they are physically protected against microbial attack and degradation (Turner et al., 2003b, 2003c). The orthophosphate monoesters found in our soil samples may originate from the applied manures because IHP is the dominant organic P form in most cereal grains fed to animals. Since monogastric animals (e.g., pig and poultry) have a limited ability to digest IHP (Taylor, 1965), high concentrations of this P form can be found in manures (Leinweber et al., 1997; Turner, 2004; Toor et al., 2005). Alternatively, orthophosphate monoesters may have been released by plant and microbial residues in soil (Anderson, 1967). The greater dry matter yield of grass (Table 1) and possibly an increased microbial biomass may have lead to buildup of plant and microbial residues in the upper soil layers of the manure treatments, contributing to enrichment of these soils with orthophosphate monoesters (McDowell and Stewart, 2006). On the other hand, orthophosphate diesters were detected in only 6 of the 24 soil samples, representing up to 1.2% of total P extracted by NaOH-EDTA. Signals for orthophosphate diesters include those assigned to deoxyribonucleic acid (DNA) (McDowell and Stewart, 2005a). The majority of the soil samples with orthophosphate diesters were taken from the control treatment. While orthophosphate diesters have been found in pig and poultry manures (Leinweber et al., 1997; Turner, 2004), this P form was almost completely absent in the soil samples from the manure treatments. Although orthophosphate diesters such as DNA can bind to clays (Greaves and Wilson, 1969; Poly et al., 2000), they can be rapidly degraded after addition to soil (Romanowski et al., 1992). For this reason, orthophosphate diesters represent only a small percentage of the total P concentration in most soils (Tate and Newman, 1982; Condron et al., 1985, 1990; Turner et al., 2003b, 2003c, 2004; McDowell and Stewart, 2006). Microbial degradation of orthophosphate diesters can explain the absence of this P form in the soil samples from the manure treatments (Turner et al., 2003b, 2003c). This may be the result of a greater microbial activity in our manure-treated soils than in the control soil due to the increased pH and the presence of fresh organic C (Beek and van Riemsdijk, 1982) (Table 1). Degradation of orthophosphate diesters susceptible to alkaline hydrolysis (e.g., phospholipids and ribonucleic acid) during extraction by NaOH-EDTA and 31P NMR analysis may be an alternative explanation for the absence of this P form in the manure-treated soils (Leinweber et al., 1997; Turner et al., 2003d). However, degradation of orthophosphate diesters is an unavoidable limitation to the use of alkaline solutions for the extraction of organic P from soil. Pyrophosphate was detected in only 9 soil samples, constituting up to 1.5% of total P. The majority of these samples were taken from the manure treatments. Pyrophosphate has been found in pig and poultry manures (Leinweber et al., 1997; Turner, 2004), and can accumulate in soil because of its reaction with metal oxides (Turner et al., 2003b, 2003c). Pyrophosphate is a short-chain polyphosphate (n = 2) and is known to be a microbial storage product appearing from microbial activity (Ghonsikar and Miller, 1973). This P form is thus indicative of an increased microbial activity and supports the idea of a greater degradation rate of orthophosphate diesters in the manure-treated soils. Hence, the presence of pyrophosphate in our soils may reflect both the input of pyrophosphate via manure application in combination with the soil potential to stabilize this P form and an increased microbial activity (Turner et al., 2003c).


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  		Table 3. Total P extracted by NaOH-EDTA from the soil samples of the field experiment and P forms as measured by solution 31P NMR spectroscopy in the redissolved NaOH-EDTA extracts.

 

Figure 3
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  		Fig. 3. Solution 31P NMR spectra of the redissolved NaOH-EDTA extracts obtained from the soil profile samples of the (A) control treatment and of the (B) poultry manure mixed with litter treatment. S/N denotes the signal/noise ratio.

 
In Fig. 4A and 4B, the depth distribution is presented for orthophosphate and orthophosphate monoesters as detected by 31P NMR in the redissolved NaOH-EDTA extracts. Long-term manure application caused the orthophosphate concentration in the top 5 cm to increase 4.5 to 10.6 times. With depth, the orthophosphate concentration decreased but remained higher than in the control treatment down to the 30- to 40-cm layer of the PM-treated soil and the 40- to 50-cm layers of the PS- and PML-treated soils. Concentration of orthophosphate monoesters increased 1.7 to 2.9 times in the top 5 cm of the manure-treated soils and decreased with depth. In contrast to orthophosphate, however, concentration of orthophosphate monoesters remained higher than in the control treatment only down to the 30- to 40-cm layer of the PS-treated soil and the 10- to 20-cm layers of the PM- and PML-treated soils. Apparently, orthophosphate monoesters were subject to accumulation in the upper layers of the manure-treated soils, and downward movement of this P form was limited in comparison with orthophosphate. In Fig. 5, the relationship between concentrations of organic P and organic C is presented. For most of the soil samples from our field experiment, a reasonably good linear relationship was observed (R2adj = 79.0%***). However, the data points representing the soil samples taken from the 0- to 5- and 5- to 10-cm layers of the PM and PML treatments clearly lie above this relationship, suggesting the presence of orthophosphate monoesters such as IHP exhibiting a high P/C ratio.


Figure 4
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  		Fig. 4. Concentrations of (A) orthophosphate and (B) orthophosphate monoesters extracted by NaOH-EDTA with depth in the soil profiles of the control, pig slurry, poultry manure, and poultry manure mixed with litter treatments.

 

Figure 5
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  		Fig. 5. Concentrations of organic P plotted against those of organic C of the soil samples taken from various depths of the control, pig slurry, poultry manure, and poultry manure mixed with litter treatments. The data points represented by the filled symbols (i.e., the samples from the 0- to 5- and 5- to 10-cm soil layers of the poultry manure and poultry manure mixed with litter treatments) were not included in the linear regression analysis. Organic C was calculated as 0.5 x organic matter (Table 1).

 
Differences in mobility between orthophosphate and orthophosphate monoesters may be due to strong competition effects between these P forms for sorption to Al and Fe oxides. Leytem et al. (2002) studied sorption of orthophosphate and orthophosphate monoesters such as IHP, adenosine 5' monophosphate (AMP), adenosine 5' diphosphate (ADP), and adenosine 5' triphosphate (ATP) to different types of soil. In general, IHP had the greatest sorption, followed by ATP, ADP and AMP, and orthophosphate. Sorption seemed to increase with a greater number of P anion groups on the organic molecule. A greater number of P anion groups and an increased negative charge density enhance the affinity of organic P forms for sorption to metal oxides (Nowack and Stone, 1999). The P anion groups of orthophosphate monoesters are thought to react with metal oxides via the same reaction mechanism as proposed for orthophosphate (Ognalaga et al., 1994): a ligand exchange reaction between P anions and OH– or H2O groups at surface sites of Al and Fe oxides (Hiemstra and van Riemsdijk, 1996). Analogous to orthophosphate, the degree of saturation of metal oxides by orthophosphate monoesters in the 0- to 5- and 5- to 10-cm layers of our manure-treated soils can be estimated as the molar ratio of orthophosphate monoesters, extracted by NaOH-EDTA (Table 3), to [Al+Fe]ox (Table 1). For the control treatment, this ratio is 0.10 and 0.09 in the 0- to 5- and 5- to 10-cm soil layers, respectively, but 0.16 and 0.12 for the PS treatment, 0.25 and 0.23 for the PM treatment, and 0.27 and 0.20 for the PML treatment. Below the upper layers of the manure-treated soils, this ratio sharply decreases with depth. Hence, the presence of orthophosphate monoesters may have caused a drastic reduction of the capacity of the upper layers of our manure-treated soils to bind orthophosphate, because the estimated P sorption maximum is 0.50 ± 0.04 (Fig. 2). In other words, orthophosphate may be out-competed by orthophosphate monoesters for sorption to Al and Fe oxides in the upper layers of our manure-treated soils, resulting in a greater mobility of orthophosphate in the soil profile. This idea has been proposed before by Leytem et al. (2002), and is supported by results obtained in competition experiments performed by Anderson et al. (1974) who demonstrated the strong preference in sorption of IHP over orthophosphate to six acidic soils. However, not all P anion groups of orthophosphate monoesters are necessarily involved in the formation of the bonding between this P form and metal oxides. For example, sorption of IHP on goethite was suggested to occur through four of the six P anion groups with the remaining two groups being free (Ognalaga et al., 1994; Celi et al., 1999). Hence, we possibly overestimated the saturation degree of Al and Fe oxides with orthophosphate monoesters. Other explanations for the increased mobility of orthophosphate in the soil profiles of the manure treatments include the formation of colloids containing orthophosphate associated with dissolved organic carbon via Al and Fe cation bridges (Gerke, 1992; Dolfing et al., 1999; Ilg et al., 2005) and displacement of orthophosphate bound to metal oxides in soil by dissolved organic anions (Geelhoed et al., 1998). Alternatively, mineralization of organic P in the upper soil layers of the manure treatments may have generated orthophosphate, which may have moved down the soil profile, as opposed to preferential sorption of orthophosphate monoesters over orthophosphate.

Our results are in good agreement with results obtained in the study by Lehmann et al. (2005) where the total P concentration in leachates obtained from soils with excessive application rates of poultry manure for >25 yr was dominated by inorganic P. In addition, using 31P NMR, Hansen et al. (2004) found an accumulation of IHP in the upper layer (0- to 10-cm layer) of soils receiving large amounts of animal manure, whereas orthophosphate and orthophosphate monoesters other than IHP were present in elevated concentrations in a deeper soil layer (45- to 65-cm layer). However, their study was conducted on calcareous soils with a pH varying from 7.3 to 8.1. In these calcareous soils, the mechanism of orthophosphate monoester retention in the upper layer of manure-treated soils may be different than in our naturally acidic soils. As we know from food chemistry, IHP can form poorly soluble precipitates with Ca (Graf, 1983), and this may have caused an accumulation of IHP in the upper soil layer in the study by Hansen et al. (2004). Indeed, the reaction of IHP with calcite has been found to involve, besides a sorption reaction, precipitation with Ca on the calcite surface (Celi et al., 2000). Considering the enriched concentrations of total Ca and orthophosphate monoesters and increased pH in the upper layers of our manure-treated soils (Table 1 and 3), precipitation of Ca-IHP compounds in our field experiment may have occurred.

Since orthophosphate monoesters accumulated in the upper layers of our animal manure-treated soils, they increased the risk of leaching to a lesser extent than orthophosphate. Nevertheless, the presence of orthophosphate monoesters in water extracts, soil solution, overland flow, and leachate from grassland soils does occur (Espinosa et al., 1999; Koopmans et al., 2003; Toor et al., 2003; McDowell and Stewart, 2005a). Formation of mobile colloidal associations between orthophosphate monoesters such as IHP and metal oxides may explain these results (Hens and Merckx, 2001), whereas solubilization of Ca-IHP precipitates under specific environmental conditions can be another explanation. For example, in periods of (excessive) rainfall, the Ca concentration in soil solution decreases, resulting in dissolution of Ca-IHP precipitates. However, the aspect of mobilization of orthophosphate monoesters requires further research. In our heavily manured soils, inorganic P may have formed the bulk of P transport via leaching. On the longer term, the inorganic P pool will form the largest risk of reaching ground or surface water via leaching because of its large size and the slow downward movement of the P saturation front (Bolt, 1982). Inorganic P leaching should thus be considered for assessment and future management of the long-term risk of P loss. This does not, however, exclude the possibility of significant organic P leaching to ground and surface water. On the short-term, organic P forms can form a more direct risk for eutrophication, since organic P has often been found to dominate the total P concentration in soil solution, especially deeper in the soil profile, and in leachate in lysimeter and field studies (e.g., Chardon et al., 1997; Toor et al., 2003; McDowell and Koopmans, 2006).


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
REFERENCES
 
Long-term application of a large P surplus via animal manure caused a strong accumulation and downward movement of P through the soil profile. Accumulation of orthophosphate monoesters was restricted to the upper layers for all manure-treated soils, whereas an increase in orthophosphate was found down to the 30- to 40-cm layer of the PM-treated soil and the 40- to 50-cm layers of the PS- and PML-treated soils. This may be ascribed to strong binding of orthophosphate monoesters to the solid phase of the soil, preventing orthophosphate sorption and facilitating downward movement of the latter. Alternatively, mineralization of organic P in the upper layers of the manure-treated soils may have generated orthophosphate, which may have moved down the soil profile. Leaching of inorganic P should be considered for the assessment and future management of the long-term risk of P loss from soils receiving large amounts of manure.


   ACKNOWLEDGMENTS
 
The authors thank L.C.N. de la Lande Cremer for initiating and supervising the field experiment, P.A.I. Ehlert for introducing us to the TAGA archive, and P. van der Meer and A.E. Frissen for collecting the 31P NMR data. We thank O. Oenema and E.J.M. Temminghoff for their comments on a previous version of our paper.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 




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