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ELSEVIER Geoderma 64 (1995) 197-214

GEODI::R~A

A literature review and evaluation of the Hedley fractionation: Applications to the biogeochemical

cycle of soil phosphorus in natural ecosystems

Anne Fernald Cross, William H. Schlesinger Departments of Botany and Geology Duke Universi~,. Durham NC 27708-0339 USA

Received 20 December 1993; accepted after revision 31 March 1994

Abstract

The Hedley fractionation recognizes plant-available forms (Resin Pi, Bicarb Pi, and Bicarb Po) and refractory forms (NaOH Pi, NaOH Po, Sonic Pi, Sonic Po, HC1 Pi, Residual P) of soil phosphorus. This updated survey of the recent literature shows that the sequential fractionation proposed by Hedley et al. can also be used to separate forms of organically bound soil phosphorus from the geochemically bound fractions. We consider that biological P includes all the extracted organic fractions (Bicarb Po, NaOH Po, Sonic Po) and geochemical P includes the remaining fractions (Resin Pi, Bicarb Pi, NaOH Pi, Sonic Pi, HC1 Pi) and the Po and Pi in the Residual fraction.

Data from the Hedley fractionation suggest that the contribution of geochemical versus biological processes to soil phosphorus availability varies with pedogenesis. The pool of primary phosphate declines and the NaOH and sonicated-NaOH phosphorus fractions increase as phosphorus becomes geochemically fixed to the iron and aluminum oxides in more highly weathered soils. The sum of organic-P fractions - - biological P - - is an increasing proportion of total available P as a function of soil development. Therefore, the Hedley fractionation provides a valuable index of the relative importance of biological processes to soil phosphorus content across a soil weathering gradient.

I. Introduction

Both geochemical and biological processes regulate the availability of phosphorus in soils. At the global scale and over the long term, geochemical processes link the movement and distribution of phosphorus between two large pools - - terrestrial soils and ocean sediments (Richey, 1983; Schlesinger, 1991; Ramirez and Rose, 1992). In most natural ecosystems, geochemical processes may also determine the long-term distribution of phosphorus in soils, but in the short-term, biological processes influence phosphorus distribution because most of the plant-available phosphorus is derived from soil organic matter (Ballard,

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198 A.F. Cross, W.H. Schlesinger / Geoderma 64 (1995) 197-214

1980; Wood et al., 1984; Smeck, 1985; Tate and Salcedo, 1988; Walbridge, 1991 ; Walbridge et al., 1991 ).

Walker and Syers (1976) suggest that the proportion of total phosphorus held in various forms changes as soils develop. The weathering of primary minerals supplies phosphate to the plant-available pool in the soil. Bacteria, fungi, and higher plants incorporate phosphate into biomass, initiating the biological cycle. Decomposition and mineralization return inorganic phosphorus to the soil solution. In a mature, undisturbed forest, the Hubbard Brook Experimental Forest, in New Hampshire, USA, about 8 times as much phosphorus cycles in the intrasystem P cycle compared to the annual release of P from rock weathering (Schlesinger, 1991 ). Biological processes regulate the movement and distribution of labile forms of phosphorus, and organic P recycling is important to the availability of soil P ( Stewart and Tiessen, 1987).

The biological portion of the phosphorus cycle is controlled primarily by bacterial and fungal decomposition, immobilization, and mineralization, and secondarily via plant uptake (Wood et al., 1984; Jurinak et al., 1986; Walbridge, 1991; Bolan, 1991). Rates of plant litter decomposition depend on substrate quality (including C/P ratios), soil moisture, and temperature (McGill and Cole, 1981; Harrison, 1982b). Microbial immobilization and mineralization of phosphorus varies depending on phosphorus availability (Harrison, 1982a). Where soil phosphorus is limiting, microbes can immobilize between 20% and 50% of the organic phosphorus of surface soils (Srivastava and Singh, 1988; Walbridge, 1991 ). Using an isotope dilution technique, Walbridge and Vitousek (1987) found that phosphorus mineralization rates from phosphorus-rich forest soils were twice as high as those from phosphorus-deficient bog soils. Harrison (1982a) has shown that in phosphorus- deficient soils only a small fraction of the organic phosphorus pool, about 1% per year, is mineralized, supplying inorganic phosphorus for plant uptake. In most phosphorus-deficient ecosystems, plant phosphorus-use-efficiency and phosphorus resorption rates are high, creating a tight, conservative phosphorus cycle (Vitousek, 1984; Wood et al., 1984; Rich- ardson, 1985; Lajtha and Schlesinger, 1988; Walbridge, 1991 ; Walbridge et al., 1991 ; Yanai, 1992).

Over time, both biological and geochemical processes transform inorganic phosphorus into stable forms of organic and inorganic phosphorus in soil (Tiessen et al., 1984; Sharpley et al., 1987). Desert soils (Aridisols) typically have low soil organic matter and high pH, and the primary geochemical reservoir of phosphorus is calcium carbonate minerals (Lind- say, 1979; Lajtha and Bloomer, 1988). Soils that dominate humid temperate and tropical regions (Ultisols and Oxisols) are highly weathered, acidic, and dominated by large quan- tities of sesquioxides. These soils easily adsorb and geochemically fix phosphorus, in many cases leading to phosphorus limitations (Johnson and Cole, 1980; Sanchez et al., 1982; Sollins et al., 1988). Thus, the geochemical portion of the phosphorus cycle is controlled initially by soil parent material and subsequently by soil properties resulting from pedogenesis (Udo and Ogunwale, 1977; Day et al., 1987; Anderson, 1988; Roberts et al., 1989). Parent material and climate determine the overall weathering rate, and these factors influence the balance between phosphorus loss and retention (Gardner, 1990).

Walker and Syers (1976) suggest that the proportion of phosphorus in labile, non-labile, non-occluded, and occluded fractions should vary between soil taxa along a gradient of soil weathering intensity. In ecosystems with young, slightly weathered soils, most of the

A.F. Cross, W.H. Schlesinger / Geoderma 64 (1995) 197-214 199

0.5 g soil samples in 50 mL screw cap centrifuge tubes

Add 30 mL deionized water plus 0.4 g Dowex 1 x 8-50 anion exchange resin in bicarbonate form, shake 16 h, remove resin bag, centrifuge end discard supernatant

h~

Add 30 mL NaHCO3 (pH 8.5), shake 16 h, centrifuge collect supernatant

Soil

Soil

h= V

Add 30 mL 0.1M NeOH. shake 16 h, centrifuge, collect supernatant

I L .

Add 20 mL 0.1M NaOH and sonicate in an ice bath at 75 W (Braunsonic 1510) for 2 rain, make to 30 mL volume, shake 16 h, centrifuge and collect supernatant

Resin P (Pi)

Bicarbonate P (P, and Po)

Hydroxide P (P, and Po)

Sonicatelhydroxide P (Pi and Po)

Soil Add 30 mL 1.0M HCI, shake 16 h, centrifuge and collect supernatant

Acid P (P.) r

Residual Soil

Digest with 5 mL H2SO4 and H202 Residue P(total P only)

Fig. 1. Hedley sequential phosphorus fractionation method for soils (after Tiessen et al., 1984).

phosphorus should be found in primary minerals, such as hydroxyapatite. In ecosystems with a moderate weathering regime, most of the phosphorus should be found in organic compounds or adsorbed to secondary clay minerals. And, finally, in ecosystems with highly weathered soils, most of the phosphorus should be in the non-labile, occluded, or stable organic forms.

Despite the widespread acceptance of the Walker and Syers paradigm, it has seldom been tested with soils from natural ecosystems (Jenny, 1980; Birkeland, 1984; Schlesinger, 1991; Vitousek et al., 1993). Tiessen et al. (1984) and Sharpley et al. (1985) analyzed soil phosphorus extracts from cultivated and native soils to examine differences in soil phosphorus fractions among seven soil orders. Here, we re-examine their conclusions using recently published data on native soils. We confirm that the Hedley fractionation (Fig. 1 ) provides a general index of how biological and geochemical forms of phosphorus change during soil development in natural ecosystems.

2. Literature survey

We collected soil phosphorus values from the literature (Table 1 ), restricting our search to studies that use the sequential fractionation developed by Hedley et al. (1982a) for natural, unfertilized or uncultivated soils. We found 60 new studies of phosphorus fractionation to add to the 28 original values from native soils that Tiessen et al. (1984) compiled from Sharpley et al. (1985). We found data from 17 studies of nine soil orders from the

200 A.F. Cross, W.H. Schlesinger / Geoderma 64 (1995) 1 9 ~ 2 1 4

Table 1 Soil phosphorus values of the literature survey. Rows in italicized print were removed before calculation of the

percentage values (Figs. 3.4. and 5)

Soil Order Resin Bicarb Res + Bic NaOH Sonic N + S HC1

Mollisol 24.9 12.8 37.7 15.3 3.6 18.9 272

Mollisol 9 7 16 11 4.72 I 1 218

Mollisol 59.9 17.9 77.8 32.8 4.72 32.8 211.3

Mollisol 9. 6 I O. 53 20.13 96.33 96.33

Mollisol 15.93 12.53 28.46 144.93 144.93 -

Mollisol 5. 73 I. 93 7. 66 62.27 62.27 .-

Mollisol 10.33 6.33 16.66 92.33 92.33

Mollisol 20.27 10.69 30.96 11.82 3.38 15.2 209.44

Mollisol 19.38 9.69 29.08 19.38 4.56 23.94 156.75

Mollisol 33.64 18.07 51.71 38 8.72 46.72 127.09

Mollisol 20.29 13.2 33.49 15.5 3.44 18.94 190.57

Mollisol 25.08 15.18 40.26 23.1 5.94 29.04 168.96

Mollisol 20.94 16.05 36.99 26.52 6.28 32.8 157.05

Mollisol 8.43 11.24 19.67 11.24 1.68 12.92 192.77

Mollisol t7.12 14.58 31.7 16.48 4.44 20.92 t42.65

Mollisol 13.06 10.57 23.63 19.27 4.61 23.88 164.35

Mollisol 21 8 29 26 4.72 30.76 280

Mollisol 8 9 17 27 4.72 31.76 252

Mollisol 59 29 88 71 9 80 70

Mollisol 20 9 29 29 7 36 197

Mollisol 17 7 24 1 l 2 13 209

Mollisol 18 8 26 15 4 19 130

Mollisol 39 24 63 69 10 79 87

Mollisol 27 14 41 41 9 50 48

Mollisol 18 11 29 41 7 48 62

Mollisol 7 4 I l 12 3 15 63

Mollisol 5 3 8 6 I 7 200

Mollisol 24 14 38 42 8 50 58

Mollisol 9 11 20 30 9 39 58

Mollisol 22.4 7.8 30.2 17.6 4.2 21.8 166.2

Mollisol 16 5.8 21.8 12.9 2.8 15.7 168.8

Mollisol 17.3 6.3 23.6 13.7 3 16.7 166

Mollisol 12.7 4.6 17.3 12.1 3 15.1 172.9

Mollisol 15.3 5.3 20.6 12 2 14 ! 68.6

Mollisol 8 5.1 13.1 13.5 3.1 16.6 203.8 Mollisol 8.5 5.3 13.8 14.5 3.4 17.9 201.2

Mollisol 19.1 9.3 28.4 19.6 3.6 23.2 199.1

Mollisol 17.6 9.3 26.9 16.5 3.1 19.6 208.4 Mollisol 9.3 5.9 15.2 12.8 2.4 15.2 204.3

Mollisol 21 21 42 83 - 83 211

Mollisol 26 17 43 54 54 402

Mollisol 34 25 59 45 45 130

Aridisol 38.39 6.7 45.09 11.43 - 11.43 580.08

Aridisol 21 19 40 8 1 9 293 Aridisol 47 12 59 30 4 34 203 Aridisol 17 19 27 35 7 42 183 Aridisol 63 36 99 96 17 113 448 Aridisol 39 32 71 101 - 101 212

A.F. Cross, W.H. Sch les inger / G e o d e r m a 64 (1995) 1 9 7 - 2 1 4 201

Resid Total P BPo NPo SPo TPo Study

363 768 10.2 57.9 8.3 66.2 254 590.8 7.5 73 11.3 80.5 243.2 682.12 14.3 86.7 11.3 101 2 6 9 . 4 7 385 .93 5 .07 -

199 .87 373 .23 14.33 -

221 .2 291 .13 20 -

184.73 293 .72 16.27 -

255.6 563 7.88 38.85 5.07 51.8 370.18 670 16.53 67.26 6.27 90.06 226.77 623.35 33.02 120.6 17.44 171.06 253.71 574.2 7.46 61.99 8.04 77.49 276.54 660 21.12 110.88 13.2 145.2 270.15 697.32 37.69 144.49 18.15 200.33 256.27 562.56 5.06 65.19 10.68 80.93 295.44 633.36 11.41 117.29 13.95 142.65 339.46 763.28 27.65 167.42 16.89 211.96 273 688.18 11 53 11.3 75.42 341 752.18 15 57 11.3 83.42 341 668 10 72 7 89 200 534 13 50 9 72 238 574 14 67 9 90 193 488 31 78 11 120 260 707 68 141 9 218 262 642 68 156 17 241 171 310 - -

199 382 16 72 6 94 191 476 9 56 5 70 220 518 37 100 15 152

201 4 50 30 84

207.5 510.5 8.3 67.2 9.3 84.8 195.6 484.2 8 65.9 8.4 82.3 198.4 483.9 7.5 61.8 9.9 79.2 208.4 490.4 8.2 58.5 10 76.7 200.6 490.4 8.7 68.6 9.3 86.6 359.5 679.5 7 65.8 13.7 86.5 361.9 701.1 7.6 85.1 13.6 106.3 364.9 718 8.7 80.4 13.3 102.4 361 712.3 12.9 74.9 8.6 96.4 377.7 711.6 8 83.8 7.4 99.2

- 336 - - -

- 499 . . . .

- 234 . . . .

260 .4 8 9 7 . . . .

120 492 5 21 4 30 107 447 6 32 6 44 132 424 8 27 5 40 171 908 14 56 7 77 - 384 . . . .

Campbell et al. 1986 McKenzie et al. 1992a O'Halloran and DeJong 1987 Pare a n d Bern ier 1989

Pare a n d Bern ier 1989

Pare a n d Bern ie r 1989

Pare a n d Bern ie r 1989

Roberts et al. 1985 Roberts et al. 1985 Roberts et al. 1985 Roberts et al. 1985 Roberts et al. 1985 Roberts et al. 1985 Roberts et al. 1985 Roberts et al. 1985 Roberts et al. 1985 Schoenau et al. 1989 Schoenau et al. 1989 Sharpley et al. 1985 Sharpley et al. 1985 Sharpley et al. 1985 Sharpley et al. 1985 Sharpley et al. 1985 Sharpley et al. 1985 Sharp ley et al. 1985

Sharpley et al. 1985 Sharpley et al. 1985 Sharpley et al. 1985 T r a s a r - C e p e d a et al. 1990

Wager et al. 1986 Wager et al. 1986 Wager et al. 1986 Wager et al. 1986 Wager et al. 1986 Wager et al. 1986 Wager et al. 1986 Wager et al. 1986 Wager et al. 1986 Wager et al. 1986 Yang a n d J a c o b s e n 1990

Yang and J a c o b s e n 1990

Yang a n d J a c o b s e n 1 9 9 0

La j tha and Sch les inger 1988

Sharpley et al. 1985 Sharpley et al. 1985 Sharpley et al. 1985 Sharpley et al. 1985 Yang a n d J a c o b s e n 1990

202

Table I continued.

A.F. Cross, W.H. Schlesinger/ Geoderma 64 (1995) 197-214

Soil Order Resin Bicarb Res + Bic NaOH Sonic N + S HC1

Aridisol 13 14 27 46 46 198

Aridisol 5.21 3.09 8.3 8.99 3.22 12.21 61.02 Aridisol 7.07 7.82 14.89 6.29 3.58 9.87 166.4

Alfisol 58 56 114 155 7.45 155 240 Alfisol 11.69 7.16 18.85 13.95 3.77 17.72 125.92 Alfisol 14.2 13.1 27.3 25.48 5.46 30.94 144.14 Alfisol 27.55 21.54 49.09 44.59 8.52 53.1 l 181.86 Alfisol 6 6 12 20 7.45 27.5 52 Alfisol 5 5 10 19 7.45 26.5 35 Alfisol 9 12 21 57 7.45 64.5 86 Alfisol 20 17 37 65 14 79 75 Alfisol 9 8 17 56 13 69 47 Alfisol 11 5 16 16 4 20 6 Alfisol 9 3 12 6 2 8 23

Alfisol 8 17 25 36 9 45 102 Alfisol 12 17 29 14 2 16 10 Entisol 5 4 9 6 2 8 536 Entisol 13 5 18 7 2 9 372 Inceptisol 45 39 84 86 6.6 92.6 174 lnceptisol 14 13 27 24 6.6 30.6 193 lnceptisol 10 9 19 60 10 70 12

lnceptisol 5 9 14 66 lO 76 12 lnceptisol 3 7 10 91 9 1 O0 6

Spodosol 27.2 20.13 47.33 96.27 96.27 Spodosol 18. 53 15.33 33.86 30. 67 30. 67

Spodosol 28 20.47 48.47 58.13 -- 58.13 Spodosol 24.2 17.8 42 93.73 - 93.73

Spodos ol 26.73 l 9. 8 46. 53 41.53 41.53 Spodosol 11 7 18 13 3 16 2

Ultisol 1 3 4 29 9 38 2 Ultisol 6 6 12 37 8 45 4 Ultisol 2 1 3 6 2 8 3 Ultisol 27 25 52 75 13 88 17 Ultisol 4 3 7 24 7 31 7 Ultisol 37 17 54 62 10 72 14 Ultisol 9 5 14 18 5 23 3

Vertisol 10 9 19 22 2 24 342 Vertisol 17 7 24 14 5 19 65 Vertisol 32 42 74 59 - 59 430

Oxisol 5 4 9 83 17 100 3

United States, Spain, Canada, and several locations in South America. The largest set of Hedley fractionation data is for Mollisols, whereas data from other soil orders, especially the Spodosols and Oxisols, are limited to a few studies, and data for Histosols and Andisols are still entirely lacking.

With the Hedley fractionation, phosphate ions from the soil solution are removed by anion exchange resins and other forms of labile, non-labile, non-occluded, and occluded inorganic and organic phosphorus are removed sequentially with a series of successively

A.F. Cross. W.H. Sch les inger / G e o d e r m a 64 (1995) 1 9 7 - 2 1 4 203

Resid Total P BPo NPo SPo TPo Study

- 271 - - - Yang a n d J a c o b s e n 1990

32.91 114.44 - - Cross a n d Sch le s inger (unpubL )

46 .49 237 .65 - - - Cross a n d Sch les inger (unpubL )

169 820 33 100 13 133 McKenzie et al. 1992b 166.63 377 6.03 35.06 6.79 47.88 Roberts et al. 1985 141.23 400.03 9.46 38.95 8.01 56.42 Roberts et al. 1985 163.33 501 10.02 39.08 4.51 53 .61 Roberts et al. 1985 66 212.5 18 37 13 55 Schoenau et al. 1989

107 225.5 14 33 13 47 Schoenau et al. 1989 94 306.5 15 26 13 41 Schoenau et al. 1989

182 509 43 79 14 136 Sharpley et al. 1985 174 439 21 95 16 132 Sharpley et al. 1985 97 196 8 36 13 57 Sharpley et al. 1985

158 280 12 55 12 79 Sharpley et al. 1985 - 301 1 98 30 129 T r a s a r - C e p e d a et al. 1991

10 188 14 99 10 123 Sattell and Morris 1992 187 765 4 18 3 25 Sharpley et al. 1985 158 604 4 34 9 47 Sharpley et al. 1985 323 849.8 44 120 12.2 1 7 6 . 2 Schoenau et al. 1989 200 514.8 14 38 12.2 64.2 Schoenau et al. 1989

- 218 17 82 18 117 T r a s a r - C e p e d a et al. 1991

235 16 96 21 133 T r a s a r - C e p e d a et al. 1991


123 300 .13 33 .53 - - 33 .53 P a r e a n d Bern ie r 1989

76.33 151.13 10.27 - - 10 .27 Pare a n d Bern ie r 1989

101.4 2 2 9 . 2 7 21 .27 - - 21 .27 P a r e a n d Bern ier 1989

113.53 276 .93 27 .67 - - 2 Z 6 7 P a r e a n d Bern ier 1989

76.93 174.92 9.93 - - 9.93 P a r e a n d Bern ie r 1989


- 64 6 9 5 20 Lee et al. 1990

89 230 I 1 55 14 80 Sharpley et al. 1985 42 81 6 16 3 25 Sharpley et al. 1985 89 435 38 122 29 189 Sharpley et al. 1985

165 300 10 66 14 90 Sharpley et al. 1985 54 257 8 45 10 63 Sharpley et al. 1985


281 736 7 57 6 70 Sharpley et al. 1985 136 289 6 31 8 45 Sharpley et al. 1985

- 563 . . . . Yang a n d J a c o b s e n 1 9 9 0

165 429 27 108 17 152 Sharpley et al. 1985

stronger reagents. In general, labile phosphorus is thought to be available to microbial and vegetation communities in the short term, because it rapidly desorbs from the surface of soil particles. Non-labile P fractions are thought to be tightly bound to soil particles, and unavailable to plants. The non-occluded phosphorus, including phosphorus that is extracted with NaOH, is considered to be biologically available over an intermediate time scale, and the occluded phosphorus is thought to be available only on a long-term basis, if at all. However, the terminology that relates phosphorus found in soil extracts to plant availability has been interpreted in various ways in the literature (Table 2).


Table 2 Terminology of phosphorus compounds and extracts in the Hedley et al. (1982a,b), extraction

Ref? Resin Pi Bicarb Pi NaOH Pi Sonic Pi

[ 1 ] Non-occluded Pi Non-occluded Pi Non-occluded Pi Occluded Pi

[21 Form of soil Pi Extracts additional Partially dissolves Pi held at the from which plants Pi that is available Fe-AI phosphates internal surfaces normally draw to plants and desorbs Pi of soil aggre- their supply from the surfaces gates

of sesquioxides

[31

[41

Labile Pi adsorbed Labile Pi adsorbed Less labile Pi asso- Less labile Pi on surfaces of on surfaces of ciated with exteri- associated with crystalline com- crystalline com- ors of amorphous interiors of pounds pounds A1 and Fe phos- amorphous AI

phates and Fe phosphates

Soluble and Labile Labile Pi in Secondary mineral Secondary min- Pi: anion resin- or equilibrium with Pi: chemiabsorbed eral Pi: chemiab- water-extractable the soil solution: to surfaces of AI sorbed within A1

isotopically and Fe oxides and and Fe oxides extractable carbonates and carbonates

[ 5 ] Most plant availa- Readily plant Of lesser plant Aggregated-pro- ble Pi that is available Pi availability and is tected Pi adsorbed on sur- chemiabsorbed to faces of crystalline amorphous and P compounds crystalline A1 and

Fe

[6] Directly exchange- Labile Pi that is More resistant Pi No information able with the soil adsorbed onto soil that is associated solution and is bio- colloids with humic com- logically available pounds and

adsorbed to AI and Fe

[ 7 ] Rapid turnover Pi Rapid turnover Pi Slow turnover Pi Slow turnover Pi

aReferences: [ 1 ] Walker and Syers ( 1976); [2] Hedley et al. ( 1982a,b); [3] Tiessen et al. ( 1984); [4] Smeck (1985); [5] Wager et al. (1986); [6] Schoenau et al. (1989); [7] Trasar-Cepeda et al. (1990).

B e f o r e H e d l e y et al. ( 1982a, b ) d e v e l o p e d the s e q u e n t i a l f r a c t i o n a t i o n (F ig . 1 ) , v a r i ous

e x t r a c t i o n a n d d i g e s t i o n m e t h o d s w e r e u s e d to q u a n t i f y t he a m o u n t o f p l a n t - a v a i l a b l e and

g e o c h e m i c a l l y f i x e d soi l p h o s p h o r u s . P l a n t - a v a i l a b l e p h o s p h o r u s , in a lka l ine soi ls , is o f t e n

e s t i m a t e d w i t h a s o d i u m b i c a r b o n a t e ex t r ac t b a s e d o n the m e t h o d o f O l s e n et al. ( 1 9 5 4 )


HCL Residual Bicarb Po NaOH and Sonic Po Comments

Occluded Pi Occluded Pi Non-occluded Po Non-occluded Po

Dissolves acid- Occluded phos- Labile form of soil Pi and Po compounds soluble Pin the phates and the Po and Po held at held more strongly by form of calcium- most stable the internal sur- chemisorption to AI phosphates and organic phos- faces of soil aggre- and Fe components of Pi which is phates gates soil surfaces occluded within sesquioxides

Largely calcium- Occluded Pi cov- Labile Po is easily Stable Po that is bound ered with ses- mineralized and involved with long

quioxides and contributes to plant term transformation other Po available P of P in soils

Distinction between non-occluded and occluded Po is not absolute

Primary P miner- Occluded Pi: Labile Po in equi- Secondary mineral als that are acid physically librium with the Po: chemiadsorbed to extractable encapsulated in soil solution: iso- surfaces of A1 and Fe

minerals that topically extracta- oxides and carbonates have no struc- ble tural P

Stable Ca-bound Probably Labile Po is easily Stable Po that is phosphate includes stable mineralized and involved with long

humic acid and contributes to plant term transformation humus and rela- available P of P in soils tively insoluble Pi and Po

More stable Pi of Highly resistant Labile Po that is More resistant Po that minerals of low Pi and Po of low adsorbed onto soil is associated with solubility such as bioavailability colloids humic compounds apatite and adsorbed to AI

and Fe

Did not use the Hedley fractionation, the translation of his terms into the Hedley is our own.

Slow turnover Pi No information Rapid turnover Po Rapid and slow turnover Po

( s e e a l so B a r r o w and S h a w , 1976; B o w m a n a n d C o l e , 1978; S i m s , 1989) . In ac id so i l s ,

p l a n t - a v a i l a b l e p h o s p h o r u s is o f t e n m e a s u r e d w i t h an ac id e x t r a c t b a s e d on the m e t h o d o f

B r a y a n d K u r t z ( 1 9 4 5 ) . I n o r g a n i c p h o s p h o r u s b o u n d to c a l c i u m c a r b o n a t e , i ron , o r a lu-

m i n u m m i n e r a l s is u sua l l y e s t i m a t e d w i t h va r i ous ac id d i g e s t s m o d i f i e d f r o m the C h a n g

206 A.F. Cross, W.H. Schlesinger / Geoderrna 64 (1995) 197-214

and Jackson (1957) methods (Jackson, 1958; Peterson and Corey, 1966). The total soil phosphorus pool is usually estimated by digestion, ignition, or fusion methods (Metha et al., 1954; Legg and Black, 1955; Dormaar and Webster, 1964; Dick and Tabatabai, 1977; Lajtha and Schlesinger, 1988; Condron et al., 1990; Fox et al., 1990). By combining results from the above methods, one could theoretically establish the proportion of phosphorus held in each form.

Several authors have found a positive correlation between values for labile phosphorus in the Hedley fractionation and inorganic phosphorus extracted by other methods (Tiessen et al., 1984; Schlesinger et al., 1989). Sharpley et al. (1987) found a correlation between the Hedley resin and bicarbonate phosphorus fractions and the labile Olsen phosphorus in alkaline soils and Bray- 1 phosphorus in highly weathered soils. Trasar-Cepeda et al. (1986) found a strong correlation between values for inorganic phosphorus extracted with the Hedley method and values obtained following Chang and Jackson (1957). While the Hedley fractionation has been used successfully for temperate soils, this fractionation results in an underestimate of microbial P in tropical soils when soils are allowed to dry (Potter et al., 1992). One advantage of the Hedley scheme over previous methods is that the same soil sample is sequentially treated with the various reagents. As a result, one can establish the proportion of labile, non-labile, non-occluded, and occluded phosphorus in each sample.

3. Methods

In this study, we use the terminology of previous authors, but we offer two new interpre- tations of soil phosphorus data from the Hedley fractionation method. First, we reconsider the common interpretation of the Hedley fractionation, which recognizes plant-available and refractory forms (see Frossard et al., 1989). In this classification, plant- and microbe- available or "labile" phosphorus includes the sum of Pi and Po from Resin and Bicarb extractions, while refractory or unavailable phosphorus includes all of the other fractions (NaOH Pi, NaOH Po, Sonic Pi, Sonic Po, HC1 Pi, Residual P). Second, we suggest an alternative interpretation of the Hedley fractionation, recognizing organically bound and geochemical fractions. In this scheme, we consider that biological P includes all the extracted organic fractions (Bicarb Po, NaOH Po, Sonic Po), which is a conservative estimate of organic P in soils, because Po may be rapidly mineralized into Pi and the Residual P fraction contains some stable forms of Po. The geochemical P includes the remaining fractions (Resin Pi, Bicarb Pi, NaOH Pi, Sonic Pi, HC1Pi) and the Po and Pi in the Residual fraction.

The literature data were analyzed using both the absolute values (/.,g P/g soil) of soil phosphorus and the percentage of total phosphorus held in each fraction. Our analyses were restricted to the P values reported for surface soils (0-15 cm). Because differences in the absolute values of soil phosphorus may be biased by the influence of parent material, percentages were used to evaluate the differences between organically bound and geochemical fractions in different soils. The studies varied in the completeness of the Hedley fractionation; therefore, studies with missing values for any extract were not included in calculation of the percentages. This resulted in the elimination of all data from Spodosols.

We ordered the data according to the weathering regime that was presented by Smeck (1985), which ranks the soil orders from least weathered to most highly weathered based


on a hypothetical C / Po ratio. All data were analyzed using SAS programs to test for outliers, normality, and heteroscedasticity. Following the removal of outliers, the data were analyzed using JMP, version 2 (SAS Institute, 1989). The percentage values were arcsin transformed and analyzed with a one-way analysis of variance, excluding the Oxisol data with an N = 1 (Sokol and Rohlf, 1982). A posteriori differences between the means were calculated with the Student's approximate t-test, and when it was inappropriate to use the pooled standard error, data were analyzed with the Tukey-Kramer test (Sokol and Rohlf, 1982; Don Burdick pers. commun.).

4. Results

The absolute values (/xg P/g soil) show that the total soil phosphorus pool decreases as a function of soil development (Fig. 2). Total phosphorus values range from an average of 684/xg P/g soil in Entisols, where HCl-extractable fractions dominate the inorganic soil phosphorus pool, to between 200 and 430/xg/g soil in Ultisols and Oxisols, where the HCl- fraction has been removed by chemical weathering.

Phosphorus Fractions of Total P (/tg P/g soil)

8 0 0

700

600

500

400

300

200

100

0

Ent lncp Arid Vert Moll Spod Alf Ult Ox N= 2 5 9 3 42 6 13 7 1

Fig. 2. Mean content (/xg P/g soil) of soil phosphorus fractions in each soil order. Error bars show one standard error for total P. Different letters indicate significant differences in the total P content among soil orders at the p < 0.05 level for a Student's t-test.

208 A.F. Cross, W.H. Schlesinger / Geoderma 64 (1995) 19~214

P h o s p h o r u s Fract ions % of Total P

120 . . . . . . .

100

80

60

40

20

N=

Inorganic P Forms [llll Res+Bic,q'P

NaOH+Somc/TP HCVFP

• Residual p,rrp

Organic P Forms [] Total PoFl'P

Ent Incp Arid Vert Moll All Ult Ox 2 2 4 2 33 12 5 1

Fig. 3. Soil phosphorus fractions for each soil order expressed as a percentage of total phosphorus.

As a percentage of total phosphorus, inorganic phosphorus in resin and bicarbonate extracts constitutes less than 6% and 4%, respectively, of the total phosphorus pool uni- formly across all soil orders (Fig. 3 ). The NaOH- and sonicated-NaOH inorganic fractions make up less than 25% and 5%, respectively, of the total phosphorus pool across all soil orders, and these are most prominent in acidic, highly weathered soils where sesquioxides dominate soil chemical reactions (e.g., Ultisols). An inverse pattern is recognized for the HC1 fraction, where interactions of phosphorus with calcium minerals dominate the soil chemical reactions of the circum-neutral, less weathered soils (e.g., Aridisols) . The percentage of HCl-extractable phosphorus in the total phosphorus pool ranges from a maximum of 66% in the Entisols to less than 1% in the highly weathered Oxisols (Fig. 3). The residual pool consistently makes up about 40% of the total phosphorus pool across all soil orders. The percentage of phosphorus in various organic forms is greater in the highly weathered soils (e.g. 35% in Oxisols) , where up to 23% is held in the NaOH- and NaOH-Sonic organic fractions.

The sum of Resin Pi, Bicarb Pi, and Bicarb Po constitutes the plant-available or labile P fraction, which consistently makes up less than 14% of the total P across all soil orders


Biological and Geochemical Phosphorus

• Organically-bound P Inorganically-bound P

= A A ABC 100 ~ ABC N ~ B CD

8o - D

% 6 0 ~

40

20 cd

Ent Incp Arid Vert Moll A l f Ult Ox

N= 2 2 4 2 33 12 5 1 Fig. 4. Biological phosphorus includes Bicarb Po, NaOH Po, and Sonic Po fractions (black bars) and geochemical phosphorus includes Resin Pi, Bicarb Pi, NaOH Pi, HCI, and Residual P fractions (striped bars). Significant differences among soil orders - - p < 0.05 level for a one-way analysis of variance -- are indicated by different letters, with small case letters for the biological fractions and upper case letters for the geochemical fractions.

(Fig. 3 ). The refractory, unavailable P fractions, NaOH Pi, NaOH Po, Sonic Pi, Sonic Po, HC1 Pi, Residual P, consistently make up about 86% of the total P across all soil orders (Fig. 3). Biologically active or organically bound P comprises Bicarb Po, NaOH Po, and Sonic Po and its percentage increases as soil weathering increases - - from 5% in Entisols to 35% in Oxisols (Fig. 4). The geochemical P fractions decrease along the weathering gradient, from about 95 % in Entisols to 65 % in Oxisols (Fig. 4). The separation into organic versus geochemical P forms appears to be more sensitive to changes in phosphorus distribution during soil development than the traditional separation into labile versus non-labile P forms.

5. Discussion

In the Spodosols of a hardwood forest of the northeastern United States, Wood et al. (1984) showed that chemical fixation by soil organic matter and by the siliceous residues of weathered minerals removed only small amounts of phosphorus from the soil solution. They suggested that biological processes may dominate the soil phosphorus cycle, or at least control phosphorus distribution in the upper soil horizons (AO and A2). In contrast, Walbridge et al. ( 1991 ) found an equal contribution of biological and geochemical proc-


100

80

Bicarb Po/ Resin Pi + Bicarb Pi +

i

Bicarb Po !

6 0

%

40

20

0 Ent Incp Arid Vert Mol l Alf Ult Ox

N= 2 2 4 2 33 12 5 1 Fig. 5. Bicarbonate Po as a percentage of the available phosphorus pool ( resin and bicarbonate extracts ). Significant differences among soil orders for a Student's t-test at the p < 0.05 level is indicated by different letters.

esses in controlling P availability at all depths of acid forest soils (Ultisols and Inceptisols) of the southeastern United States. Because organic acids inhibit crystallization of Fe and AI oxides in these soils, most phosphorus is fixed by amorphous Fe and A1 minerals. Thus, biotic processes act indirectly to control P availability by influencing the form of soil minerals that geochemically fix phosphorus.

The relative contribution of biological processes to the distribution of total soil phosphorus can be estimated by using soil phosphorus values from the Hedley fractionation method. The bicarbonate Po as a percent of the total labile forms of phosphorus (Resin Pi, Bicarb Pi, Bicarb Po) represents a minimum index of the portion of phosphorus that may be easily mineralized through biological processes. Along the weathering gradient, the fraction of bicarbonate Po increases (Fig. 5). This suggests that values from the Hedley fractionation can be used to generate an index of the importance of organically bound P as a source of labile, plant-available P.

If the resin and bicarbonate fractions represent soil phosphorus that is both exchangeable and easily mineralizable, then the fraction of the total soil phosphorus pool that is available to vegetation is a minute fraction of the total phosphorus pool, either as an absolute value or as a percentage of total phosphorus (Figs. 2 and 3). This suggests that the dominant processes that regulate the soil phosphorus cycle are the geochemical reactions. Within the labile pool (resin- and bicarbonate-extractable phosphorus), the percentage held in organic


form (bicarbonate Po) increases with soil weathering, indicating an increasing importance of organic-P as a source of plant-available P with soil age (Fig. 5).

Data from the Hedley fractionation also support the ideas of Walker and Syers (1976), Stewart and Tiessen (1987) , and Smeck ( 1985 ) that the pool of primary phosphate declines and the stable organic pool increases during soil development. Phosphorus moves from the labile pools into the non-occluded and occluded pools. In particular, data from the NaOH, the sonicated-NaOH, and HC1 extracts illustrate these dynamics (Figs. 2 and 3). The NaOH and sonicated-NaOH phosphorus fractions increase as phosphorus becomes geochemically fixed to the iron and aluminum oxides in the more highly weathered soils (Sharpley et al., 1987).

Traditionally, the Hedley fractionation has been used to separate plant-available or " l a b i l e " forms of P from various refractory phosphorus pools in the soil (Tiessen and Moir,

1993). Our analysis of soil phosphorus data suggests that the Hedley fractionation also offers a useful index of the relative importance of phosphorus cycling by biological versus geochemical processes in soils at different stages of development. In order to more com- pletely test our hypothesis, additional studies using this fractionation scheme are needed to evaluate the soil phosphorus cycle in Spodosols, Histosols, and many soils of the tropics.

Acknowledgements

We appreciate comments provided by Mark Walbridge, Dan Richter, and members of our lab group: Patrick Megonigal, Antonio Gallardo, and Anne Hartley. Statistical advice was generously given by Don Burdick and David Tremmel. The manuscript was improved by the comments and editorial remarks of L.R. Gardner, an anonymous reviewer, and Robert S. Cross. This research was supported in part by a NASA Graduate Student Fellowship for Global Change Research granted to AFC.

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