GEODI::R~A

ELSEVIER Geoderma 64 (1995) 197-214

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, 0016-7061/95/$09.50 1995 Elsevier Science B.V. All rights reserved SSDIO01 6-706 1 (94) 00023-4

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 phosphorusdeficient 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; Richardson, 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 (Lindsay, 1979; Lajtha and Bloomer, 1988). Soils that dominate humid temperate and tropical regions (Ultisols and Oxisols) are highly weathered, acidic, and dominated by large quantities 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~

Resin P (Pi) Bicarbonate P (P, and Po) Hydroxide P (P, and Po)

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

h= V

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

IL.

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

Sonicatelhydroxide P
(Pi and Po)

Acid P (P.)

Residual Soil Digest with 5 mL H2SO4 and H202

Residue P(total P only)

Fig. 1. Hedleysequentialphosphorusfractionationmethodfor soils (afterTiessenet 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 Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Mollisol Aridisol Aridisol Aridisol Aridisol Aridisol Aridisol Resin 24.9 9 59.9 9. 6 15.93 5. 73 10.33 20.27 19.38 33.64 20.29 25.08 20.94 8.43 t7.12 13.06 21 8 59 20 17 18 39 27 18 7 5 24 9 22.4 16 17.3 12.7 15.3 8 8.5 19.1 17.6 9.3 21 26 34 38.39 21 47 17 63 39 Bicarb 12.8 7 17.9 I O.53 12.53 I. 93 6.33 10.69 9.69 18.07 13.2 15.18 16.05 11.24 14.58 10.57 8 9 29 9 7 8 24 14 11 4 3 14 11 7.8 5.8 6.3 4.6 5.3 5.1 5.3 9.3 9.3 5.9 21 17 25 6.7 19 12 19 36 32 Res + Bic 37.7 16 77.8 20.13 28.46 7. 66 16.66 30.96 29.08 51.71 33.49 40.26 36.99 19.67 31.7 23.63 29 17 88 29 24 26 63 41 29 Il 8 38 20 30.2 21.8 23.6 17.3 20.6 13.1 13.8 28.4 26.9 15.2 42 43 59 45.09 40 59 27 99 71 NaOH 15.3 11 32.8 96.33 144.93 62.27 92.33 11.82 19.38 38 15.5 23.1 26.52 11.24 16.48 19.27 26 27 71 29 1l 15 69 41 41 12 6 42 30 17.6 12.9 13.7 12.1 12 13.5 14.5 19.6 16.5 12.8 83 54 45 11.43 8 30 35 96 101 Sonic 3.6 4.72 4.72 N+ S 18.9 I1 32.8 96.33 144.93 62.27 92.33 15.2 23.94 46.72 18.94 29.04 32.8 12.92 20.92 23.88 30.76 31.76 80 36 13 19 79 50 48 15 7 50 39 21.8 15.7 16.7 15.1 14 16.6 17.9 23.2 19.6 15.2 83 54 45 11.43 9 34 42 113 101 HC1 272 218 211.3
.-

3.38 4.56 8.72 3.44 5.94 6.28 1.68 4.44 4.61 4.72 4.72 9 7 2 4 10 9 7 3 I 8 9 4.2 2.8 3 3 2 3.1 3.4 3.6 3.1 2.4 -

1 4 7 17 -

209.44 156.75 127.09 190.57 168.96 157.05 192.77 t42.65 164.35 280 252 70 197 209 130 87 48 62 63 200 58 58 166.2 168.8 166 172.9 ! 68.6 203.8 201.2 199.1 208.4 204.3 211 402 130 580.08 293 203 183 448 212

A.F. Cross, W.H. S c h l e s i n g e r / G e o d e r m a 64 ( 1 9 9 5 ) 1 9 7 - 2 1 4

201

Resid 363 254 243.2

269.47 199.87 221.2 184.73

Total P 768 590.8 682.12

385.93 373.23 291.13 293.72

BPo 10.2 7.5 14.3

5.07 14.33 20 16.27

NPo 57.9 73 86.7

-

SPo 8.3 11.3 11.3

TPo 66.2 80.5 101

Study Campbell et al. 1986 McKenzie et al. 1992a O'Halloran and DeJong 1987
Pare and Bernier 1989 Pare and Bernier 1989 Pare and Bernier 1989 Pare and Bernier 1989

255.6 370.18 226.77 253.71 276.54 270.15 256.27 295.44 339.46 273 341 341 200 238 193 260 262
171

563 670 623.35 574.2 660 697.32 562.56 633.36 763.28 688.18 752.18 668 534 574 488 707 642
310

7.88 16.53 33.02 7.46 21.12 37.69 5.06 11.41 27.65 11 15 10 13 14 31 68 68

-

38.85 67.26 120.6 61.99 110.88 144.49 65.19 117.29 167.42 53 57 72 50 67 78 141 156
-

5.07 6.27 17.44 8.04 13.2 18.15 10.68 13.95 16.89 11.3 11.3 7 9 9 11 9 17 6 5 15
30

51.8 90.06 171.06 77.49 145.2 200.33 80.93 142.65 211.96 75.42 83.42 89 72 90 120 218 241 94 70 152
84

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
S h a r p l e y et al. 1 9 8 5

199 191 220 207.5 195.6 198.4 208.4 200.6 359.5 361.9 364.9 361 377.7
260.4

382 476 518

201

16 9 37
4

72 56 100
50

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. 1 9 9 0

510.5 484.2 483.9 490.4 490.4 679.5 701.1 718 712.3 711.6
336 499 234 897

8.3 8 7.5 8.2 8.7 7 7.6 8.7 12.9 8

. . . . . .

67.2 65.9 61.8 58.5 68.6 65.8 85.1 80.4 74.9 83.8
. . . . . .

9.3 8.4 9.9 10 9.3 13.7 13.6 13.3 8.6 7.4

-

84.8 82.3 79.2 76.7 86.6 86.5 106.3 102.4 96.4 99.2

Wager et al. Wager et al. Wager et al. Wager et al. Wager et al. Wager et al. Wager et al. Wager et al. Wager et al. Wager et al.

1986 1986 1986 1986 1986 1986 1986 1986 1986 1986

Yang and Jacobsen 1990 Yang and Jacobsen 1990 Yang and Jacobsen 1990 Lajtha and Schlesinger 1988

120 107 132 171

-

492 447 424 908

384

5 6 8 14
. .

21 32 27 56
. .

4 6 5 7

30 44 40 77

Sharpley et al. Sharpley et al. Sharpley et al. Sharpley et al.

1985 1985 1985 1985

Yang and Jacobsen 1990

202 Table I continued. Soil Order Aridisol Aridisol Aridisol Alfisol Alfisol Alfisol Alfisol Alfisol Alfisol Alfisol Alfisol Alfisol Alfisol Alfisol Alfisol Alfisol Entisol Entisol Inceptisol lnceptisol lnceptisol lnceptisol lnceptisol Spodosol Spodosol Spodosol Spodosol Spodos ol Spodosol Ultisol Ultisol Ultisol Ultisol Ultisol Ultisol Ultisol Vertisol Vertisol Vertisol Oxisol Resin 13 5.21 7.07 58 11.69 14.2 27.55 6 5 9 20 9 11 9 8 12 5 13 45 14 10 5 3 27.2 18. 53 28 24.2 26.73 11 1 6 2 27 4 37 9 10 17 32 5

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

Bicarb 14 3.09 7.82 56 7.16 13.1 21.54 6 5 12 17 8 5 3 17 17 4 5 39 13 9 9 7 20.13 15.33 20.47 17.8 l 9.8 7 3 6 1 25 3 17 5 9 7 42 4

Res + Bic 27 8.3 14.89 114 18.85 27.3 49.09 12 10 21 37 17 16 12 25 29 9 18 84 27 19 14 10 47.33 33.86 48.47 42 46. 53 18 4 12 3 52 7 54 14 19 24 74 9

NaOH 46 8.99 6.29 155 13.95 25.48 44.59 20 19 57 65 56 16 6 36 14 6 7 86 24 60 66 91 96.27 30. 67 58.13 93.73 41.53 13 29 37 6 75 24 62 18 22 14 59 83

Sonic

N+ S 46 12.21 9.87 155 17.72 30.94 53.1 l 27.5 26.5 64.5 79 69 20 8 45 16 8 9 92.6 30.6 70 76 1O0 96.27 30. 67 58.13 93.73 41.53 16 38 45 8 88 31 72 23 24 19 59 100

HC1 198 61.02 166.4 240 125.92 144.14 181.86 52 35 86 75 47 6 23 102 10 536 372 174 193 12 12 6

3.22 3.58 7.45 3.77 5.46 8.52 7.45 7.45 7.45 14 13 4 2 9 2 2 2 6.6 6.6 10 lO 9

-3 9 8 2 13 7 10 5 2 5 17

2 2 4 3 17 7 14 3 342 65 430 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. S c h l e s i n g e r / G e o d e r m a 6 4 ( 1 9 9 5 ) 1 9 7 - 2 1 4

203

Resid
-

Total P
271 114.44 237.65

BPo
-

NPo
-

SPo

TPo
-

Study
Yang and Jacobsen 1990 C r o s s a n d S c h l e s i n g e r (unpubL ) C r o s s a n d S c h l e s i n g e r (unpubL )

32.91 46.49

169 166.63 141.23 163.33 66 107 94 182 174 97 158

-

820 377 400.03 501 212.5 225.5 306.5 509 439 196 280
301

33 6.03 9.46 10.02 18 14 15 43 21 8 12

1

100 35.06 38.95 39.08 37 33 26 79 95 36 55

98

13 6.79 8.01 4.51 13 13 13 14 16 13 12

30

133 47.88 56.42 53.61 55 47 41 136 132 57 79

129

McKenzie et al. 1992b Roberts et al. 1985 Roberts et al. 1985 Roberts et al. 1985 Schoenau et al. 1989 Schoenau et al. 1989 Schoenau et al. 1989 Sharpley 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. 1991

10 187 158 323 200

123 76.33 101.4 113.53 76.93 -

188 765 604 849.8 514.8

218 235 285 300.13 151.13 229.27 276.93 174.92 97 64

14 4 4 44 14
17 16 32 33.53 10.27 21.27 27.67 9.93 5 6

99 18 34 120 38
82 96 127 42 9

10 3 9 12.2 12.2
18 21 10 14 5

123 25 47 176.2 64.2

117 133 169 33.53 10.27 21.27 2Z67 9.93 61 20

Sattell and Morris 1992 Sharpley et al. 1985 Sharpley et al. 1985 Schoenau et al. 1989 Schoenau et al. 1989
T r a s a r - C e p e d a et al. 1991 T r a s a r - C e p e d a et al. 1991 T r a s a r - C e p e d a et al. 1991 Pare and Bernier 1989 Pare and Bernier 1989 Pare and Bernier 1989 Pare and Bernier 1989 Pare and Bernier 1989 T r a s a r - C e p e d a et al. 1 9 9 0 L e e et al. 1 9 9 0

89 42 89 165 54
-

230 81 435 300 257

99

I1 6 38 10 8
8

55 16 122 66 45
39

14 3 29 14 10
12

80 25 189 90 63
59

Sharpley et al. Sharpley et al. Sharpley et al. Sharpley et al. Sharpley et al.

1985 1985 1985 1985 1985

T r a s a r - C e p e d a et al. 1 9 9 0

281 136
-

736 289
563

7 6
. .

57 31
. .

6 8 17

70 45 152

Sharpley et al. 1985 Sharpley et al. 1985

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

165

429

27

108

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).

204

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

Table 2 Terminology of phosphorus compounds and extracts in the Hedley et al. (1982a,b), extraction Ref? [ 1] Resin Pi Non-occluded Pi Bicarb Pi Non-occluded Pi NaOH Pi Non-occluded Pi Sonic Pi Occluded Pi

[21

Form of soil Pi from which plants normally draw their supply

Extracts additional Pi that is available to plants

Partially dissolves Fe-AI phosphates and desorbs Pi from the surfaces of sesquioxides

Pi held at the internal surfaces of soil aggregates

[31

Labile Pi adsorbed on surfaces of crystalline compounds

Labile Pi adsorbed on surfaces of crystalline compounds

Less labile Pi associated with exteriors of amorphous A1 and Fe phosphates

Less labile Pi associated with interiors of amorphous AI and Fe phosphates Secondary mineral Pi: chemiabsorbed within A1 and Fe oxides and carbonates

[41

Soluble and Labile Pi: anion resin- or water-extractable

Labile Pi in equilibrium with the soil solution: isotopically extractable

Secondary mineral Pi: chemiabsorbed to surfaces of AI and Fe oxides and carbonates

[5 ]

Most plant available Pi that is adsorbed on surfaces of crystalline P compounds

Readily plant available Pi

Of lesser plant availability and is chemiabsorbed to amorphous and crystalline A1 and Fe More resistant Pi that is associated with humic compounds and adsorbed to AI and Fe Slow turnover Pi

Aggregated-protected Pi

[6]

Directly exchangeable with the soil solution and is biologically available

Labile Pi that is adsorbed onto soil colloids

No information

[7 ]

Rapid turnover Pi

Rapid 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 t h e s e q u e n t i a l f r a c t i o n a t i o n ( F i g . 1 ), v a r i o u s 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 h e a m o u n t o f p l a n t - a v a i l a b l e a n d g e o c h e m i c a l l y f i x e d soil 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 l k a l i n e soils, 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 e x t r a c t b a s e d o n t h e m e t h o d o f O l s e n et al. ( 1 9 5 4 )

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

205

HCL Occluded Pi

Residual Occluded Pi

Bicarb Po Non-occluded Po

NaOH and Sonic Po Non-occluded Po

Comments Distinction between non-occluded and occluded Po is not absolute

Dissolves acidsoluble Pin the form of calciumphosphates and Pi which is occluded within sesquioxides Largely calciumbound

Occluded phosphates and the most stable organic phosphates

Labile form of soil Po and Po held at the internal surfaces of soil aggregates

Pi and Po compounds held more strongly by chemisorption to AI and Fe components of soil surfaces

Occluded Pi covered with sesquioxides and other Po

Labile Po is easily mineralized and contributes to plant available P

Stable Po that is involved with long term transformation of P in soils

Primary P minerals that are acid extractable

Occluded Pi: physically encapsulated in minerals that have no structural P Probably includes stable humic acid and humus and relatively insoluble Pi and Po Highly resistant Pi and Po of low bioavailability

Labile Po in equilibrium with the soil solution: isotopically extractable

Secondary mineral Po: chemiadsorbed to surfaces of A1 and Fe oxides and carbonates

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

Stable Ca-bound phosphate

Labile Po is easily mineralized and contributes to plant available P

Stable Po that is involved with long term transformation of P in soils

More stable Pi of minerals of low solubility such as apatite

Labile Po that is adsorbed onto soil colloids

More resistant Po that is associated with humic compounds and adsorbed to AI and Fe

Slow turnover Pi

No information

Rapid turnover Po

Rapid and slow turnover Po

( s e e a l s o B a r r o w a n d S h a w , 1976; B o w m a n a n d C o l e , 1978; S i m s , 1 9 8 9 ) . I n a c i d soils, 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 a n a c i d e x t r a c t b a s e d o n t h e 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 , iron, o r alum i n u m m i n e r a l s is u s u a l l y e s t i m a t e d w i t h v a r i o u s a c i d d i g e s t s m o d i f i e d f r o m t h e 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 interpretations 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 microbeavailable 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

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

207

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 HClfraction has been removed by chemical weathering.

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

800

700

600

500

400

300

200

100

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

Inorganic P Forms [llll Res+Bic,q'P NaOH+Somc/TP HCVFP Residual p,rrp

P h o s p h o r u s Fractions % of Total P
120
. . . . . . .

Organic P Forms [] Total PoFl'P

100

80

60

40

20

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

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

209

Biological and Geochemical Phosphorus

= 100 A ~ A N ABC ~ Organically-bound P Inorganically-bound P B CD

ABC

8o %60 ~

40

20

cd

Ent Incp Arid Vert Moll Alf Ult Ox N= 2 2 4 2 33 12 5 1 Fig. 4. BiologicalphosphorusincludesBicarbPo, NaOHPo, and SonicPo fractions(blackbars) and geochemical phosphorus includes Resin Pi, Bicarb Pi, NaOH Pi, HCI, and Residual P fractions (striped bars). Significant differencesamongsoil orders-- p < 0.05 levelfor a one-wayanalysis of variance-- are indicatedby different letters, with small case lettersfor the biologicalfractionsand uppercase lettersfor the geochemicalfractions. (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-

210

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

B i c a r b Po/ Resin Pi + Bicarb Pi + Bicarb Po

100
i !

80

60

% 40

20

0 Ent Incp Arid Vert Moll Alf Ult Ox N= 2 2 4 2 33 12 5 1 Fig. 5. BicarbonatePo as a percentageof the availablephosphoruspool (resin and bicarbonateextracts). Significant differences amongsoil orders for a Student's t-test at the p < 0.05 level is indicated by differentletters. 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

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

211

form (bicarbonate Po) increases with soil weathering, indicating an increasing importance of organic-P as a source o f plant-available P with soil age (Fig. 5). Data from the Hedley fractionation also support the ideas of W a l k e r 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 completely 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
W e 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 N A S A Graduate Student Fellowship for Global Change Research granted to AFC.

References
Anderson, D.W., 1988. The effect of parent material and soil development on nutrient cycling in temperate ecosystems. Biogeochemistry,5:71-97. Ballard, R., 1980. Phosphorusnutrition and fertilizationof forest trees. In: F.E. Khasawneh, E.C. Sample, and E.J. Kampreth (Editors), The Role of Phosphorus in Agriculture.Am. Soc. of Agronomy, Madison, WI, pp. 763804. Barrow, N.J. and Shaw, T.C., 1976. Sodium bicarbonate as an extractant for soil phosphate. I1. Effect of varying the initially displaced and on the secondary adsorption. Geoderma, 16: 109-123. Birkeland, P.W., 1984. Soils and Geomorphology.Oxford Univ. Press, New York. Bolan, N.S., 1991. A critical review on the role of mycorrhizal fungi in the uptake of phosphates by plants. Plant Soil, 134: 189-207. Bowman, R.A. and Cole, C.V., 1978. Transformationsof organic phosphorus substrates in soils as evaluated by NaHCO3 extractions. Soil Sci., 125: 49-54. Bray, R.H. and Kurtz, L.T., 1945. Determinations of total, organic and available forms of phosphorus in soils. Soil Sci., 59: 39-45. Campbell, C.A., Schitzer, M., Stewart, J.W.B., Biederbeck, V.O. and Selles, F., 1986. Effect of manure and P fertilizer on properties of a Black Chernozem in southern Saskatchewan. Can. J. Soil Sci., 66:601~613.

212

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

Chang, S.C. and Jackson, M.L., 1957. Fractionation of soil phosphorus. Soil Sci., 84: 133-144. Condron, L.M., Moir, J.O., Tiessen, H., Stewart, J.W.B., 1990. Critical evaluation of methods for determining total organic phosphorus in tropical soils. Soil Sci. Soc. Am. J., 54:1261-1266. Day, L.D., Collins, M.E. and Washer, N.E., 1987. Landscape position and particle-size effects on soil phosphorus distributions. Soil Sci. Soc. Am. J., 51:1547-1553. Dick, W.A. and Tabatabai, M.A., 1977. An alkaline oxidation method for determination of total phosphorus in soils. Soil Sci. Soc. Am. J., 41:511-514. Dormaar, J.F. and Webster, G.R., 1964. Losses inherent in ignition procedures for determining total organic phosphorus. Can. J. Soil Sci., 44: l ~ . Fox, T.R., Comerford, N.B. and White, W.W., 1990. Kinetics of phosphorus release from Spodosols: Effects of oxalate and formate. Soil Sci. Soc. Am. J., 54: 1441-1447. Frossard, E., Stewart, J.W.B., and St. Arnaud, R.J., 1989. Distribution and mobility of phosphorus in grassland and forest soils of Saskatchewan. Can. J. Soil Sci., 69: 401-416. Gardner, L.R., 1990. The role of rock weathering in the phosphorus budget of terrestrial watersheds. Biogeochemistry, 11: 97-110. Harrison, A.F., 1982a. 32P-metfiod to compare rates of mineralization of labile organic phosphorus in woodland soils. Soil Biol. Biochem., 14: 337-341. Harrison, A.F., 1982b. Labile organic phosphorus mineralization in relationship to soil properties. Soil Biol. Biochem., 14: 343-351. Hedley, M.J., Stewart, J.W.B. and Chauhan, B.S., 1982a. Changes in inorganic and organic soil phosphorus fractions by cultivation practices and by laboratory incubations. Soil Sci. Soc. Am. J., 46: 970-976. Hedley, M.J., White, R.E. and Nye, P.H., 1982b. Plant induced changes in the rhizosphere of rape, Brassica napus var. Emerald. seedlings. III. Changes in L value, soil phosphate fractions, and phosphatase activity. New Phytol., 91: 45-56. Jackson, M.L., 1958. Soil Chemical Analysis. Prentice-Hall, Englewood Cliffs, NJ. Jenny, H., 1980. The Soil Resource: Origin and Behavior. Springer, New York. Johnson, D.W. and Cole, D.W., 1980. Anion mobility in soils: Relevance to nutrient transport from forest ecosystems. Environ. Int., 3: 79-90. Jurinak, J.J., Dudley, L.M., Allen, M.F., and Knight, W.G., 1986. The role of calcium oxalate in the availability of phosphorus in soils of semiarid regions: A thermodynamic study. Soil Sci., 142: 255-262. Lajtha, K. and Bloomer, S.H., 1988. Factors affecting phosphate sorption and phosphate retention in a desert ecosystem. Soil Sci., 146: 160-167. Lajtha, K. and Schlesinger, W.H., 1988. The biogeochemistry of phosphorus cycling and phosphorus availability along a desert soil chronosequence. Ecology, 69: 24-39. Lee, D., Han, X.G. and Jordan, C.F., 1990. Soil phosphorus fractions, aluminum, and water retention as affected by microbial activity in an Ultisol. Plant Soil, 121: 125-136. Legg, J.D. and Black, C.A., 1955. Determination of organic phosphorus in soils. II. Ignition method. Soil Sci. Soc. Am. Proc., 19: 139-142. Lindsay, W.L., 1979. Chemical Equilibria in Soils. Wiley, New York. McGill, W.B. and Cole, C.V., 1981. Comparative aspects of cycling organic C, N, S. and P through soil organic matter. Geoderma, 26: 267-28~. McKenzie, R.H., Stewart, J.W.B., Dormaar, J.F. and Schaalje, G.B., 1992a. Long-term crop rotation and fertilizer effects on phosphorus transformations: I. In a Chemozemic soil. Can. J. Soil Sci., 72: 569-579. McKenzie, R.H., Stewart, J.W.B., Dormaar, J.F. and Schaalje, G.B., 1992b. Long-term crop rotation and fertilizer effects on phosphorus transformations: I. In a Luvisolic soil. Can. J. Soil Sci.. 72: 581-589. Metha, N.C., Legg, J.O., Goring, C.A.1. and Black, C.A., 1954. Determination of organic phosphorus in soils. I. Extraction method. Soil Sci. Soc. Am. Proc., 18: 443~-48. O'Halloran, I.P. and DeJong, E., 1987. Changes in P forms and availability as influenced by management practices. Plant Soil, 100: 113-126. Olsen, S.R., Cole, C.V., Watanabe, F.S. and Dean, L.A., 1954. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. USDA Circular 939. Pare, D. and Bernier, B., 1989. Origin of the phosphorus deficiency observed in declining sugar maple stands in the Quebec Appalachians. Can. J. For. Res. 19: 24-34. Peterson, G.W. and Corey, R.B., 1966. A modified Chang and Jackson procedure for routine fractionation of inorganic soil phosphorus. Soil Sci. Soc. Am. Proc., 30:563-56 5.

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

213

Potter, R.L., Jordan, C.F., Guedes, R.M., Batmanian, G.J.B. and Han, X.G., 1992. Assessment of a phosphorus fractionation method for soils: problems for further investigation. Agric. Ecosyst. Environ., 34: 453-463. Ramirez, A.J. and Rose, A.W., 1992. Analytical geochemistry of organic phosphorus and its correlation with organic carbon in marine and fluvial sediments and soils. Am. J. Sci., 292:421-454. Richardson, C.J., 1985. Mechanisms controlling phosphorus retention capacity in freshwater wetlands. Science, 228: 1424-1427. Richey, J.E., 1983. The phosphorus cycle. In: B. Bolin and R.B. Cook (Editors), The Major Biogeochemical Cycles and Their Interactions. John Wiley, New York, pp. 51-56. Roberts, T.L., Stewart, J.W.B. and Bettany, J.R., 1985. The influence of topography on the distribution of organic and inorganic soil phosphorus across a narrow environmental gradient. Can. J. Soil Sci.; 65:651-665. Roberts, T.L., Bettany, J.R. and Stewart, J.W.B., 1989. A hierarchical approach to the study of organic C, N, P, and S in western Canadian Soils. Can J. Soil Sci., 69: 739-749. Sanchez, P.A., Gichuru, M.P., and Katz, L.B., 1982. Organic matter in major soils of the tropical and temperate regions. 12th int. Congr. of Soil Science Symposia Papers I, I: 99-114. SAS Institute, 1989. JMP User's Guide, Version 2 of JMP. SAS Institute Inc., Cary, North Carolina. Sattell, R.R. and Morris, R.A., 1992. Phosphorus fractionations and availability in Sri Lankan Alfisols. Soil Sci. Soc. Am. J., 56: 1510-1515. Schlesinger, W.H., DeLucia, E. and Billings, W.D., 1989. Nutrient-use efficiency of woody plants on contrasting soils in the Western Great Basin, Nevada. Ecology, 70:105-113. Schlesinger, W.H., 1991. Biogeochemistry: An Analysis of Global Change. Academic Press, San Diego, CA. Schoenau, J.J., Stewart, J.W.B. and Bettany, J.R., 1989. Forms and cycling of phosphorus in prairie and boreal forest soils. Biogeochemistry, 8: 223-237. Sharpley, A.N., Jones, C.A., Gray, Cole, C.V., Tiessen, H. and Holzhey, C.S., 1985. A detailed phosphorus characterization of seventy-eight soils. USDA Agricultural Research Services. ARS-31. Sharpley, A.N., Tiessen, H. and Cole, C.V., 1987. Soil phosphorus forms extracted by soil tests as a function of pedogenesis. Soil Sci. Soc. Am. J., 51: 362-365. Sims, J.T., 1989. Comparison of Melich I and Melich 3 extractants for P, K, Ca, Mg, Mn, Cu, and Zn in Atlantic coastal plain soils. Commun. Soil Sci. Plant Anal., 20: 1707-1726. Smeck, N. E., 1985. Phosphorus dynamics in soils and landscapes. Geoderma, 36: 185-189. Sokol, R.R. and Rohlf, F.J., 1982. Biometry: The Principles and Practice of Statistics in Biological Research. Freeman, New York. Sollins, P., Robertson, G.P. and Uehara, G., 1988. Nutrient mobility in variable- and permanent-charge soils. Biogeochemistry, 6: 181-199. Stewart, J.W.B. and Tiessen, H., 1987. Dynamics of soil organic phosphorus. Biogeochemistry, 4: 41-60. Srivastava, S.C. and Singh, J.S., 1988. Carbon and phosphorus in the soil biomass of some tropical soils of India. Soil Biol. Biochem., 20: 743-747. Tate, K.R. and Salcedo, I., 1988. Phosphorus control of soil organic matter accumulation and cycling. Biogeochemistry, 5: 99-107. Tiessen, H. and Moir, J.O., 1993. Characterization of available P by sequential extraction. In: M.R. Carter (Editor), Soil Sampling and Methods of Analysis. Lewis Publishers, Ann Arbor, pp. 75-86. Tiessen, H., Stewart. J.W.B. and Cole, C.V., 1984. Pathways of phosphorus transformations in soils of differing pedogenesis. Soil Sci. Soc. Am. J., 48: 853-858. Trasar-Cepeda, M.C., Gil-Sotres, F. and Giutain-Ojea, F., 1986. Caracterizacion del fosforo en suelos gallegos: Estudio comparativo del los procedimientos de Chang y Jackson, 1957, y de Hedley et al., 1982. An. Edaful. Agrobiol., 45: 37-52. Trasar-Cepeda, M.C., Gil-Sotres, F. and Giutain-Ojea, F., 1990. Relation between phosphorus fractions and development of soils from Galicia, NW Spain. Geoderma, 27:139-150 Trasar-Cepeda, M.C., Carballas, T., Gil-Sotres, F. and deBlas, E., 1991. Liming and the phosphate activity and mineralization of phosphorus in an andic soil. Soil Biol. Biochem., 23: 209-215. Udo, E.J. and Ogunwale, J.A., 1977. Phosphorus fractions in selected Nigerian soils. Soil Sci. Soc. Am. J., 41:
1141-1146.

Vitousek, P., 1984 Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology, 65: 285-298. Vitousek, P., Walker, L.R., Whiteaker, L.D., and Matson, P.A., 1993. Nutrient limitations to plant growth during primary succession in Hawaii Volcanoes National Park. Biogeochemistry, 23: 197-215.

214

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

Wager, B.I., Stewart, J.W.B. and Moir, J.O., 1986. Changes with time in the form and availability of residual fertilizer phosphorus on Cheruozemic soils. Can. J. Soil Sci., 66:105-119. Walbridge, M.R., 1991. Phosphorus availability in acid organic soils of the lower North Carolina coastal plain. Ecology, 72: 2083-2100. Walbridge, M.R. and Vitousek, P.M., 1987. Phosphorus mineralization potentials in acid organic soils: Processes affecting 32po3- isotope dilution measurements Soil Biol. Biochem., 19: 709-717. Walbridge, M.R., Richardson, C.J. and Swank, W.T., 1991. Vertical distribution of biological and geochemical phosphorus subcycle in two southern Appalachian forest soils. Biogeochemistry, 13: 61-85. Walker, T.W. and Syers, J.K., 1976. The fate of phosphorus during pedogenesis. Geoderma, 15: 1-19. Wood, T.M., Bormann, F.H. and Voigt, G.K., 1984. Phosphorus cycling in a northern hardwood forest: Biological and chemical control. Science, 223: 391-393. Yang, J.E. and Jacobsen, J.S., 1990. Soil inorganic phosphorus fractions and their uptake relationships in calcareous soils. Soil Sci. Soc. Am. J., 54: 1666-1669. Yanai, R.D., 1992. Phosphorus budget of a 70-year-old northern hardwood forest. Biogeochemistry, 17: 1-22.