ORIGINAL PAPER

Changes in phosphorus fractions, sorption and releasein Udic Mollisols under different ecosystems

C. Song & X. Z. Han & C. Tang

Received: 14 October 2006 /Revised: 31 January 2007 /Accepted: 5 February 2007 / Published online: 24 February 2007# Springer-Verlag 2007

Abstract A 20-year field trial was conducted to study theeffects of ecological factors and fertilization on phosphoruscharacteristics of fertile Udic Mollisols under three ecosys-tems: (1) bare land ecosystem with no vegetation orfertilizers (BE), (2) natural ecosystem with native grassesbut no fertilizers (NE) and (3) agroecosystem with arotation of wheat–soybean–corn. The agroecosystem hadreceived N and P fertilizers during 1985–1993 and hadreceived no fertilizers (CK), N and P fertilizers (NP) or Nand P fertilizers along with pig manure (NPM) during1994–2005. While there was no P input or removal in theBE and NE, the CK had a net P loss of 174 kg ha−1, whereasthe NP had a net gain of 96 kg/ha and the NPM 504 kgha−1. Increasing net P input increased both Olsen P andtotal P in the 0–20-cm soil. The amounts of NaHCO3-extractable (Ca2–P) and NH4Ac-extractable P fractions(Ca8–P) were in an order of NPM > NP > CK > NE > BE.The H2SO4-extractable fraction (Ca10–P) was lowest inthe BE and highest in the NPM but was similar in theother treatments. The CK had the least, and the NPM hadthe highest amounts of NH4F-extractable (Al–P) andNaOH–Na2CO3-extractable fractions (Fe–P). Among the

inorganic P, the percentage of Ca2–P, Ca8–P and Al–Pincreased, whereas that of Fe–P, occluded P and Ca10–Pdecreased with increasing P input into the system. SoilP adsorption was in an order of CK > NE > NP > BE >NPM, whereas P release was in an order of NPM ≫ NP >CK > NE > BE. The study concluded that soil P can besustained under the natural ecosystem while annualapplications of chemical fertilizers and animal manureincreased both labile and non-labile P pools in theagroecosystem.

Keywords Animal manure . Ecosystems . Fractionation .

Long term . Nutrient management . P sorption

Introduction

Phosphorus dynamics in soil and maintenance of itsadequate supply are important for sustainability of nativeand agricultural ecosystems. Phosphorus may accumulateand its bio-availability may increase in soils after contin-uous applications of fertilizers, which can have negativeimpacts on the environment as accumulated soil P in thetopsoil is a major source of soluble and particulate P insurface runoff (Daniel et al. 1998). On the other hand, Pmay be depleted to cause P deficiencies in crops if theoutputs exceed inputs in the long term.

Phosphorus is present in both inorganic and organicforms. Different forms of P exist in different amounts andproportions, depending on soil type and management. Theycan be transformed under certain conditions (Sharpley2000). Phosphorus fractionation provides an effectiveapproach for investigating soil P availability and Ptransformation in soil and the likelihood of its transport(Hedley et al. 1982a,b; Sui et al. 1999). While organic P

Biol Fertil Soils (2007) 44:37–47DOI 10.1007/s00374-007-0176-z

C. Song :X. Z. HanNortheast Institute of Geography and Agricultural Ecology,Chinese Academy of Sciences,Harbin 150081, China

C. Tang (*)Department of Agricultural Sciences, La Trobe University,Bundoora, Melbourne, Vic 3086, Australiae-mail: c.tang@latrobe.edu.au

C. SongGraduate School of Chinese Academy of Sciences,Beijing 100039, China

fractions are not well characterised, soil inorganic P canusually be divided into fractions as Ca–P, Al–P, Fe–P andoccluded P (Chang and Jackson 1957; Hedley et al. 1982a,b).

The P absorbed by plants directly comes from the soilsolution, and there is a dynamic equilibrium between P inthe soil solution and on the surface of clay particles(Barrow 1983). Such equilibrium is governed by P sorptionand release from the solid phase and plant P uptake(Sharma et al. 1995). Previous studies indicated that therelease rate of absorbed phosphorus directly affects the Psupply to plants (e.g. Hughes et al. 2000) and the useefficiency of P fertilizers (e.g. Fox and Kamprath 1970).

Phosphorus characteristics and fractionation have beenstudied in many soils under different farming systems (e.g.Börling et al. 2004; Shen et al. 2004; Allen and Mallarino2006). By contrast, little information is available about Pifractions and P transformation under different ecosystemsin Udic Mollisols, a soil type that is important for theproduction of high-quality grains in China. It is alsounknown whether soil fertility including P supply issustainable after the conversion from the native prairie tofarming lands. The present study used a 20-year long-termfield trial and aimed to compare P fractions, sorption andrelease under various ecosystems, to investigate the impactof fertilization on crop production, P balance and Ptransformation under an agroecosystem and, ultimately, tounderstand whether current ecosystems are sustainable in Pfertility.

Materials and methods

Field site description

The field site was located at the Hailun National FieldStation, Chinese Academy of Sciences, in the central areaof the black soil (Udic Mollisol) region in northeast China(47°26′N, 126°38′E). The site has annual rainfall of 500–600 mm, 88% of which is distributed in May–September,cumulative temperature (≥10°C) of 2,400–2,500°C, andannual day length of 2,600–2,800 h. Average temperaturesin January range from −22 to −25°C, and in July rangefrom 20 to 22°C. The field was flat plain and had been thenative prairie before land clearing for cropping more than100 years ago. The soil had not been fertilized in the first60 years after clearing and then had been supplied withfarm manures for 20 years. The fertilizer nitrogen had beenintroduced in the last 20 years before the trial.

Experimental design

A long-term trial was initiated in 1985. It consisted of threesoil ecosystems: (1) bare land ecosystem (BE), (2) Natural

soil ecosystem (NE) and (3) Agroecosystem. The threesystems were not randomised, and each was replicated fourtimes. In the BE ecosystem, the soil were kept bare withoutany vegetation, and weeds were hoed as soon as theybecame visible. The NE ecosystem had native vegetationbut without any fertilizer inputs or tillage. The agro-ecosystem had received chemical fertilizers the same asthe NP treatment between 1985 and 1993, and then in 1994,three different fertilizer treatments had been introduced;they were (1) no fertilizer control (CK), (2) continuousapplication of chemical N and P fertilizers (NP) and (3)chemical N and P fertilizers along with pig manure (NPM).The fertilizer treatments were randomized within the agro-ecosystem. Therefore, this trial eventually consisted of fivetreatments, each of which had four replicates. Plot sizeswere 360 m2 for the NE, 180 m2 for the BE and 60 m2 foreach fertilizer treatment within the agroecosystem.

Crops grown in the agroecosystem were wheat (Triticumaestivum L. cv. Long 4083), corn (Zea mays L. cv. Haiyu 6)and soybean [Glycine max (Merrill.) L. cv. Heinong 35] inrotation. Such a rotation represented the main croppingsystem in the region. The crops were grown one season peryear. The fertilizers were applied at the following rates(kg ha−1) for each crop: 120 N and 24 P as urea and(NH4)2HPO4, respectively, and 15,000 pig manure forwheat; 32.3 N, 36 P and 15,000 pig manure for soybean;and 150 N, 32.75 P and 30,000 pig manure for corn. Thepig manure contained average total N, P and K concen-trations of 22.1, 2.6 and 2.4 g kg−1, respectively, and anaverage organic P 2.3 g kg−1. Other nutrients including Kwere at adequate levels in the soil and thus were not appliedas fertilizers.

Grain yields and shoot biomass were recorded for eachcrop. Phosphorus inputs were calculated based on theapplied amounts of chemical P fertilizers, and pig manurewith a P concentration of 2.6 g kg−1. The P outputs wereestimated according to the grain yield and biomassproduction using an average P concentrations (g kg−1) of3.90 in grains and 0.70 in shoot for corn, 6.29 in grains and0.72 in shoot for soybean, and 3.40 in grains and 0.59 inshoot for wheat. The P balance during 1985–2005 wascalculated using the data of soil bulk density (ρ) and total P(Ptot) in 0–20 cm soil layer according to the followingequation.

P balance ¼ r� Ptotð Þ2005 � r� Ptotð Þ1985 ð1Þ

Soil collection and measurements

According to the results of a previous study on the samesoil type (Han et al. 2005a), long-term fertilizationinfluenced the P content mainly in 0–20 cm soil layer.

38 Biol Fertil Soils (2007) 44:37–47

Therefore, only 0–20 cm topsoil was sampled in this study.More than six soil cores were taken randomly from eachplot in October 1985 and in October 2005 after the cropwas harvested. The soil cores were then bulked, air-driedand sieved through 2 mm. Both the samples from 1985 and2005 were analysed at the same time.

Soil pH was measured in water extracts at a H2O:soilratio of 2.5:1. Organic C was determined using a wetoxidation method with K2Cr2O7 and concentrated H2SO4.The remaining dichromate was titrated using FeSO4 withthe indicator of O-phenylanthranilic acid (Nelson andSommers 1996). Total N was measured using a micro-Kjeldahl digestion method (Bremner 1996). Soil availableN was analysed through quantifying alkali-hydrolysable Nin the Conway diffusion unit with Devarda’s alloy in theouter chamber and boric acid-indicator solution in the innerchamber (Shen et al. 2004). Total K was determined in0.02 M HCl solution after the soil was fused with NaOH at720°C for 15 min, while available K was extracted in 1 MCH3COONH4 (pH 7; soil:solution=1:10) for 30 min. Soilbulk density was measured using the core method. Total Pin the soil was determined using the molybdenum-bluemethod after digestion with concentrated HClO4–H2SO4,while available P was determined with the Olsen method(Kuo 1996). Organic P was measured using the ignitionmethod described by Legg and Black (1955).

Inorganic P fractions were measured according to afractionation scheme (Jiang and Gu 1989) based on themethods described by Chang and Jackson (1957) andHedley et al. (1982a). Briefly, the fractionation involved asequential extraction with (1) 0.25 M NaHCO3 (pH 7.5) toextract Ca2–P, (2) 0.5 M CH3COONH4 (pH 4.2) to extractCa8–P, (3) 0.5 M NH4F (pH 8.2) to remove Al–P, (4) 0.1 MNaOH–0.1 M Na2CO3 to obtain Fe–P, (5) 0.3 M sodiumcitrate–Na2S2O4–0.5 M NaOH to obtain the occluded P and(6) 0.5 M H2SO4 to extract Ca10–P. These fractions weredesignated as NaHCO3-soluble P (Ca2–P), NH4Ac-solubleP (Ca8–P), NH4F-soluble P (Al–P), NaOH–Na2CO3-solubleP (Fe–P), occluded P (O–P), H2SO4-soluble P (Cal0–P).

The P adsorption was characterised using the method ofHasemen et al. (1950). Briefly, 1 g of soil was equilibratedfor 24 h with 20 ml 0.01 M CaCl2 solution with different Pconcentrations (0 to 50 mg l−1 as KH2PO4). The adsorptionisotherms were described using the Langmuir equation.

Y ¼ a� b� X= l þ bXð Þ ð2Þwhere Y is the amount of P adsorbed in the soil at anequilibrium P concentration in soil solution, X; a and b arethe maximal adsorptive capacity (adsorption maxima) inmg P kg−1 soil and a parameter to show the P-bondingenergy (Sharma et al. 1995), respectively. The b is equal tothe reciprocal of the equilibrium P concentration at one-halfsaturation on the P fixing sites (Olsen and Watanable 1957).

The values of a and b were calculated using the trans-formed Langmuir Eq. 2.

X=Y ¼ X=aþ 1= a� bð Þ ð3ÞThe supply capacity (releasing rate) of P was determined

using the method of Cooke (1966). The soil was shakenwith an anion exchange resin (No. 717 Huachang Polymer,Shanghai) at 25±1°C for various durations from 0 to120 min. The soil suspension with the resin was sievedthrough the 80-mesh screen. The P in the resin was thenextracted with 0.5 M HCl. The supply capacity (R) wascalculated according to the empirical equation of Cooke(1966).

P ¼ Rt1=2 þ B ð4Þ

where P is the amounts of P (mg kg−1) released in time tmin, and B is the initial P concentration.

Statistical analysis

The data for Fig. 1 were analysed using an analysis ofvariance with SAS 9.0 software (SAS Institute 2005). Allsignificance tests were made with the shortest significantranges (SSR) test at a 0.05 significance level. The standarddeviation was used for other measurements.

Results

The basic properties of soils are listed in Table 1 and shownsome differences between the treatments. Organic C andtotal N were highest in the NPM treatment, followed by theNE treatment, and lowest in the bare land. The NE andNPM treatments had higher while the other treatments hadlower organic C and total N than those in 1985. Total Kwas kept relative constant over time and between thetreatments except that the NPM treatment had a higher totalK than others. The CK had the lowest and the NPMtreatment had the highest available N. The available K washighest under the natural ecosystem and lowest in the NPtreatment due to net crop removal. Soil pH was lower in thefertilized agroecosystem than other treatments. The bulkdensity was higher in the bare land and no-fertilizer controlthan in the other treatment, and it was negatively related tothe content of organic matter.

Crop yield and P budget under agroecosystem

Under the agroecosystem with a rotation of corn–soybean–wheat, the grain yield of the corn crop receiving chemicalfertilizers generally increased with time from 1985 to 1994and then plateaued at around 9 t ha−1 (Fig. 1a). The yields

Biol Fertil Soils (2007) 44:37–47 39

of soybean and wheat receiving chemical fertilizers alsotended to increase over time with average yields of 1.9 and2.6 t ha−1 for soybean and wheat, respectively. However,the yield increases over time for wheat and soybean werenot as marked as for the corn. Withholding chemical

fertilizers since 1994 (CK) decreased the grain yield ofcorn but not of wheat or soybean (Fig. 1a). Compared withchemical fertilizers alone (NP), the combined application ofchemical fertilizer and pig manure (NPM) increasedaverage yields of corn and soybean but not wheat.

Fig. 1 Grain yields (a), shootbiomass production (b) and Premoval (c) of wheat (W), soy-bean (S) and corn (C) grownduring 1985–2005 in the agro-ecosystem without fertilizer ap-plication since 1994 (CK), andwith N and P fertilization (NP)and NP fertilizer plus pig ma-nure (NPM). Treatments underthe agroecosystem commencedin 1994 before which the plotsreceived N and P fertilizers.Phosphorus removal was esti-mated from grain yields andshoot biomass. Error bars repre-sent l.s.d. at P=0.05 for indi-vidual crops during 1994–2005

40 Biol Fertil Soils (2007) 44:37–47

The effects of time and withholding chemical fertilizeron the shoot biomass and P removal followed the samepattern as the effects on grain yields (Fig. 1b and c).Compared with chemical fertilizers alone, the application ofpig manure did not further increased shoot biomass of cornor soybean but increased wheat biomass (Fig. 1b), indicat-ing that manure application increased the harvest index forcorn and soybean but decreased it for wheat. Comparedwith the NP, the application of pig manure (NMP) did notfurther increased P removal by corn but tended to increaseit by wheat in 1996 and soybean in 1995, 2001 and 2004(Fig. 1c). On average, corn removed the highest amount ofP, followed by soybean, and wheat the lowest.

During 1985–2005, the no-fertilizer control (CK) hadtotal P input of 198 kg ha−1. The total P input was 2.7 timesgreater in the fertilizer treatment (NP) and 4.9 times greaterin the manure treatment (NPM; Table 2). In comparison, theP removal in crop products was 18 and 23% greater in theNP and NPM treatments, respectively, as compared with Premoval in the CK (Table 2). As a result, the CK had a netP loss of 174 kg ha−1, whereas the NP had a net gain of96 kg ha−1 and the NPM had 504 kg ha−1. The bare landand natural ecosystem did not have P input or removal fromthe systems (Table 2). The P balance calculated using thebulk density and total P in 0–20 cm ranged from −81 kgha−1 for the BE to 733 kg ha−1 for the NPM treatment.

Although there are some discrepancies, the calculated Pbalance is in the same order of magnitude as the net P input(Table 2).

Total, Olsen and organic P in soil

Total P content in soils sampled at 0–20 cm differed betweendifferent ecosystems (P<0.01; Fig. 2). Total P in the naturalecosystem (NE) was 18% greater than the bare land (BE).Where P fertilizers were withheld from 1994 (CK), total Pwas greater than the BE but lower than the NE system. Incomparison, the continuous application of chemical fertil-izers increased total P by 17%, and manure applicationdoubled total P as compared with the CK. The NE had thesame total P as the initial value of the soil sampled in 1985(757 mg kg−1). The BE and CK had lower total P whereasthe NP and NPM had higher than this initial value.

The effect of ecosystem and fertilizer application onOlsen P was more pronounced than the effect on total P(Fig. 2b). The BE had the lowest while the NPM had thehighest Olsen P. The CK had twice much Olsen P as the BEtreatment, indicating that application of fertilizers during1985–1993 have a positive effect on soil P supply in 2005.Compared with the initial value of 21 mg kg−1, Olsen Pdecreased with time in the BE, NE and CK treatments butincreased in the other two treatments (Fig. 2b).

Table 1 The basic physical and chemical properties of soils sampled in 1985, and in 2005 under the bare land, natural ecosystem andagroecosystem without fertilizer application since 1994 (CK), and with N and P fertilization (NP) and NP fertilizer plus pig manure (NPM)

Treatments Organic C(g kg−1)

Total N(g kg−1)

Total K(g kg−1)

Available N(mg kg−1)

Available K(mg kg−1)

pH(H2O)

Bulk density(g cm−3)

1985 sample 26.9 2.00 24.1 224 191 6.1 0.95BE (bare land) 23.8 1.78 24.0 222 164 6.1 1.06NE (naturalecosystem)

29.4 2.18 23.5 220 183 6.2 0.95

CK (agroecosystem) 25.6 1.75 23.2 180 140 6.3 1.03NP (agroecosystem) 27.8 1.95 24.4 210 110 5.9 0.97NPM (agroecosystem) 32.1 2.45 26.0 231 174 5.8 0.92

The ecosystem treatments commenced in 1985. The treatments under agroecosystem commenced in 1994 before which the plots received N and Pfertilizers

Table 2 Total P input, estimated P removal by crops and P balance during 1985–2005 under bare land, natural ecosystem and agroecosystemwithout fertilizer application since 1994 (CK), and with N and P fertilization (NP) and NP fertilizer plus pig manure (NPM)

Treatments P input (kg ha−1) P removal (kg ha−1) Net P input (kg ha−1) P balance (kg ha−1)BE (bare land) 0 0 0 −81

NE (natural ecosystem) 0 0 0 −10CK (agroecosystem) 198 373 −174 −17NP (agroecosystem) 538 442 +96 129NPM (agroecosystem) 963 459 +504 737

Treatments under agroecosystem commenced in 1994 before which the plots received N and P fertilizers. The P balance was calculated using soilbulk density and total P in 0–20 cm.

Biol Fertil Soils (2007) 44:37–47 41

The NE had the highest organic P, followed by NPM,NP and CK, and the BE had the lowest (Fig. 2c). Organic Pas percent total P ranged from 42 to 69%. The BE, NE andCK had similar organic P as percent total P, which waslower in the NP treatment. Interestingly, the NPM had thelowest portion of organic P to total P (Fig. 2d), although ithad the second highest content of organic P among thetreatments.

Inorganic P fractions under different ecosystems

The amounts of Ca2–P and Ca8–P in the three systemsand the fertilizer treatments under the agroecosystemfollowed the same pattern as the Olsen P, in order ofNPM > NP > CK > NE > BE (Fig. 3). The CK soil underthe agroecosystem had the least amounts of Al–P and Fe–P.The continuous application of N and P fertilizers and pigmanure substantially increased Al–P and Fe–P compared tothe BE and NE systems where there were no removal orinput of P. The occluded P was 9% lower in the CK and11% higher in the NPM than the other treatments. Theamount of Ca10–P was lowest in the BE and highest in theNPM but was similar in the other treatments (Fig. 3).Among the inorganic P, the percentage of Ca2–P, Ca8–P andAl–P increased, whereas the percentage of Fe–P, occludedP and Ca10–P decreased with increasing P input into thesystem (Fig. 4).

Phosphorus characteristics under different ecosystems

The soils from the five treatments differed greatly withrespect to their P sorption behaviour. The soil from the CKhad the strongest P adsorption, followed by those from theNE, NP and BE, and the soil from the NPM had theweakest (Fig. 5). The P concentration of equilibriumsolution was within the range of 0–40 mg l−1, and thequantity of P adsorbed by soil increased along with the Pconcentration of equilibrium solution. The P adsorptionisotherm line of each treatment was fitted well with theLangmuir equation (R2=0.94–0.97). The P adsorptionmaxima and bonding energy were then calculated accord-ing to the Eq. 2. The NPM treatment had the lowestadsorption maxima while the bare land had higheradsorption maxima than the other three treatments. Incontrast, the CK and NE had the highest bonding energyfollowed by the CK and NPM, whereas the NP had thelowest. The degrees of P saturation (DPS) markedlyincreased as the P input increased in the system (Table 3).

The amounts of P released from soil increased with time,and P released faster in the first 20 min (Fig. 6). The effectof system and fertilizer treatment on P release displayeddifferent pattern from that on P adsorption; P release wasgreatest in the soil from the NPM treatment and lowest

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Fig. 2 Total P (a), available P (Olsen P; b), organic P (c) andpercentage of organic P (d) in soils sampled in 2005 under bare land(BE), natural ecosystem (NE) and agroecosystem without fertilizerapplication since 1994 (CK), and with N and P fertilization (NP) andNP fertilizer plus pig manure (NPM). Treatments under agroecosystemcommenced in 1994 before which the plots received N and P fertilizers.The dotted line indicates initial P content before treatment in 1985.Error bars are the standard deviation of means of four replicates

42 Biol Fertil Soils (2007) 44:37–47

from the BE and NE systems. When the amounts of Preleased are plotted against t1/2, the slope (R) of theregression line provides an index of P supply capacity.Clearly, the P supply capacity increased with increasing Pinput into the system with the BE being the lowest and theNPM the highest (Table 3), which correlated well with theOlsen P.

Discussion

Phosphorus balance and fertility

Where no P had been applied for 20 years, the soil underthe natural ecosystem had higher total P and a lowernegative P balance than the bare land. The greater negativeP balance in the BE than in the NE treatment might resultfrom greater surface runoff in the bare land and thus higher

P losses during wet seasons. The results suggest that thenative grasses had taken up P from deeper soil layers andaccumulated it in the topsoil through the deposit andaccumulation of plant residues. It is evident that organicmatter was higher in the NE than the BE treatment, and thattotal P in the NE was similar in soils sampled in 1985 andin 2005. Furthermore, the higher bulk density in the BEthan the NE treatment meant that soil samples from the BEtreatment had a higher portion of subsoil while subsoilgenerally contained a much lower P than the topsoil (Han etal. 2005a). The results from this study also suggest that thenatural ecosystem can sustain P level in the soil. Incomparison, the Olsen P had been decreased from theinitial value of 21 to less than 10 mg kg−1 over the 20 years.The reason for this is unknown. A previous studydemonstrated that P vertical movement was limited in thissoil (Han et al. 2005a), and thus, a leaching loss is unlikelyto be a cause. The decrease in Olsen P over time cannot be

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Fig. 3 Phosphorus fractions ofsoils sampled in 2005 under thebare land (BE), natural ecosys-tem (NE), and agroecosystemwithout fertilizer applicationsince 1994 (CK), and with Nand P fertilization (NP) and NPfertilizer plus pig manure(NPM). Treatments under agro-ecosystem commenced in 1994before which the plots receivedN and P fertilizers. Error barsare the standard deviation ofmeans of four replicates

Biol Fertil Soils (2007) 44:37–47 43

explained by the transformation of available to lessavailable P forms (Fig. 3). One plausible explanation isthat the soils of these two treatments (BE and NE) had notbeen disturbed by cultivation and might have built upmicrobial biomass (Drijber et al. 2000), which couldtemporarily immobilize P from the available pool.

In the agroecosystem, both total and Olsen P, andcalculated P balance increased with increasing net P inputs.The higher values of calculated P balance than the net Pinput (Table 2) had most probably resulted from plantuptake of P from the subsoil. The continuous application ofchemical fertilizers alone (NP) and in combination with the

animal manure (NPM) clearly had a P surplus, and thus, theapplication rates should be reduced to minimize a possiblenegative impact on the environment without sacrificing theproduction. Where the chemical fertilizers were appliedduring 1985–1993 but were withheld thereafter (CK), totalP was lower than that in the NE but higher than that in theBE treatment. The Olsen P was halved compared to theinitial value, and dropped to below the critical levels of 15–24 mg kg−1 (Reuter and Robinson 1997). Although the cropyields were lower in the CK than in the other treatments,withholding chemical fertilizers could still sustain the cropyields over 10 years, indicating that the soil still had thecapacity of supplying nutrients, particularly P, to the crops.The changes in P fertility over time are in agreement withfindings of other long-term studies (e.g. Motavalli andMiles 2002; Shen et al. 2004).

Phosphorus fractions and transformation

The fractions are strictly empirical and overlap to someextent, but roughly correspond to the several P pools. TheCa2–P represents monocalcium phosphate and dicalciumphosphate equivalents that are readily available to plants.The Ca8–P represents a group of phosphates with chemicalstructure similar to Ca8H2(PO4)6·nH2O and can be partlyavailable to plants. The Al–P and Fe–P represent alumin-ium phosphates and iron phosphates, respectively, and havelow availability to plants. The Ca10–P represents a group ofphosphates with chemical structure similar toCa10(PO4)6·(OH)2 that is considered to be unavailable toplants (Jiang and Gu 1989). The soil had a high proportionof organic P, ranging from 42 to 69% of total P, which isprobably related to the high content and slow decomposi-tion of organic matter in the soil with the cold climate of theregion. Among the inorganic pools, Al–P, Fe–P andoccluded P are three major fractions in the soil. They aresparingly soluble sources with availability to the plants inorder of Al–P > Fe–P > occluded P (Shen et al. 2004; Hanet al. 2005b). Whereas the bare land (BE) had the lowestCa2–P, Ca8–P and Ca10–P, it is interesting to note that theno-fertilizer control (CK) had the lowest Fe–P and occludedP. The results imply that when P is not supplied, the cropplants are able to access these sparingly soluble pools fromthe soil. Alternatively, the plant uptake had resulted in aconsiderable decrease in Olsen P with time, which wouldenhance dissolution of the sparingly soluble P. This issupported by the fact that the changes over time in availableP were more sensitive than the changes in total P tocontinuous P fertilization and depletion by plant uptake(Fig. 2). In albic luvisols, the initial concentrations of Fe–P,Al–P and Ca–P correlated significantly (P<0.05) with cornshoot biomass (Han et al. 2005b). Similar results were alsoobserved in a Vertisol (Tang et al. 2006). In a calcareous

Fig. 4 Percent (%) of various inorganic P fractions of soils sampled in2005 under the bare land (BE), natural ecosystem (NE), andagroecosystem without fertilizer application (CK), and with N and Pfertilization (NP) and NP fertilizer plus pig manure (NPM)

0

50

100

150

200

250

300

350

400

450

0 5 10 15 20 25 30 35 40

Qu

antit

y o

f P a

dso

rptio

n (m

g k

g-1

)

BE

NE

CKNP

NPM

0

50

100

150

200

250

300

350

400

450

0 5 10 15 20 25 30 35 40

P concentration of equilibrium solution (mg L-1)

Qu

antit

y o

f P a

dso

rptio

n (m

g k

g-1

)

BE

NE

CKNP

NPM

BE

NE

CKNP

NPM

Fig. 5 Langmuir P adsorption isotherms of soils sampled in 2005under the bare land (BE), natural ecosystem (NE), and agroecosystemwithout fertilizer application (CK), and with N and P fertilization (NP)and NP fertilizer plus pig manure (NPM)

44 Biol Fertil Soils (2007) 44:37–47

soil where no P was applied, concentrations of Ca–P, Fe–P,Al–P and occluded P had all decreased with time over14 years of rice cultivation although Ca2–P and Ca8–Pdepleted faster, parallel to the depletion of Olsen–P (Shen etal. 2004). It is suggested that P compounds in sparinglysoluble fractions can be transformed to more soluble forms,or insoluble compounds are dissolved under depletion ofsoil P.

With increasing P inputs, the Ca–P and Al–P increased,whereas the Fe–P and occluded P decreased. The contin-uous supply of chemical P for 20 years under theagroecosystem increased the Olsen P by 74% and hadincreased and sustained crop production. All P fractionsexcept the occluded P were increased in this treatment,

suggesting that the applied P had been transferred to thesefractions including sparingly soluble forms. An excessiveapplication of chemical P fertilizers over crop demandscould thus decrease the use efficiency of P fertilizers andshould be avoided.

Phosphorus sorption and release

The application of animal manure is a common practice anda cheap way to improve soil fertility in many countries,particularly in developing countries where the farmerscannot afford to purchase large quantities of chemicalfertilizers (Haynes and Mokolobate 2001). This studyclearly demonstrated that the application of pig manuremarkedly decreased P adsorption and increased P supplycapacity. In other studies, the long-term application ofanimal manure also increased Olsen P and decreased Psorption (Sharpley et al. 1984; Motavalli and Miles 2002;Allen and Mallarino 2006).

The long-term application of the pig manure might havecontributed the decreased P adsorption in three ways. First,the long-term application of manure being a source of P hadclearly over supplied P than crop demands (Table 2), andthus, the surplus P would have saturated a portion of Pfixing sites on the surface of clay colloids. This is supportedby the data of the lowest adsorption maxima and the highestdegree of P saturation. It is also evident from this study thatboth labile and non-labile P fractions had been increasedwith manure addition (Fig. 3). Second, the organiccompounds in the manure directly compete with P for thesorption sites (Guppy et al. 2005). Further, organic matterreleases large amounts of organic acids when decomposedby the microorganisms. Organic acids can complex Fe, Aland Ca and thus mobilize sorbed P.

The application of pig manure also improved the Psupply capacity of the soil that is associated with high

Table 3 Adsorption maxima, bonding energy, release rate, DPS and supply capacity of P in soils under bare land, natural ecosystem andagroecosystem without fertilizer application since 1994 (CK), and with N and P fertilization (NP) and NP fertilizer plus pig manure (NPM)

Treatments Adsorption maximaa

(a; mg kg−1)Bonding energya

(b; ml mg−1)DPSb (%) Supply capacityc

(R; mg P kg−1 min−1/2)Initial concentrationc

(B; mg P kg−1 soil)

BE (bare land) 357 0.269 1.4 0.32 8.0NE (natural ecosystem) 476 0.145 1.3 0.95 4.3CK (agroecosystem) 476 0.193 2.3 1.68 7.6NP (agroecosystem) 455 0.135 6.0 3.21 16.5NPM (agroecosystem) 238 0.178 51.2 12.46 41.9

Treatments under agroecosystem commenced in 1994 before which the plots received N and P fertilizers.a Adsorption maxima (a) and bonding energy (b) are calculated from the Langmuir equation: Y ¼ a� b� X= 1þ bXð Þ, where X and Y representadsorbed P and solution P at equilibrium, respectively

b The DPS is calculated as Olsen P as a percentage of P sorption capacity (adsorption maxima) derived from the P sorption isotherm (Börling et al.2004)

c Supply capacity (R) and initial concentration (B) of soil P are calculated according to the equation (Cooke 1966); P ¼ Rt1=2 þ B, where P is theamount of P released from the soil at t time

0

40

80

120

160

200

0 20 40 60 80 100 120

Time of P release (min)

BENECK

NPNPM

Am

ou

nt

of

P r

elea

sed

(m

g k

g-1

soil)

0

40

80

120

160

200

0 20 40 60 80 100 120

Time of P release (min)

BENECK

NPNPM

Am

ou

nt

of

P r

elea

sed

(m

g k

g-1

soil)

Fig. 6 Relationship between the amount of P released and releasingtime of soils sampled under the bare land (BE), natural ecosystem(NE), and agroecosystem without fertilizer application since 1994(CK), and with N and P fertilization (NP) and NP fertilizer plus pigmanure (NPM)

Biol Fertil Soils (2007) 44:37–47 45

degree of P saturation and initial concentration (Table 3).There are three reasons for the increased P supply capacityby the manure. First, the application of the manureincreased total P input. The organic P in the manureappeared to be effectively mineralized by microorganismsand thus transferred into various inorganic P pools,particularly available P pools (Figs. 2 and 3). The contentof organic P was higher after 12 years of application of pigmanure compared to the CK and NP treatments, whereasthe proportion of organic P as percent total P was virtuallythe lowest. Second, added organic matter might havedecreased specific adsorption of P onto the soil colloids asdiscussed above so that the released P from organic matteror newly applied P were more available to plants. Third, ahigh P saturation on the sorption sites meant that largequantities of P would have been released upon the depletionof P in soil solution.

The soil in the manure-amended treatment released thehighest amounts of P. The high P release and high Olsen Pmight increase the risk of P loss from the system. Althoughthe vertical movement of P was minimal in this soil type(Han et al. 2005a), a substantial P surplus was observed inthe NPM treatment. Based on current crop yield and Premoval, only less than half of the annual application ratesin the NPM treatment are required to sustain the P output.

The other treatments showed a much greater P adsorp-tion and lower release capacity than the manure treatment.Where no P had been added, the soils (BE, NE and CK)released little P over time (Fig. 6), and were unable toreplenish P in soil solution upon depletion. The BE soil hadthe highest P bonding energy but a low adsorption maxima,indicating that the P supply of this soil is mediated by thetype of adsorption rather than total number of fixing sites.The reason for the high P bonding energy and lowadsorption maxima of this soil is unknown, but it may berelated to the type and content of organic matter. Organicmatter, on the one hand, protects P from adsorption oninorganic colloids when P in soil solution is available. Onthe other hand, organic matter is a source of fixing sites(functional groups). The BE soil had the lowest content oforganic matter, and had not received fresh organic materialsfor 20 years, and thus, the organic matter was probably lessactive than that of the other treatments. The continuousapplication of inorganic P fertilizers (NP) resulted in a net Pgain, and led to a low bonding energy and increased Psupply capacity and saturation. The results are consistentwith previous long-term studies on different soil types(Börling et al. 2004; Allen and Mallarino 2006).

In conclusion, the black soil was generally fertile andcould sustain P supply under both natural and currentagricultural ecosystems. In the natural ecosystem, the nativevegetation appeared to redistribute P in the soil profile,from deeper soil layers to the topsoil, and might store the

labile P in organic forms. In the agroecosystem, whileexcessive applications of chemical P fertilizers increasedboth available and unavailable P fractions but did notsignificantly decreased P adsorption, the use of the pigmanure clearly decreased P adsorption and increased Prelease. The current rates of chemical and organic P used inthis study obviously exceed the crop demands, and shouldbe at least halved in the NPM system. Although the verticalmovement of P is minimal in this soil type, the available P(Olsen-P) had decreased over time in the bare land andnatural ecosystems. It is unknown whether the decreasedavailable P is a result of P loss through surface runoffduring wet seasons. Further studies with this respect arerequired.

Acknowledgment This research was supported by the KnowledgeInnovation Project of Chinese Academy of Sciences (KSCX2-YW-N-002) and the National Basic Research Program of China(2005CB121101). We thank Professor G X Pan for soil taxonomy,and the editor and two anonymous referees for their constructivecomments.

References

Allen BL, Mallarino AP (2006) Relationships between extractable soilphosphorus and phosphorus saturation after long-term fertilizeror manure application. Soil Sci Soc Am J 70:454–463

Barrow NJ (1983) On the reversibility of phosphate sorption by soil.J Soil Sci 34:751–758

Börling K, Otabbong E, Barberis AP (2004) Soil variables forpredicting potential phosphorus release in Swedish noncalcareoussoils. J Environ Qual 33:99–106

Bremner JM (1996) Nitrogen-total. In: Sparks DL (ed) Methods ofsoil analysis: Chemical methods, Part 3. Soil Science Society ofAmerica, Madison, WI, pp 1085–1121

Chang SC, Jackson ML (1957) Fractionation of soil phosphorus. SoilSci 84:133–144

Cooke IJ (1966) A kinetic approach to the description of soilphosphate status. J Soil Sci 17:56–64

Daniel TC, Sharpley AN, Lemunyon JL (1998) Agriculturalphospho-rus and eutrophication—a symposium overview. J Environ Qual27:251–257

Drijber RA, Doran JW, Parkhurst AM, Lyon DJ (2000) Changes insoil microbial community structure with tillage under long-termwheat–fallow management. Soil Biol Biochem 32:1419–1430

Fox RL, Kamprath EJ (1970) Phosphate sorption isotherms forevaluating the phosphate requirements of soils. Soil Sci SocAm Proc 34:902–906

Guppy CN, Menzies NW, Moody PW, Blamey FPC (2005)Competitive sorption reactions between phosphorus and organicmatter on soil: a review. Aust J Soil Res 43:189–202

Han XZ, Song CY, Wang SY, Tang C (2005a) Impact of long-termfertilization on phosphorus status in black soil. Pedosphere15:319–326

Han XZ, Tang C, Song CY, Wang SY, Qiao YF (2005b) Phosphoruscharacteristics correlate with soil fertility of albic luvisols. PlantSoil 270:47–56

Hasemen JF, Brown EF, Whitt CD (1950) Some reactions ofphosphate with clays and hydrous oxides of iron and aluminum.Soil Sci 70:257–271

46 Biol Fertil Soils (2007) 44:37–47

Haynes RJ, Mokolobate MS (2001) Amelioration of Al toxicity and Pdeficiency in acid soils by addition of organic residues: a criticalreview of the phenomenon and the mechanisms involved. NutrCycl Agroecosyst 59:47–63

Hedley MJ, Stewart JWB, Chauhan BS (1982a) Changes in inorganicand organic soil phosphorus fractions induced by cultivationpractices and by laboratory incubations. Soil Sci Soc Am J46:970–976

Hedley MJ, White RE, Nye PH (1982b) Plant-induced changes in therhizosphere of rape (Brassica napus var. Emerald) seedlings. III.Changes in L value, soil phosphate fractions and phosphataseactivity. New Phytol 91:45–56

Hughes S, Reynolds B, Bell SA, Gardner C (2000) Simple phosphorussaturation index to estimate risk of dissolved phosphorus in runofffrom arable soils. Soil Use Manage 16:206–210

Jiang BF, Gu YC (1989) A suggested fractionation scheme ofinorganic phosphorus in calcareous soils. Sci Agric Sin 22:58–66

Kuo S (1996) Phosphorus. In: Sparks DL (ed) Methods of soilanalysis: chemical methods. Part 3. Soil Science Society ofAmerica, Madison, WI, pp 869–919

Legg JO, Black CA (1955) Determination of organic phosphorus insoils. II. Ignition method. Soil Sci Soc Am Proc 19:139–143

Motavalli PP, Miles RJ (2002) Soil fractions after 111 years of animalmanure and fertilizer application. Biol Fertil Soils 36:35–42

Nelson DW, Sommers LE (1996) Total C, organic C, and organic matter.In: Sparks DL (ed)Methods of soil analysis: chemical methods. Part3. Soil Science Society of America, Madison, WI, pp 961–1010

Olsen SR, Watanable KS (1957) A method to determine a phosphorusadsorption maximum of soil as measured by the Langmuirisotherm. Soil Sci Soc Am Proc 21:144–149

Reuter DJ, Robinson JB (1997) Plant analysis: an interpretationmanual. CSIRO Publishing, Collingwood

Sharma KN, Singh H, Vig AC (1995) Influence of continuouscropping and fertilization on adsorption and desorption of soilphosphorus. Fert Res 40:121–128

Sharpley A (2000) Phosphorus availability. In: Sumner EM (ed)Handbook of soil science. CRC, New York, pp D18–D37

Sharpley AN, Smith SJ, Stewart BA, Mathers AC (1984) Forms ofphosphorus in soil receiving cattle feedlot waste. J Environ Qual13:211–215

Shen J, Li R, Zhang F, Tang C, Rengel Z (2004) Crop yields, soilfertility and phosphorus fractions in response to long-termfertilization under the rice monoculture system on a calcareoussoil. Field Crops Res 86:225–238

Sui Y, Thompson ML, Shang C (1999) Fractionation of phosphorus ina Mollisol amended with biosolids. Soil Sci Soc Am J 63:1174–1180

Tang C, Dart L, Rogers C, Vu DT, Armstrong RD (2006) Phosphorusfractions in a Vertosol after 88-year crop rotations. In: AlvesVMC, Guimarães CT, de Magalhães JV, Schaffert RE, CoelhoAM, de Castro Bahia Filho AF, Santana DP (eds) Proceedings ofthe third international symposium on phosphorus dynamics in thesoil–plant continuum. Embrapa Milho e Sorgo, Sete Lagoas,Brazil, pp 67–68

Biol Fertil Soils (2007) 44:37–47 47