agronomic measures for better utilization of soil and fertilizer phosphates

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Agronomic measures for better utilization of soil and fertilizer phosphates Konrad Mengel* Institute of Plant Nutrition Justus Liebig University, Su ¨danlage 6, D 39390 Giessen, Germany Accepted 16 June 1997 Abstract Global known phosphate deposits are a finite resource which will run out in about four centuries at the present consumption rate. Since about 90% of the phosphate mined is used for fertilizer, soil and fertilizer phosphate should be efficiently used. Various agronomic measures are discussed relevant for saving phosphate and avoiding losses. Phosphate fertilizer rates should be adjusted to measured requirements for phosphate using soil tests. Particularly in areas with high livestock intensities soils frequently are much enriched in available phosphate and do not need further phosphate application whether in organic or in inorganic form. Excessively high levels of available soil phosphate, much higher than required for optimum crop production increase the hazard of phosphate loss by wind and water erosion and even leaching. Loss of plant available phosphate in soils occurs by phosphate fixation which is especially strong in acid mineral soils. Such losses can be dramatically reduced by liming soils to a pH of 6–7. In tropical areas where lime frequently is not available row placement of phosphate fertilizer is recommended. Oxisols with a very low pH liming, however, may promote phosphate fixation due to the formation of phosphate adsorbing Al complexes. Biological assimilation of phosphate may prevent inorganic phosphate from fixation by soil particles. Organic anions produced during the decomposition of organic matter in soils as well as the excretion of anions by plant roots depress phosphate adsorption by competing with phosphate for binding sites at the adsorbing surface. Hence farming systems and rotations which bring much organic matter into soils contribute to a better use of soil and fertilizer phosphate. Mycorrhization of plant roots with appropriate fungi ecotypes may essentially improve the exploitation of soil phosphates. The choice of the appropriate phosphate fertilizer type is crucial for its efficient use. This applies particularly for apatitic fertilizers of which the availability is poor in weakly acid to neutral and calcareous soils. 1997 Elsevier Science B.V. Keywords: Phosphate availability; Phosphate fertilizer; Livestock; Farm yard manure; Phosphate reserves; Phosphate fixation; Ca phosphates; pH; Liming; Mycorrhiza; Cropping systems 1. Introduction Phosphate deposits are finite resources. According to Sheldon (1982) known deposits of phosphate rock will last about 400 years at current rates of exploitation. Werner (1982) distinguishes between three categories of phosphate resources as shown in Table 1. Reserves are phosphate deposits which under the prevailing economic and technological conditions are worth mining. Phosphate resources comprise all known global phosphate deposits including those which under the present conditions cannot be mined for economic and technological reasons. Technologi- cal reasons are mainly the contamination of phosphate European Journal of Agronomy 7 (1997) 221–233 1161-0301/97/$17.00 1997 Elsevier Science B.V. All rights reserved PII S1161-0301(97)00037-3 * Tel.: +49 641 9939161; fax: +49 641 9939199.

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Agronomic measures for better utilization of soiland fertilizer phosphates

Konrad Mengel*

Institute of Plant Nutrition Justus Liebig University, Su¨danlage 6, D 39390 Giessen, Germany

Accepted 16 June 1997

Abstract

Global known phosphate deposits are a finite resource which will run out in about four centuries at the present consumptionrate. Since about 90% of the phosphate mined is used for fertilizer, soil and fertilizer phosphate should be efficiently used.Various agronomic measures are discussed relevant for saving phosphate and avoiding losses. Phosphate fertilizer rates shouldbe adjusted to measured requirements for phosphate using soil tests. Particularly in areas with high livestock intensities soilsfrequently are much enriched in available phosphate and do not need further phosphate application whether in organic or ininorganic form. Excessively high levels of available soil phosphate, much higher than required for optimum crop productionincrease the hazard of phosphate loss by wind and water erosion and even leaching. Loss of plant available phosphate in soilsoccurs by phosphate fixation which is especially strong in acid mineral soils. Such losses can be dramatically reduced byliming soils to a pH of 6–7. In tropical areas where lime frequently is not available row placement of phosphate fertilizer isrecommended. Oxisols with a very low pH liming, however, may promote phosphate fixation due to the formation ofphosphate adsorbing Al complexes. Biological assimilation of phosphate may prevent inorganic phosphate from fixationby soil particles. Organic anions produced during the decomposition of organic matter in soils as well as the excretion ofanions by plant roots depress phosphate adsorption by competing with phosphate for binding sites at the adsorbing surface.Hence farming systems and rotations which bring much organic matter into soils contribute to a better use of soil and fertilizerphosphate. Mycorrhization of plant roots with appropriate fungi ecotypes may essentially improve the exploitation of soilphosphates. The choice of the appropriate phosphate fertilizer type is crucial for its efficient use. This applies particularly forapatitic fertilizers of which the availability is poor in weakly acid to neutral and calcareous soils. 1997 Elsevier ScienceB.V.

Keywords:Phosphate availability; Phosphate fertilizer; Livestock; Farm yard manure; Phosphate reserves; Phosphate fixation;Ca phosphates; pH; Liming; Mycorrhiza; Cropping systems

1. Introduction

Phosphate deposits are finite resources. Accordingto Sheldon (1982) known deposits of phosphate rockwill last about 400 years at current rates ofexploitation. Werner (1982) distinguishes between

three categories of phosphate resources as shown inTable 1. Reserves are phosphate deposits which underthe prevailing economic and technological conditionsare worth mining. Phosphate resources comprise allknown global phosphate deposits including thosewhich under the present conditions cannot be minedfor economic and technological reasons. Technologi-cal reasons are mainly the contamination of phosphate

European Journal of Agronomy 7 (1997) 221–233

1161-0301/97/$17.00 1997 Elsevier Science B.V. All rights reservedPII S1161-0301(97)00037-3

* Tel.: +49 641 9939161; fax: +49 641 9939199.

rock with Fe, Al, and/or Mg which disturb the proces-sing, or logistic reasons such as the far remoteness ofdeposits. High Cd concentrations in phosphate rock istoday also a reason for European countries not to use itas fertilizer source (Baechle and Wolstein, 1984).Speculative resources (line 3 in Table 1) are phos-phates not yet discovered and the existence of whichis based on geological hypothesis. This latter categoryalso comprises deposits at great depth and depositswith low P concentrations. Since this category isvery hypothetical, it should not be considered as arealistic phosphate reserve. The longevity of phos-phate deposits shown in Table 1 is based on theassumption that the phosphate consumption rates peryear still increase during the last two decades of the20th century and then remain constant from the begin-ning of the year 2000. According to the FAO FertilizerYearbook the phosphate consumption rates increaseduntil 1988/89 with a peak consumption of 38× 106 t/year and then declined with a minimum consumptionof 29 × 106 t in 1994 followed by an increasing ten-dency. From this trend it is clear that the longevities ofthe reserves and the reserves plus resources are veryshort as compared with the history of mankind andtherefore mining and consumption of phosphatesshould be handled with much care and any waste ofthis resource should be avoided.

About 90% of the phosphate mined is used for theproduction of fertilizers (Werner, 1982). The fertilityof European soils being exhausted of available phos-phate in the last century by cropping without compen-sating for phosphates removed from the soil by crops,was much improved by phosphate fertilizer applica-tion at the end of the last century and in the first half ofthe 20th century (Boulaine, 1992). In developingcountries there are still large areas of agriculturalland with insufficient available phosphate and hencerequire phosphate fertilization particularly under thepressure of an increasing world population. This pre-carious situation demands very careful and economicuse of phosphates.

The flow of phosphate goes from the deposits toagricultural land and from here partially into thecrops which may be eaten by humans and animals.Phosphate in crops consumed by farm animals is lar-gely recycled with farmyard manure or slurry to thesoils. Phosphate in plant parts or in animals and inanimal products exported from the farm is lost for

the farm and in many cases also as potential sourcesof fertilizer phosphate. From the phosphate harvestedin crops a high proportion is discharged into publicwaste systems and not returned to agricultural land. InEurope about 25% of the phosphate excreted by manis used as fertilizer (Winteringham, 1992). In devel-oping countries the proportion of phosphate recycledto agricultural land with human excrements willdecline with the increasing proportion of populationliving in primitive urban societies where recycling ofphosphate in wastes is hardly possible. A considerableamount of available plant phosphate is also lost inagricutural land by a permanent transformation ofsoil phosphates into stable forms which are not avail-able to plant roots. Even phosphate leaching into dee-per soil layers not accessible to roots may occurparticularly in organic soils (Munk, 1972). Deforesta-tion and overgrazing leads to wind and water erosionand therefore also to a loss of phosphates bound to fineorganic and inorganic soil particles. A substantialamount of phosphate in eroded particles and also inurban wastes finally flows into the ocean from where itcannot be recovered (Isermann, 1990).

Saving phosphate is also a question of an efficientuse of soil and fertilizer phosphate by farmers. In thispaper, pertinent agronomic measures for improvingphosphate efficiency are discussed. These measuresare: fertilizing phosphate according to soil tests foravailable phosphate, providing an optimum soil pHfor phosphate availability, using appropriate phos-phate fertilizer types and practicing rotations andfarming systems with crop species capable of mobi-lizing fixed or less soluble soil phosphates.

2. Phosphate fertilizing according to P soil tests

The level of available soil phosphate should meet

Table 1

Phosphate reserves, resources and longevity (Werner, 1982)

P reserves and resources 109 t Longevity,years

Reserves 35 85Reserves+ resources 130 360Reserves+ resources+

hypothetical resources1130 3400

222 K. Mengel / European Journal of Agronomy 7 (1997) 221–233

the demand of crops but should not be much higherthan the optimum since otherwise major losses ofavailable phosphate may occur. In this context theterm available means phosphate which is accessibleto and can be taken up by plant roots. Loss by run offof available soil phosphate with soil particles (Sharp-ley, 1993) will be higher when soils are richer inavailable phosphate. The same is true for the hazardof leaching of phosphate out of the rooting zone whichmay occur in organic soils (Munk, 1972) and in sandysoils particularly if overloaded with fertilizer phos-phate (Isermann, 1990; Mozaffari and Sims, 1996;Peters and Basta, 1996). Consequently levels of avail-able phosphate in soils which are above the optimumrequirement for crop growth lead to a dissipation ofphosphate and hence should be avoided.

In the last five decades a remarkable number of Psoil test methods has been developed which apply tovarious soil types (Hesse, 1971). In the following,particular investigations were carried out in Germanyin which the ‘DL method’ was used. DL denotes dou-ble lactate since soils are extracted with a Ca lactatesolution brought to a pH of 3.6 by the addition of HCl(Egner, 1955; Hoffmann, 1991). Numerous earlier(Schwerdt and Jessen, 1961) and more recent fieldtrials (Brune and Heyn, 1984) with arable cropshave shown that the DL-method is a reliable soiltest precisely indicating the available soil phosphate.Only in cases in which soils were fertilized with rockphosphates the DL extract yields data which arehigher than the actual available soil phosphate (Wer-ner, 1969). For such soils the ‘CAL method’ is recom-mended. Although reliable soil tests for availablephosphate are at disposition regular P soil testing cov-ers only a limited percentage of agricultural land. InGermany with about 17× 106 ha agricultural landabout 600 000 P soil tests are made per year whichrepresent only a small percentage of agricultural land(information from VDLUFA, Association of the Ger-man Research Stations). It is supposed that many soilsare enriched in available phosphate and crops do notrespond to further P fertilization as was reported byArnold and Shepherd (1990) quoted after Bhogal etal., 1996) for UK. The same is true for areas withintensive livestock husbandry (Leinweber, 1996;Mozaffari and Sims, 1996; Peters and Basta, 1996).Fertilizing these soils wastes phosphate. Leinweber etal. (1994), taking representative soil samples from an

area in north Germany with intensive livestock hus-bandry, found low to medium DL-P concentrations inforest soils while far more samples from arable landand grassland showed high to extremely high DL-Pconcentrations. The frequency distribution of DL-P ofLeinweber’s investigation is shown in Fig. 1 for thevarious cropping systems. About 95% of the samplesfrom grassland, arable land and special cultures,mainly raspberries and asparagus, had DL-P concen-trations which were higher than the level above whichcrops do not respond to P fertilizer application. Inthese soils, heavily treated with slurries, phosphateis not only enriched in the top layer but also in deepersoil layers up to 1 m (Werner et al., 1988). Since cropsalso feed from phosphate in deeper layers of the root-

Fig. 1. Frequency of distribution of available phosphate in NorthernGermany in an area with intensive livestock husbandry (Leinweberet al., 1994). Available phosphate measured by the extraction witha lactate solution (DL method, Egner, 1955). A concentration of100 mg DL soluble P/kg soil may be considered as sufficient forarable crops. Special cultures are mainly raspberries and asparagus.

223K. Mengel / European Journal of Agronomy 7 (1997) 221–233

ing zone this deeper located available phosphate mustbe taken into consideration when assessing the quan-tity of available soil phosphate. The problem of phos-phate surplus in agricultural land is comprehensivelydiscussed by Isermann (1993). Spiertz (1991) reportedthat on average, milking farms in the Netherlands hadan excess of 30 kg P/ha per year which lead to anenormous accumulation of P in soils. To reduce theP fertilization in such farms is not easy since the P isimported into farms with the concentrates required forfeeding the high livestock rates and farmers need thishigh intensity for making their living because theirown acreage for forage production is not sufficient.Under environmental aspects and the aspect that phos-phate is a finite resource, a solution must be found forthese farms.

3. Phosphate fixation

The term phosphate fixation means the transforma-tion of plant available phosphate in soils into a non-available form. Two major processes may be involvedin this transformation: the formation of less soluble Caphosphates from water soluble phosphates and theadsorption of phosphate to the surfaces of soil parti-cles. The latter process is the most important. In thiscontext the term phosphate fixation includes phos-phate occlusion brought about by adsorption by FeIII

oxides and oxyhydroxides.Formation of less soluble Ca phosphates follows

the sequence: Ca dihydrogen phosphate. Ca mono-hydrogen phosphate. Ca octophosphate. apatite,from which Ca dihydrogen phosphate is most solubleand apatite sparingly soluble in water (Olsen et al.,1977; Sposito, 1989). The reaction sequence to lesssoluble phosphates is promoted by high pH and highCa2+ concentrations in the soil solution whereas highH+ and low Ca2+ concentrations have an inverse effect.It is doubtful whether even under favorable conditionssuch as in calcareous soils with high pH and high Ca2+

concentrations in the soil solution the crystalline apa-tite is formed. At least this process of crystalline Caphosphate formation proceeds at low rates (Parfitt,1978). According to Olsen et al. (1977) it is the octo-phosphate which accumulates in soils with higher soilpH. The solubility of octophosphate is high enoughfor optimum plant supply (Olsen et al., 1977; Sposito,

1989). Therefore, the formation of less soluble Caphosphates does not represent a major process inphosphate fixation.

Uptake and metabolization of inorganic phosphateby microorganisms means a transient reduction ofplant-available phosphate. Assimilation of inorganicphosphate is paralleled by the formation of inorganicphosphates from organic phosphate which partiallyoriginates from dead microbial biomass. Particularlyin the rhizosphere there is a high turnover of organicphosphates into inorganic phosphate (Helal andSauerbeck, 1984) mediated by the relatively highphosphatase concentrations near the root surface (Tar-afdar and Jungk, 1987; Helal and Dressler, 1989).

The most important process of phosphate fixation isrepresented by the specific adsorption of phosphate tosoil particles such as sesquioxides, clay minerals, allo-phanes, calcite as well as Al and Fe humate com-plexes. This so called chemi-adsorption occurs byligand exchange in which the OH− on the adsorbingsurface is exchanged by a phosphate anion (Fig. 2). Inthe first step the phosphate is bound only with onebond to the surface (mononuclear bond) in the follow-ing step a second anion equivalent of the phosphate isbound to the surface (binuclear bond) the latter beingmuch more stable than the mononuclear bond (Parfitt,1978). The adsorption process is promoted by low

Fig. 2. Principle of phosphate adsorption onto an adsorbing surface.(1) Ligand exchange between the OH− of the surface and the phos-phate. (2) The mononuclear bound phosphate is deprotonated. (3)The deprotonated phosphate exchanges with another OH− of thesurface and a binuclear bond is formed. The reaction sequence isreversible and phosphate desorption is driven by OH−.

224 K. Mengel / European Journal of Agronomy 7 (1997) 221–233

OH− concentrations (Fig. 2) which means that adsorp-tion is particularly strong at low soil pH. This relation-ship is of utmost agronomic importance and isdiscussed in detail in the remaining part of this sec-tion.

Barekzai and Mengel (1985) investigated the influ-ence of the contact time between soil and phosphatefertilizer (superphosphate) on its P availability forLolium perennegrown in pots. From the ten soilstested only the results of the two extreme soils areshown (Fig. 3), an acid brown earth (7% clay, DL-P = 9 mg P/kg soil, in KCl solution, pH 4.6) and asubsoil from a rendzina (67% CaCO3, DL-P = 0.8 mgP/kg soil, pH 7.6). According to these characteristicsthe first soil should favor phosphate adsorption andthe latter the formation of less soluble Ca phosphates.Both soils were very low in available phosphate. Inthe acid soil the contact time had a highly significantimpact on the phosphate uptake of the grass. Phos-phate fertilizer, given 6 months before seeding,yielded a significantly lower recovery than phosphate

fertilizer applied just before seeding. Also a 3 monthscontact time still had a significantly negative effect onthe efficiency of the P fertilizer. This pattern found inthe first cut of the grass was also evident in the secondcut. In the calcareous soil the fertilizer/soil contacttime had no influence on the P uptake of the grass.Obviously there was no major formation of unavail-able Ca phosphates during a period of 6 months other-wise the rates of phosphate uptake by the grass shouldhave declined with an increase in the soil/fertilizercontact time. This statement is in line with results ofOlsen et al. (1977) who found that above pH 6 it is thesolubility of the octocalcium phosphate which con-trols the phosphate availability, and added phosphatesto such soils have a very high coefficient of recovery.The fast adsorption of fertilizer phosphate in acid soilswas also found by Mozaffari and Sims (1996).

In the acid soil, laboratory experiments of Barekzaiand Mengel (1985) showed a strong phosphateadsorption (Fig. 4). In the treatment with zero contacttime the adsorption curve was much flatter than thecurves obtained after a contact time of 6 and 12weeks. At the zero contact time the highest P rateresulted in a P concentration of 32 mg P/l; the sameP application rate gave only a P concentration in thesoil solution of about 2 mg P/l after a contact time of 6weeks. This demonstrates the enormous reduction in Pavailability most likely due to specific adsorption.Further, it could be shown in laboratory experimentsthat phosphate availability in this acid soil was sub-stantially increased by the incorporation of CaO intothe soil (Barekzai and Mengel, 1985). From thisexperiment it is clear that the efficiency of soil andfertilizer phosphates depends highly on soil pH. Thisprobably is true for all mineral soils with a potentialfor phosphate adsorption.

The relevance of soil pH for the efficiency of phos-phate fertilizer is supported by field trials. Accordingto Werner and Wichmann (1972) the recovery ofphosphate by crop uptake was much higher on neutraland calcareous soils than on acid soils. Sturm andIsermann (1978) in evaluating the phosphate recoveryin long-term field experiments also found that soil pHwas of high importance for P recovery. The recoveryof fertilizer P was calculated from the P uptake ofcrops and the change in available soil phosphatesince an increase in available soil P means a corre-sponding increase in the recovery of fertilizer P and

Fig. 3. Uptake of fertilizer phosphate byLolium perennefrom anacid and a calcareous soil as related to the time of P fertilizerapplication: 6 months before seeding, 3 months before seeding,at seeding. Grass was cut two times (Barekzai and Mengel,1985). ‘a’ denotes a significant difference at the 0.1% levelbetween phosphate application at seeding and 6 months before;‘b’ a significant difference at the 5% level between phosphateapplication at seeding and 3 months before seeding; ‘c’ a signifi-cant difference at the 5% level between phosphate application 3months before seeding and 6 months before seeding.

225K. Mengel / European Journal of Agronomy 7 (1997) 221–233

vice versa a decrease of available P a reduction of Precovery. Available soil phosphate was determined bythe DL- method. In the field trials quoted by Sturmand Isermann (1978) no rock phosphate was appliedand therefore the data in Table 2 give a good indica-tion of the fertilizer phosphate recovery. The mostinteresting results of this investigation are shown inTable 2 which clearly demonstrate the enormousimpact of soil pH on phosphate use efficiency andfrom which the conclusion is drawn that much phos-phate can be saved if soil pH is appropriate. A highrecovery of phosphate on Luvisols with a neutral toalkaline pH was also found by Jungk et al. (1993).

Humates may be involved in phosphate adsorptionwhich is particularly true for large areas of represen-tative arable soils derived from loess. According toinvestigations of Gerke and Hermann (1992) andGerke et al. (1995) Fe and Al may be adsorbed by

carboxylic groups of humic acids and then adsorbphosphate as shown in Fig. 5. In the experiments ofGerke et al. (1995) phosphate adsorption was some-what higher at pH 6.2 than 5.2. This surprising pHeffect presumably is due to a higher deprotonationof humate carboxylic groups at the higher pH whichmay promote the adsorption of Fe hydroxides. Gerkeand Hermann (1992) suggest that these P-Fe–humatecomplexes play a role in the turnover of fertilizerphosphate particularly in Luvisols derived fromloess. Whether this kind of phosphate complex has astronger impact on phosphate availability than thatassociated with sequioxides is not yet clarified.

Phosphate adsorption is a particular problem inhighly weathered soils of the tropics (Oxisols andUltisols) because of their high phosphate adsorptionpotential. For phosphate melioration they require highP fertilizer rates in the range of 170 kg P/ha (Haynes,1984). Most of these soils are acid and require limingwhich does not improve phosphate availability in allcases. Liming may induce polymerization of Al cationspecies which because of their high positive chargeare strong phosphate adsorbers (Haynes, 1984).According to Hauter (1983) the decrease of phosphateavailability due to liming of Oxisols is associated withtheir very low pH (3.7–4.4) while at a soil pH of 5.5liming had a beneficial effect on phosphateavailability. Sims and Ellis (1983) reported that lim-ing an Ultisol increased the available soil P andenhanced P uptake by oats considerably. In order tosave fertilizer phosphate on these strongly phosphatefixing soils band placement of fertilizers is recom-mended (Werner and Scherer, 1995).

As shown earlier (Fig. 2) adsorption is an exchangeof ligands and with an increase in soil pH the OH−

Fig. 4. Phosphate buffer curve of an acid soil. Directly after Papplication (0 weeks), 6 weeks and 12 weeks after P application(Barekzai and Mengel, 1985).

Table 2

Percentage recovery of fertilizer phosphate in long-term field trialson representative agricultural soils in relation to the lime status ofsoils. Recovery= P uptake of the crop+ change in DL-P in the soil(Sturm and Isermann 1978)

Lime status % Recovery

Arable soils, very well supplied with lime 80Arable soils, well supplied with lime 70Arable soils, moderately supplied with lime 65Arable soils, poorly supplied with lime 60Arable soils, poorly supplied dry locations 50Grassland 80

Fig. 5. Adsorption of phosphate to an humate Fe complex. The FeIII

is adsorbed onto the humate with a covalent bond and a coordinatebond (modified after Gerke and Hermann, 1992).

226 K. Mengel / European Journal of Agronomy 7 (1997) 221–233

concentration increases, OH− competing with phos-phates for binding sites at the adsorbing surface.Organic anions may also compete with phosphatefor binding sites (Parfitt, 1978). Fox et al. (1990)found a number of organic anions capable of replacingphosphates from adsorbing surfaces. Citrate seems tobe a very potent competitor for adsorbed phosphate(Gerke, 1994).

Under anaerobic conditions soluble phosphateincreased in the soil solution (Welp et al., 1983)mainly due to the reduction of complex bound FeIII

associated with the release of soluble phosphate. Aswas shown by Sah and Mikkelsen (1986) occludedphosphates may be solubilized under anaerobic con-ditions because of the reduction of FeIII to Fe2+ (theRoman superscript indicating an Fe complex, the Ara-bic superscript a dissolved Fe ion). The process is ofparticular importance for flooded rice soils.

4. Organic phosphate and mycorrhiza in soilcropping systems

In arable land the concentration of organic phos-phate is in the order of 50% of total phosphate in theupper soil layer and in grassland soils the proportionof organic phosphate may be even higher (Sharpley,1985). A substantial part of organic phosphate, up to100 kg P/ha, may be fixed in microbial biomass(Brookes et al., 1984). Phosphate thus immobilizedmay easily be mineralized and hence become avail-able for crops. Sharpley (1985) reported that there is aseasonal variation in available organic soil phosphatedecreasing in spring with crop growth and increasingin late autumn and winter. This pattern was particu-larly distinct in soils not treated with inorganic phos-phate fertilizer showing that the plants drewphosphate from this organic pool. In calcareoussoils, the phosphate of the soil solution is mainly pre-sent in organic form (Dalal, 1977) and therefore inthese soils phosphate transport to plant roots is mainlybrought about by organic phosphates which may beeasily mineralized in the plant rhizosphere enrichedwith phosphatases (Tarafdar and Claassen, 1988; Douand Steffens, 1993). About half of the organic phos-phates in soils is present as myo-inositol-phosphatesfrom which the inositol-hexaphosphate is adsorbed tosequioxides similar as inorganic phosphate (Dalal,1977). The adsorption of inositol-hexaphosphate isrelatively strong since the molecule has six phosphategroups which may be bound to soil particles. Dimin-ishing the numbers of phosphate groups bound to ino-sitol decreases the possibility of phosphate adsorptionand thus improves phosphate availability (Evans,1985). Myo-inositol-2-monophosphate is virtuallynot adsorbed (Evans, 1985), and quite mobile insoils (Dou and Steffens, 1993). In addition inositol-hexaphosphate can also form rather insoluble saltswith Ca2+ and Mg2+, a process which may affect phos-phate availability. Other organic phosphates such asphospholipids and nucleotide phosphates do not accu-mulate in soils as they are easily mineralized (Dalal,1977; Tarafdar and Claassen, 1988). Hence the largepool of organic soil phosphate is potentially availablefor plants. This is also true for the non-soluble organicphosphate from which a great part is present in theform of microbial biomass and which will be miner-alized after the death of microorganisms. Therefore,

Fig. 6. Water soluble phosphate originating from various phosphatefertilizers in the rhizosphere of young rape. The phosphate fertilizerhad been dressed in a 10 years lasting field trial. The horizontallines designate the level of water soluble phosphate in the bulk soil.PARP, partially acidulated rock phosphate (Steffens, 1987). Tho-mas slag is a non-crystalline, non-water soluble phosphate fertilizerwhich gradually dissolves in soils and therefore is well available toplant roots. Rock phosphate is a crystalline phosphate fertilizer(apatite), non-soluble in water which is dissolved in acid soils.PARP, partially acidulated rock phosphate which consists ofabout to 50% of rock phosphate and 50% of water soluble phos-phate.

227K. Mengel / European Journal of Agronomy 7 (1997) 221–233

in contrast to the fixed inorganic phosphate the immo-bilized organic phosphate represents a potential poolof available phosphate and measures which promotethe formation of organic phosphate in soils and mayrestrict the fixation of inorganic phosphate and thuscontribute to an efficient use of soil phosphates.

Sources of organic phosphates in soils are plantresidues, green manure, microbial biomass, and farmyard manure (FYM). For this reason cropping systemshave a distinct impact on the content of organic phos-phates in soils as well as on the assimilation of inor-ganic phosphates by fungi and bacteria and themineralization of organic phosphates by phos-phatases. Oberson et al., 1993, 1996; reported thatregular application of FYM to soil increased theorganic phosphate content. This effect may be dueto organic phosphate present in the FYM but also toinorganic phosphate being assimilated by soil micro-organisms after FYM application. The latter espe-cially raised the ATP concentration which,according to the authors means an increase in micro-bial biomass. The impact of FYM on the concentra-tion of ATP in the upper soil layer is shown in Table 3,from the work of Oberson et al. (1993). It is evidentthat in all treatments receiving FYM the ATP concen-tration was significantly increased which means thatFYM had a beneficial effect on microbial biomassdevelopment and hence on the storage of potentiallyavailable phosphate. Parallel with the increase ofmicrobial biomass the acid phosphatase activity wasincreased by FYM application which means that alsothe enzyme activity rendering organic phosphate intoa form directly taken up by plant roots was promoted.The positive effect of FYM on the efficient use of soil

and fertilizer phosphate availability is enhanced byorganic anions produced during the decompositionof organic matter. They compete with inorganic phos-phate for adsorption sites and thus reduce the fixationof phosphate (Werner and Scherer, 1995). In additionFYM may improve soil structure and favor rootgrowth and thus the exploitation of soil phosphatesby roots (Keita and Steffens, 1989). Farms producingFYM frequently also grow arable forage crops such asred clover and alfalfa which not only contribute to thenitrogen status of soils by symbiotic N2 fixation butthey also may exploit fixed soil phosphate by theexcretion of root exudates as was shown for red cloverexcreting citrate which mobilizes adsorbed soil phos-phate (Gerke, 1994). Rotations with diverse crop spe-cies generally will contribute to a better exploitationof soil phosphates. Mycorrhization of plant roots mayconsiderably improve the accessibility of soil phos-phate to plants mainly by increasing the contact sur-face between the soil matrix and the mycorrhizedplant root. This is particularly true for leguminousspecies (Barea and Acon-Aguilar, 1983). The problemwith mycorrhiza exploiting soil phosphate for the hostplant is the high specificity between the host plant andthe endomycorrhizal fungi (Lioi and Giovannetti,1987; Diederichs, 1991). Inoculation of soils withthe appropriate fungi still meets with difficulty(Hall, 1987). If the fungi/root symbiosis is efficientremarkable crop yield increases may be obtaineddue to a better exploitation of soil phosphate (Hall,1984).

5. Phosphate fertilizer types

Phosphate fertilizer types differ in their solubilitywith the most important difference between amor-phous and crystalline forms. The latter comprisesthe rock phosphates and partially acidulated rockphosphate (PARP) which still contains a portionwhich is crystalline and represents apatite. The solu-bility of fluoro-apatite is given by the following equa-tion:

Ca5(PO4)3F + 4H+N 5Ca2+ + 3HPO2−

4 + HF

From the equation it is evident that high Ca2+ andphosphate concentrations hamper, and increasing H+

concentrations in the soil solution promote the disso-

Table 3

Effect of FYM on the ATP concentration in soils. Soil samplestaken at ear emergence of winter wheat (Oberson et al., 1993)

P fertilizer kg P/ha Rate of P appl.kg P/ha per year

ATP mg/kg soil*

No – 843a

FYM 28 1217c

80% FYM + 20%mineral P

31 1160bc

40% FYM + 60%mineral P

47 1006abc

100% mineral P 46 945ab

228 K. Mengel / European Journal of Agronomy 7 (1997) 221–233

lution of apatites. Solubility of apatites (rock phos-phates) depends also on the degree of isomorphicsubstitution of PO4

3− by CO32− and is higher the more

phosphate is substituted by carbonate (Anderson etal., 1985). Generally in acid soils pH, 5.0 (mea-sured in CaCl2 solution) the efficiency of rock phos-phate is as high as that of acidulated phosphate(Mengel, 1986). In soils with a higher pH, however,the efficiency is poorer and may be even nil. In suchcases the application of rock phosphate means awaste of the phosphate resource. Steffens (1994)investigated a number of representative arable soilsfor their availability of phosphate originating fromvarious fertilizer types. Phosphate release ratesobtained by repeated extraction of soils with elec-tro-ultrafiltration (EUF) followed the Elovich equa-tion and reflected well the phosphate availability ofvarious fertilizer types for crops. The agreement ofthe released phosphate with the Elovich equationmeans that the P release rates declined with the num-ber of extractions. Highest release rates wereobtained from basic slag (Thomas phosphate) andsuperphosphate and lowest rates from rock phos-phate. This pattern of phosphate fertilizer solubilitywas also found in the rhizosphere of rape as shown inFig. 6 (Steffens, 1987) from which can be seen thatpartially acidulated phosphate took an intermediateposition. This means that mainly the water solubleportion contributed to P solubility. For this reasonalso the application of partially acidulated rock phos-phates on soils with a poor solubility for apatitemeans a waste of phosphate (Resseler and Werner,1989). The pretention that apatitic phosphate willrender soluble in soils by time is only correct ifsoils are acid (Renno and Steffens, 1985). Suchsoils, however, if not organic soils, should be limedin order to improve the availability of adsorbed phos-phate as discussed above. If lime is not available rockphosphates may be an alternative choice. The poorperformance of apatitic phosphate found in represen-tative arable soils in Europe (Mengel, 1986) is inagreement with experiences made on laterite soilsin Western Australia (Bolland et al., 1988; Bollandand Gilkes, 1990). Also in these field trials the directand residual effect of apatitic fertilizer was poor ascompared with superphosphate. Only on the humicsandy podsols in south Western Australia with annualrainfall .800 mm Bolland (1996) found a superiority

of apatitic fertilizers as compared with superpho-sphate. Under these particular conditions superpho-sphate may be leached out from the top soil layer.

Proton excretion and mycorrhizal colonization ofplant roots may contribute to the solubilization ofapatite. According to Hauter and Steffens (1985) thehigh proton excretion of red clover roots, typically forsymbiotically living leguminous species (Mengel,1994), contributed to the dissolution of rock phos-phate. An interesting effect of mycorrhizal infectionwas found by Steffens (1992). A farmer havingapplied rock phosphate for years on a calcareoussoil finally ended in a severe phosphate deficiencyof sugar beets. Field trials carried out on this soilwith different phosphate fertilizer types gave theresults shown in Table 4. It is evident that the responseof sugar beets to rock phosphate application was nil incontrast to superphosphate which produced a remark-able yield increase. In sunflowers, however, the effectof rock phosphate was as high as the effect of super-phosphate; in wheat the high rate of rock phosphatewas as good as the low rate of superphosphate. Sun-flower roots were well colonized with mycorrhiza,sugar beet roots were not. This example shows thebeneficial effect of mycorrhiza on the acquisition ofrock phosphate. The decision for a farmer to applyrock phosphate depends therefore also on the cropspecies and on the species in the rotation. If the rota-tion comprises a sugar beet crop the level of availablesoil phosphate should be maintained by applyingacidulated phosphates or amorphous forms of phos-phate such as sinterphosphate (CaNa phosphate pro-

Table 4

Effect of superphosphate and hyperphos (phosphate rock) on thebeet yield and grain yield of various crops. The calcareous soil hada pH of 7.4 (after Steffens, 1992)

Phosphate, applied Sugar beet,1987

Sunflowers,1988

Wheat,1989

Yield in t/ha

No phosphate 32.8 3.77 6.59Hyperphosphate low rate 32.3 4.35 6.81Superphosphate low rate 46.5 4.19 7.33Hyperphosphate high rate 32.3 4.18 7.55Superphosphate high rate 50.0 4.39 7.51Least significant

difference, 5%7.9 0.31 0.51

229K. Mengel / European Journal of Agronomy 7 (1997) 221–233

duced in soda production) or Thomas phosphate. Inmany cases 50% of an amorphous phosphate will givethe same yield as 100% of the apatitic phosphate asshown in Table 4. Hence from the viewpoint of savingthe phosphate resource 50% of the amorphous phos-phate is the better choice.

6. Perspectives

As shown above (Table 4) mycorrhizal symbiosiswith plant roots represents an interesting mechanismfor the efficient use of soil phosphates. This potentialwill be only used if the available soil phosphate levelis not too high. The high specificity in the relationshipbetween fungus species/host plant species (Hall,1987; Lioi and Giovannetti, 1987; Diederichs, 1991)and the problem of inoculating soils with the properfungus species still represents severe obstacles for theuse of mycorrhiza in practical farming and needfurther scientific and technical efforts. Excretion oforganic anions and protons by plant roots under theconditions of insufficient phosphate supply is a furthermechanism which merits attention. Proton excretionmay help to solubilize apatitic phosphates (Hofflandet al., 1990), and the excretion of organic anions todesorb adsorbed phosphate (Hedley et al., 1982). Thelatter authors were the first who found thatBrassicanapuswas capable of responding to an insufficientphosphate supply by an enhanced excretion of H+.Protons alone, however, would rather depress theavailability of adsorbed phosphate than mobilize it.In addition to the proton excretion, rape roots alsoexcrete organic anions, especially malate which maydesorb adsorbed soil phosphate (Hoffland et al.,1989). This response ofBrassica napusto low phos-phate supply was not found withLolium multiflorum(Ruiz, 1992). Zhyu et al. (1990) found that rice plantsexcrete citrate under the conditions of insufficientphosphate supply and thatJaponica species weremore efficient in citrate excretion thanIndicaspecies. Ae et al. (1990) reported that pigeon peashave no particular potential to exploit Ca phosphatesbut they are capable of excreting a tartrate derivate(piscidic acid) which mobilizes adsorbed soil phos-phate. Of particular interest are the proteoid roots ofLupinus albuscapable of excreting large amounts ofcitrate (Gardner and Parbery, 1982) which mobilize

insoluble soil phosphate the effect being due to thecitrate and not to the release of H+ (Gardner et al.,1983). According to Dinkelacker et al. (1989) citrateexcreted by proteoid roots ofLupinus albusmay alsosolubilize Ca phosphate by chelating the Ca2+ of inso-luble Ca phosphate. Red clover is also a potentialspecies in excreting citrate by roots (Gerke, 1994)the quantities being released were in the same rangeas citrate excreted by proteoid roots ofLupinus albus(Gerke et al., 1994).

7. Conclusions

A more efficient use of soil and fertilizer phos-phates demands agronomic and scientific efforts.From the agronomic measures such as the selectionof the appropriate phosphate fertilizer type, adjustingfertilizer rates to soil tests and liming soils to an opti-mum pH level may be easily implemented by Eur-opean farmers since lime and various phosphatefertilizer types are available. In areas with excessivelyhigh levels of available soil phosphate due to intensivelivestock farming, cropping systems should be devel-oped with a closer integration of crop and animalproduction so that phosphates excreted by farm ani-mals are efficiently used for crop production. Suchfarming systems should comprise a broader diversityof crop species in the rotation including forage cropswhich are particularly efficient in exploiting soil phos-phates by mycorrhiza and/or excretion of organicanions by roots. The implementation of such farmingsystems substituting the intensive livestock produc-tion needs not only agronomic but particularly politi-cal and economical measures.

Scientific and technical efforts are required forselecting appropriate endomyccorhizal fungi ecotypesand practicable soil inoculation techniques. The phy-siological mechanism by which plants respond to aninsufficient phosphate supply such as the secretion oforganic anions by plant roots needs elucidation.

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