Iron oxides and organic matter on soil phosphorus availability

Óxidos de ferro e matéria orgânica na disponibilidade de fósforo no solo

ABSTRACT

Continuous crop expansion has led to a growing demand for phosphate fertilizers. A sound knowledge of the dynamics of phosphorus, and its interaction with iron oxides and organic matter, can be useful to develop effective strategies for sustainable management, especially in a scenario of increasing shortage of mineral phosphate resources. In this paper, we review the relationship of phosphate to iron oxides and organic matter, and its effect on phosphorus availability. Crops typically obtain phosphate from weathered minerals and dissolved fertilizers. However, the amount of phosphorus present in the soil solution depends on the extent to which it is adsorbed or desorbed by iron oxides, which may be influenced by interactions with organic matter. Therefore, systems for fertilizer recomendation based on methodologies considering interactions between soil components such as oxides and organic matter, and the phosphorus sorption capacity resulting from such interactions (e.g. residual P analysis), may be more reliable to ensure efficient, rational use of phosphate.

Index terms:
Goethite; hematite; phosphorus adsorption; phosphorus desorption; organic carbon

RESUMO

A contínua expansão da produção agrícola tem levado a uma crescente demanda de fertilizantes fosfatados. O conhecimento da dinâmica do fósforo no solo e suas interações com óxidos de ferro e matéria orgânica podem ser uteis no desenvolvimento de estratégias eficientes para o manejo sustentável, especialmente em um cenário de crescente escassez de fontes de minerais fosfatados. Nesta revisão bibliográfica foi abordado a relação do fósforo com óxidos de ferro e matéria orgânica, e seu efeito na disponibilidade de fósforo. As culturas, normalmente, obtém fosfato de minerais intemperizados ou fertilizantes dissolvidos. No entanto, a quantidade de fósforo presente na solução do solo depende das reações de adsorção e dessorção por óxidos de ferro, as quais podem ser influenciadas por interações com a matéria orgânica. Portanto, os sistemas de recomendação de fertilizantes com base em metodologias que consideram as interações entre componentes do solo, tais como óxidos e matéria orgânica, e a capacidade de adsorção de fósforo, resultantes de tais interações (por exemplo, análise de P remanescente), pode ser mais confiável para garantir o uso eficiente e racional de fertilizantes fosfatados.

Termos para indexação:
Goethita; hematita; adsorção de fósforo; dessorção de fósforo; carbono orgânico

INTRODUCTION

The world population is expected to rise from 7.2 billion at present to 9.1 billion by 2050; also, food demand is estimated to double over this period. The increasing food demand for food and shortage of fertilizer worldwide (Cordell et al., 2009; Grantham, 2012) has raised the need for efficient use of nutrients in order to meet the demands for increased agricultural production while ensuring environmental sustainability (Tenkorang; Lowenberg-DeBoer, 2008; Worstall, 2013). Brazil is expected to play a central role in this scenario (Tollefson, 2010), where traditional food production practices will have to be transformed into sustainable, healthy, economically efficient agriculture (Sachs et al., 2010).

Productivity can be boosted through appropriate crop nutrition, which involves a number of chemical, physical and biological processes occurring in soil that are influenced by mineralogy, organic composition, fertilization and soil management. The dynamics and kinetics of these processes are affected by interactions between clay fraction and organic components of soil, which influence nutrient availability to plants (Barber, 1995; Sposito, 2008). Phosphorus (P) is especially influential on agricultural production in countries such as Brazil (Novais; Smith, 1999), where soils -largely highly weathered Oxisols and Ultisols- are typically poor in this element. These two types of soil account for approximately 170 million hectares in 72 countries and 50% of all terrestrial agriculture in the world. In Brazil, they occupy 58% of the territory (IBSRAM, 1985), and are rich in iron and aluminium oxides, as well as in 1:1 phyllosilicates such as kaolinite; also, they contain substantial amounts of 2:1 minerals (Kämpf; Curi, 2003; Schaefer et al., 2008).

PHOSPHORUS

Phosphorus is one of essential elements and also one of the most important macronutrients for plant life. In fact, P plays a crucial role in phosphorylation and in the production of adenosine triphosphate by photosynthesis. It is the eleventh most abundant element in the terrestrial crust, with average content of 1050 mg kg^-1 (Heirinch, 1980), and is found in more than 370 minerals (Huminicki; Hawthorne, 2002). However, only minerals in the apatite group contain enough P to justify its mineralization, whether as hydroxyapatite [Ca₅(PO₄)₃(OH)], fluorapatite [Ca₅(PO₄)₃F] or chlorapatite [(Ca₅(PO₄)₃Cl)] (Hughes; Rakovan, 2002).

Morocco and Western Sahara in Africa, and China -mainly- in Asia, have 66% of all phosphate rocks in the world (Fixen, 2009). However, there are estimates that P mineral reserves will decay over this century if phosphate demand and production continue to grow at the current rate (Vaccari, 2009). According to Cordell et al. (2009), extraction of phosphatic rocks might peak in 2030 and then decline in parallel to an increase in price.

Global use of P increased markedly from 1961 to 2007 (Metson; Bennett; Elser, 2012); however, the imminent P crisis has refocused international attention in recent years, especially, after the 2008 rise in the price of phosphate rocks by about 800% (Gilbert, 2009). This scenario has raised increasing awareness of the P shortage and, together with also increasing worries about the environmental impact of P pollution, has boosted research to improve the use of this element by reducing losses in the agro-ecosystem (Dawson; Hilton, 2011; Fernandez-Mena; Nesme; Pellerin, 2016).

PHOSPHORUS IN SOIL

Phosphorus in soil parent materials is primarily in mineral form (Figure 1) and especially as apatite (calcium phosphate) (Tiessen et al., 1984). The action of different factors (e.g., parent material, climate, slope, organisms, time) and processes (translocation, transformation, addition, removal) involved in soil formation drives the primary mineral to a thermodynamic equilibrium with stable pedogenic forms. In these transformations, P from primary minerals is released into the soil solution, from which plants can absorb it. Concomitantly, elements such as Ca, Mg, K and Na, silicates and carbonates, are leached. Transformation of Fe and Al into oxides, hydroxides or oxyhydroxides creates new functional groups for P adsorption.

Figure 1:
Phosphorus cycle in the environment.

Soil weathering causes dissolved phosphate from primary minerals to (a) precipitate with some cations and lead, for example, to the neo-formation of calcium phosphate in alkaline soils (Beck and Sánchez, 1994); (b) be adsorbed by functional groups of iron or aluminium oxides to form thermodynamically stable complexes (Bortoluzzi et al., 2015; Fink et al., 2016b) or (c) form biologically active organic compounds that remain as organic P in soil (Conte et al., 2002; Martinazzo et al., 2007; Dodd; Sharpley, 2015). Transformations between inorganic and organic forms of P are governed by factors affecting its mineralization and immobilization (e.g., microbial activity, moisture, physico-chemical and mineralogical soil properties) (Santos et al., 2008; Shen et al., 2011; Tiecher et al., 2012).

The dissolution of minerals or phosphate fertilizers, and the mineralization of organic components in soils, produce different anionic species (Lindsay et al., 1989) that are protonated to a variable extent depending mainly on pH (Hinsinger, 2001). Inorganic P species derived from orthophosphoric acid (H₃PO₄) such as H₂PO₄ ^- and HPO₄ ^2-are preferentially absorbed by plants. To what extent P remains in the soil solution depends on the degree to which it is adsorbed, desorbed and mineralized (Hinsinger, 2001; Fink et al., 2016b). Most tropical and subtropical soils in Brazil are low in available P because of strong phosphate adsorption on soil minerals (Almeida et al., 2003; Johnson; Loeppert, 2006; Bortoluzzi et al., 2015).

IRON OXIDES IN SOILS

Brazilian soils -particularly well-drained soils (Schaefer et al., 2008)- typically contain iron oxides in amounts ranging from a few grams to about 800 g kg^-1 (Kämpf; Curi, 2003). Goethite and hematite are the most common pedogenic iron oxides, accompanied by maghemite and ferrihydrite in small amounts (Kämpf; Schwertmann, 1982; Schaefer et al., 2008; Carvalho Filho et al., 2015). The presence and abundance of these iron oxides depend on the conditions of soil evolution (Bortoluzzi et al., 2015). Thus, Oxisols, which are found near the Equator Line, contain aluminium oxides (gibbsite) mainly. On the other hand, the oxides hematite, goethite, maghemite and magnetite prevail in tropical and subtropical Oxisols (Alleoni; Camargo, 1995). Ferrihydrite and lepidocrocite are found in poorly drained soils and exhibit greater, and faster phosphate adsorption (Wang et al., 2013) as a result of their nanometric size and poorly crystalline structure leading to a high specific surface area (SSA). The presence of goethite is favoured by the high organic matter contents and acid pH of the soils (Cornell; Schwertmann, 1996), which usually exhibit a higher affinity for this mineral than for hematite (Guzmán et al., 1994).

Structurally, hematite (α-Fe₂O₃) consists of O layers superimposed on the z-axis, with Fe³⁺ occupying 66% of all octahedra formed and each octahedron sharing a face with another in the upper layer (Bigham et al., 2002). The (SSA) of synthetic hematite ranges from 2 to 115 m² g^-1 (Cornell; Schwertmann, 1996; Barrón et al., 1988); whereas that of natural hematite does not exceed 47 m² g^-1 (Torrent et al., 1994).

Goethite (α-FeOOH) is the most abundant iron oxide. Its structure comprises a double network of FeO₃(OH)₃ octahedra on the z-axis. The octahedron spaces juxtaposed to the network are empty as a result of Fe³⁺ occupying only one-half of all spaces; also, each double network is bonded to another by hydrogen bonding and by sharing the apical oxygen (Bigham et al., 2002). SSA for goethite ranges from 21 to 70 m² g^-1 (Cornell; Schwertmann; 1996; Torrent et al., 1990).

Ferrihydrite is an iron oxyhydroxide precursor of hematite formation (Bigham et al., 2002) with a varying formula as a result of its also varying degree of hydration and of continuous reorganization of atoms in its structure. Michel et al. (2010) synthesized an ordered ferrihydrite with an increased crystalline structure [Fe_8.2O_8.5(OH)_7.4 + 3H₂O] and ferrimagnetic behaviour, but failed to directly observe this phase in soils. Because of its low atomic order, identifying this iron oxide requires using X-ray diffractometry with synchrotron radiation and supplementary techniques such as selective chemical extraction with ammonium oxalate and Vis-IR or Mössbauer spectroscopy. This mineral is present in soil and sediments predominantly in form of nanometric particles and hence with a high SSA [up to 400 m² g^-1 according to Schwertmann; Taylor (1989)].

Maghemite (γ-Fe₂O₃) is typically formed by oxidation (Fe²⁺ → Fe³⁺⁾ of magnetite. This mineral is isomorphic to hematite and isostructural to magnetite; also, it possesses a cubic structure consisting of iron tetrahedra and octahedra in addition to empty spaces formed by effect of changes in Fe valence (Bigham et al., 2002; Schwertmann; Taylor, 1989). A stoichiometric imbalance of spins makes maghemite magnetic. This mineral is present in amounts up to 297 g kg^-1 in soils (Souza et al., 2010; Costa et al., 1999); also, it can exhibit a high SSA depending on the particular formation conditions (Camargo et al., 2015).

PHOSPHORUS ADSORPTION ON IRON OXIDES

The high affinity of iron oxides for phosphate has for decades boosted research into the adsorption, desorption and diffusion dynamics of P, and its availability, in soils (Table 1). Some studies have revealed that the actual importance of P adsorption by other clay minerals has been underestimated. Thus, P is adsorbed less markedly by functional groups at the edges of 1:1 and 2:1 minerals, and this affects the amount and energy of P adsorption -and hence P availability to plants (Devau et al., 2009). Recently, Gérard (2016) revisited experimental studies on the topic conducted over the past 70 years and concluded that the P adsorption capacity of clay minerals may be similar to or even higher than that of iron and aluminium oxides depending on the SSA of the particular soil components.

Table 1:
Selected studies on phosphorus adsorption in soils.

Phosphorus adsorption and desorption depend on concentration, crystallinity, SSA, and the configuration and concentration of hydroxyl groups on the surface of iron oxides. These factors in turn are affected by the formation route, parent material, degree of weathering, soil solution composition, drainage conditions and pH (Barrón; Torrent, 1996; Inda; Kämpf, 2005; Schaefer et al., 2008). Well-drained soils weathered to a variable degree have been found to differ in maximum phosphorus adsorption capacity (P_max) depending on the particular type of iron or aluminium oxide and on its properties (Curi; Franzmeier, 1984; Torrent et al., 1994; Barrón; Torrent, 1996; Almeida et al., 2003; Cessa et al., 2009; Lair et al., 2009; Broggi et al., 2010; Fink et al., 2014).

Adsorption of phosphate in the soil solution by functional groups in iron oxides results in the formation of surface complexes with no intercalated water molecules that are specifically adsorbed (Figure 2). These surface complexes are called "inner sphere complexes" to indicate that they are strongly bonded to highly structured mineral surfaces via covalent binding (Essington, 2003; Sparks, 2003; Sposito, 2008). Phosphorus is preferentially adsorbed by hydroxyl surface groups in iron oxides, which are protonated below pH 7-9 (zero-charge point; Table 2) (Essington, 2003; Sparks, 2003; Sposito, 2008). Hydroxylation occurs when Fe ions on mineral surfaces are exposed to water and complete its coordination with hydroxyl groups (Stumm, 1992). Hydroxyl groups may be coordinated by one (type A, ≡Fe-OH^-0.5), two (type C, ≡Fe₂-OH⁰⁾ or three Fe atoms (type B, ≡Fe₃-OH^+0.5), corresponding to hydroxyls of simple, double or triple coordination (Figure 2), respectively (Russel et al., 1974; Essington, 2003; Sparks, 2003; Sposito, 2008). Type A hydroxyls are the most easily protonated (Fontes et al., 2001) as a result of the charge balance in Fe-O bonds, where the electron cloud of oxygen is more electronegative than in doubly or triply coordinated hydroxyls. Protonation of these functional groups confers Lewis acid properties, with the metal cation reacting with empty electronic orbitals. These sites are very reactive because a positively charged water molecule (≡Fe-OH₂ ^+0.5) is very unstable and easily exchanged with an organic or inorganic anion in solution. Protonation weakens the Fe-OH bond by displacing the electron cloud of oxygen to the hydrogen side (Fontes et al., 2001). As a result, hydroxyl protonation triggers two different processes in P adsorption, namely: (a) protonated surfaces generate a positive electric field that attracts phosphate ions; and (b) phosphate replaces protonated hydroxyl groups. The phosphate may be absorbed in monodentate or bidentate form depending on the number of OH groups in the phosphate that are bonded to Fe atoms, or in binuclear form when two OH phosphate groups are adsorbed by two Fe atoms (Figure 2).

Figure 2:
Phosphorus adsorption in monodentade/ mononuclear and bidentate/binuclear forms onto goethite surfaces.

Table 2:
Zero-charge point (ZCP) for major organic and inorganic soil components. Adapted from Essington (2003), Sparks (2003) and Sposito (2008).

Thermodynamically, all adsorbed phosphate may be desorbed (Barrow, 1983a, 1983b); however, the desorption kinetics depends on the interplay of various factors such as the types of clay minerals where the phosphate is adsorbed (Chintala et al., 2014). According to Parfitt (1989), the binding energy increases in the sequence monodentate > bidentate > binuclear complexes and the probability of phosphate desorption increases in the reverse sequence.

Barrón and Torrent (1996) estimated the concentration of monocoordinated hydroxyl groups in various goethite and hematite faces, which adsorb P via binuclear complexes. Adsorbed phosphate can increase the proportion of binuclear complexes through so-called "phosphorus aging" (Santos et al., 2008; de Campos et al., 2016). This accounts for the reported fact that phosphate diffuses with time, through defects on the mineral surface, thereby significantly increasing P_max and decreasing desorption (Barrow, 1985; Torrent et al., 1992; Barrow, 1987). Willian and Reith (1971) found 8-20% of all P added to soil to remain available one year after application, and the proportion to decrease to 2.7% after 6 years.

Barrón et al. (1988) and Torrent et al. (1994) found P_max for hematite to range from 0.8 to 4.1 µmol P m^-2 in natural samples and from 0.2 to 3.3 µmol P m^-2 in synthetic samples, depending on the size, morphology, and degree of Al substitution in its crystal structure. In goethite, P_max ranges from 1.62 to 3.13 µmol P m^-2 (Torrent et al., 1994); in ferrihydrite, it is close to 7 µmol P m^-2 (Guzman et al., 1994). Although the average phosphate adsorption per surface area unit is similar for goethite and hematite, the goethita typically adsorbs more P as a result of its higher SSA (Torrent et al., 1994). This is consistent with the results of Parfitt (1989) and Wang (2013), who found P adsorption to decrease in the mineral sequence ferrihydrite > goethite > hematite. Ferrihydrite can considerably alter P_max in soil, even at low concentrations in well-weathered soils (Johnson and Loeppert, 2006; Ranno et al., 2007; Fink et al., 2014). Fink et al. (2016a) examined the effect of SSA on P adsorption in two Oxisols with similar contents in iron oxides and found P_max to be twice greater in the soil where goethite prevailed over hematite.

INTERACTION OF ORGANIC MATTER WITH IRON OXIDES AND PHOSPHORUS

Organic matter is an important influential factor for chemical, physical and biological soil properties. Negatively charged functional groups in organic substances (e.g., carboxyl, phenol) can interact with positively charged minerals such as iron oxides and alter phosphorus adsorption as a result (Schwertmann; Kodama; Fischer, 1986; Liu et al., 1999). In fact, adsorption of organic functional groups onto iron oxides can (a) promote anion adsorption via cation bridges (Al³⁺ and Fe³⁺⁾; (b) increase SSA by inhibiting mineral crystal growth; (c) alter surface charges; (d) boost competition with other anions for adsorption sites; and (e) cause adsorbed anions to be desorbed (Hinsiger et al., 2011; Borggaard et al., 2005; Guppy et al., 2005; Hinsinger, 2001). These phenomena are illustrated in Figure 3.

Figure 3:
Effects of organic carbon on phosphorus adsorption onto iron oxides.

As can be seen, condition I in the figure increases P adsorption (Yaghi; Hartikainen, 2013); however, if it decreases the P concentration in the soil solution, then the bond is reversible. In condition II, the presence of organics acids inhibiting crystal growth increases SSA in iron oxides and hence P adsorption (Barrón et al., 1988). However, Mikutta et al. (2006) found citrate (an organic anion) to block goethite pores and prevent phosphate diffusion into mineral defects as a result.

Organic acids in soil also can compete for P adsorption sites (condition IV; Schwertmann; Kodama; Fischer, 1986; Bayon et al., 2006; Redel et al., 2007; Zamuner et al., 2008) or, if previously adsorbed, alter the surface charge of iron oxides and cause phosphates to be electrostatically repelled (condition III; Antelo et al., 2007). Phosphorus sorption is decreased in both cases.

Several studies have shown humic acids to affect the reduction of phosphorus adsorption (Sibanda; Young, 1986; Andrade et al., 2003; Antelo et al., 2007) and hence the increase in P availability (Pavinato; Merlin; Rosolem, 2008). Recently, Yan et al. (2015) studied the phosphorus adsorption capacity of humic acid complexes of ferrihydrite and goethite under variable conditions of pH and ionic strength. The authors found P adsorption to be substantially reduced by iron oxides in the presence of organic compounds. However, Borggaard et al. (2005) and Guan, Chang and Chen (2006) found the adsorption energy of P onto iron oxides to be much higher than that of organic acids, being that the natural concentration of organic carbon in soil had no effect on P adsorption. These results are consistent with those of Afif et al. (1995), who found the concentration of low-molecular weight organic acids in extracts from P-containing soils to increase; this suggests that the acids may delay but not prevent P adsorption. The previous results make phosphate desorption by organic matter unlikely (condition V in Figure 3), even though Souza et al. (2014) found the addition of citrate to soil to increase P desorption.

Some studies have revealed that increasing the organic matter content of soil does not decrease P_max (Boschetti; Quintero; Benavidez, 1998; Valladares; Pereira; Anjos, 2003; Fink et al., 2014, 2016a); others, however, suggest that organic matter affects the binding energy of adsorbed P (Kreller et al., 2003, Rheinheimer; Anghinoni; Conte, 2003) and can therefore increase the efficiency of phosphate fertilizer -possibly as a result of phosphate adsorption with little energy (e.g., via cation bridges; Guppy et al., 2005; Figure 3).

Some recent studies have addressed the dynamics of P adsorption in the presence of C added in biochar forms (Yao et al., 2012; Lin et al., 2012; Xu et al., 2014). Biochar is a product of the pyrolysis, with oxygen limitation, of biological materials (Cernansky, 2015) whose characteristics depend on the production conditions (viz., residue composition, temperature, time, oxygen supply during burning). Biochar has proved be an efficient sorbent for organic pollutants by effect of its high SSA and porosity (Lehmann, 2007; Glaser; Lehmann; Zech, 2009; Cornelissen et al., 2005). An increased number of phenol, hydroxyl, carboxyl and quinone groups can increase negative surface charge (Cohen-Ofri et al., 2006) and decrease P adsorption as a result. However, this assumption requires further investigation in order to confirm the favourable and adverse effects of biochar on tropical soils.

CONCLUSIONS

The growing global demand for food and fibre, and the impending shortage of phosphate mineral reserves, have made it indisputably necessary to understand the processes and mechanisms governing phosphorus availability in soil. Iron oxides and organic matter are the soil constituents most strongly affecting the reactions and rate of phosphorus adsorption and desorption, especially in highly weathered soils. A sound knowledge of the interaction of iron oxides and organic matter with soil P is essential with a view to developing effective nutrient management strategies for agro-ecosystems allowing crop productivity to be maintained or even increased with a concomitant reduction in phosphate fertilizer use. Recent studies in highly weathered Brazilian soils have shown that organic matter and various iron oxides have a direct effect on P adsorption/desorption and availability (Bortoluzzi et al, 2015; Fink et al., 2016b, 2014). As a result, fertilizer recommendation systems based on soil buffering categories established in terms of clay content may be ineffective. Therefore, systems for fertilizer recommendation based on methodologies considering interactions between soil components such as oxides and organic matter, and the phosphorus sorption capacity resulting from such interactions (e.g., residual P), may be more reliable to ensure efficient, rational use of phosphate fertilizers.

REFERENCES

• AFIF, E.; BARRÓN, V.; TORRENT, J. Organic matter delays but does not prevent phosphate 19 sorption by Cerrado soils from Brazil. Soil Science, 159(3):207-211, 1995.
• ALLEONI, L. R. F.; CAMARGO, O. A. Óxidos de ferro e de alumínio e a mineralogia da fração argila desferrificada de Latossolos ácricos. Scientia Agricola, 52:416-421, 1995
• ALMEIDA, J. A.; TORRENT, J.; BARRÓN, V. Cor de solo, formas do fósforo e adsorção de fosfatos em Latossolos desenvolvidos de basalto do Extremo-Sul do Brasil. Revista Brasileira de Ciência do Solo, 27:985-1002, 2003.
• ANDRADE, F. V. et al. Adição de ácidos orgânicos e húmicos em Latossolos e adsorção de fosfato. Revista Brasileira de Ciência do Solo, 27:1003-1011, 2003.
• ANTELO, J. et al. Adsorption of soil humicacidat the surface of goethite and its competitive interaction with phosphate. Geoderma, 138:12-19, 2007.
• BARBER, S. A. Soil nutrient bioavailability: A mechanistic approach. New York: John Wiley & Sons, 1995, 414p.
• BARRÓN, V.; HERRUZO, M.; TORRENT, J. Phosphate adsorption by aluminous hematites of different shapes. Soil Science Society of America Journal, 52:647-651, 1988.
• BARRÓN, V.; TORRENT, J. Surface hydroxyl configuration of various crystal faces of hematites and goethites. Journal of Colloid and Interface Science, 177:407-410, 1996.
• BARROW, N. J. Effects of previous additions of phosphate on phosphate adsorption by soils. Soil Science, 118:82-89, 1974.
• BARROW, N. J. Reactions of anions and cations with variable charge soils. Advances in Agronomy, 38:183-230, 1985.
• BARROW, N. J. Reactions with variable charge soils. Fertilizer Research, 14:1-100, 1987.
• BARROW, N. J. On the reversibility of phosphate sorption by soils. Journal of Soil Science, 34:751-758, 1983a.
• BARROW, N. J. A mechanistic model for describing the sorption and desorption of phosphate by soil. Journal of Soil Science, 34: 733-750, 1983b.
• BAYON, R. C. L. et al. Soil phosphorus uptake by continuously cropped Lupinus albus: A new microcosm design. Plant Soil, 283:309-321, 2006.
• BECK, M. A.; SANCHEZ, P. A. Soil phosphorus fraction dynamics during 18 years of cultivation on a Typic Paleudult. Soil Science Society of America Journal, 58:1424-1431, 1994.
• BHAT, K. K. S.; NYE, P. H.; BALDWIN, J. P. Diffusion of phosphate to plant roots in soil - IV. The concentration distance profile in the rhizosphere of roots with root hairs in a low-P soil. Plant and Soil, 44:63-72, 1973.
• BIGHAM, J. M.; FITZPATRICK, R. W.; SCHULZE, D. Iron oxides. In: DIXON, J. B.; SCHULZE, D. G. Soil mineralogy with environmental applications. Madison: Soil Science Society of America Book Series, 2002. p. 323-366.
• BORGGAARD, O. K. et al. Influence of humic substances on phosphate adsorption by aluminium and iron oxides. Geoderma, 127:270-279, 2005.
• BORTOLUZZI, E. C. et al. Occurrence of iron and aluminum sesquioxides and their implications for the P sorption in subtropical soils. Applied Clay Science, 104:196-204, 2015.
• BOSCHETTI, A. N. G.; QUINTERO, G. C. E.; BENAVIDEZ, Q. R. A. Caracterização do fator capacidade de fósforo em solos de Entre Rios, Argentina. Revista Brasileira de Ciência do Solo, 22:95-99, 1998.
• BROGGI, F. et al. Adsorption and chemical extraction of phosphorus as a function of soil incubation time. Revista Brasileira de Engenharia Agrícola e Ambiental, 14:32-38, 2010.
• CAMARGO, L. A. et al. Mapping of clay, iron oxide and adsorbed phosphate in Oxisols using diffuse reflectance spectroscopy. Geoderma, 251-252:124-132, 2015.
• CARVALHO FILHO, A. et al. Iron oxides in soils of different lithological origins in Ferriferous Quadrilateral (Minas Gerais, Brazil). Applied Clay Science, 118:1-7, 2015.
• CERNANSKY, R. State-of-the-art soil. Nature, 517:258-260, 2015.
• CESSA, R. M. A. et al. Specific surface area and porosity of the clay fraction and phosphorus adsorption in two Rhodic ferralsols. Revista Brasileira de Ciência do Solo , 33:1153-1162, 2009.
• CHINTALA, R. et al. Phosphorus Sorption and Availability from Biochars and Soil/Biochar Mixtures. CLEAN - Soil, Air, Water, 42:626-634, 2014.
• COHEN-OFRI, I. et al. Modern and fossil charcoal: aspects of structure and diagenesis. Journal of Archaeological Science, 33:428-439, 2006.
• CONTE, E.; ANGHINONI, I.; RHEINHEIMER, D. S. Fósforo da biomassa microbiana e atividade de fosfatase ácida após aplicação de fosfato em solo no sistema plantio direto. Revista Brasileira de Ciência do Solo, 26:925-930, 2002.
• CORDELL, D.; DRANGERT, J. O.; WHITE, S. The story of phosphorus: Global food security and food for thought. Global Environmental Change, 19:292-305, 2009.
• CORNELISSEN, G. et al. Extensive sorption of organic compounds to black carbon, coal, and kerogen in sediments and soils: mechanisms and consequences for distribution, bioaccumulation, and biodegradation. Environmental Science & Technology, 39:6881-6895, 2005.
• CORNELL. R. M.; SCHWERTMANN, U. The iron oxides. Weinheim: VCH Verlag, 1996. 570p.
• COSTA, A. C. et al. Quantification and characterization of maghemite in soils derived from volcanic rocks in southern Brazil. Clays and Clay Minerals, 47:466-473, 1999.
• CURI, N.; FRANZMEIER, D. P. Toposequence of Oxisols from the central plateau of Brazil. Soil Science Society of America Journal, 48:341-346, 1984.
• DAWSON, C. J.; HILTON, J. Fertiliser availability in a resource-limited world: Production and recycling of nitrogen and phosphorus. Food Policy, 36:S14-S22, 2011.
• DE CAMPOS, M.; ANTONANGELO, J. A.; ALLEONI, L. R. F. Phosphorus sorption index in humid tropical soils. Soil Tillage Research, 156:110-118, 2016
• DEVAU, N. et al. Soil pH controls the environmental availability of phosphorus: Experimental and mechanistic modelling approaches. Applied Geochemistry, 24:2163-2174, 2009.
• DODD, R. J.; SHARPLEY, A. N. Recognizing the role of soil organic phosphorus in soil fertility and water quality. Resources Conservation Recycling, 105:282-293, 2015.
• ESSINGTON, M. E. Soil and water chemistry: an integrative approach. Boca Raton: CRC Press, 2003, 553p.
• FERNANDEZ-MENA, H., NESME, T., PELLERIN, S. Towards an Agro-Industrial Ecology: A review of nutrient flow modelling and assessment tools in agro-food systems at the local scale. Science Total Environmental, 543:467-479, 2016.
• FINK, J. R. et al. Mineralogy and phosphorus adsorption in soils of south and central-west Brazil under conventional and no-tillage systems. Acta Scientiarum. Agronomy, 36:379-387, 2014.
• FINK, J. R. et al. Adsorption and desorption of phosphorus in subtropical soils as affected by management system and mineralogy. Soil Tillage Research , 155:62-68, 2016a.
• FINK, J. R. et al. Diffusion and uptake of phosphorus, and root development of corn seedlings, in three contrasting subtropical soils under conventional tillage or no-tillage. Biology and Fertility of Soils, 52:203-210, 2016b.
• FIXEN, P. E. Reserva mundial dos nutrientes dos fertilizantes. IPNI: Informações agronômicas. 126:8-14, 2009.
• FONTES, M. P.; CAMARGO, O. A.; SPOSITO, G. Eletroquímica das partículas coloidais e sua relação com a mineralogia de solos altamente intemperizados. Scientia Agricola, 58:627-646, 2001.
• FONTES, M. P. F.; WEED, S. B. Phosphate adsorption by clays from Brazilian Oxisols: Relationships with specific surface area and mineralogy. Geoderma , 72:37-51, 1996.
• GÉRARD, F. Clay minerals, iron/aluminum oxides, and their contribution to phosphate sorption in soils - A myth revisited. Geoderma , 262, 213-226, 2016.
• GILBERT, N. Environment: The disappearing nutrient. Nature, 461:716-718, 2009.
• GLASER, B.; LEHMANN, J.; ZECH, W. Ameliorating physical and chemical properties of highly weathered soils in the tropics with charcoal - A review. Biology and Fertility of Soils. 35:219-230, 2002.
• GRANTHAM, J. Be persuasive. Be brave. Be arrested (if necessary). Nature , 491:303-303, 2012.
• GUAN, X-H.; CHANG, C.; CHEN, G-H. Competitive adsorption of organic matter with phosphate on aluminum hydroxide. Journal of Colloid Interface Science, 296:51-58, 2006.
• GUPPY, C. N. et al. Competitive sorption reactions between phosphorus and organic matter in soil: A review. Australian Journal of Soil Research, 43:189-202, 2005.
• GUZMAN, G. et al. Phytoavailability of phosphate adsorbed on ferrihydrite, hematite, and goethite. Plant and Soil, 159:219-225, 1994.
• HEINRICH, E. W. The geology of carbonatites. Nova York: Robert Krieger Publishing Company, 1980, 585p.
• HINSINGER, P. Bioavailability of soil inorganic P in the rhizosphere as affected by root-induced chemical changes: a review. Plant Soil, 237:173-195, 2001.
• HINSINGER, P. et al. Acquisition of phosphorus and other poorly mobile nutrients by roots. Where do plant K nutrition models fail? Plant Soil, 348:29-61, 2011.
• HUGHES, J. M.; RAKOVAN, J. The crystal structure of apatite, Ca₅(PO₄)₃(F,OH,F). Reviews in Mineralogy and Geochemistry, 48:1-12, 2002.
• HUMINICKI, D; HAWTHORNE, F. The crystal chemistry of the phosphate minerals. Reviews in Mineralogy and Geochemistry , 48:123-253, 2002.
• International Board of Soil Research and Management - IBSRAM. Acid tropical soils management network. Bangkok, Tailândia, 1985, 40p.
• INDA JUNIOR, A. V.; KÄMPF, N. Variabilidade de goethita e hematita via dissolução redutiva em solos de região tropical e subtropical. Revista Brasileira de Ciência do Solo, 29:851-866, 2005.
• JOHNSON, S.; LOEPPERT, R. H. Role of organic acids in phosphate mobilization from iron oxide. Soil Science Society of American Journal, 70:222-234, 2006.
• KÄMPF, N.; CURI, N. Argilominerais em solos brasileiros. In: CURI, N. et al. Tópicos em ciência do solo. Viçosa: Sociedade Brasileira de Ciência do Solo, 2003. v.3. p.1-54.
• KÄMPF, N.; SCHWERTMANN, U. The 5M - NaOH concentration treatment for iron oxides in soils. Clays and Clay Minerals, 30:401-408, 1982.
• KRELLER, D. I. et al. Competitive adsorption of phosphate and carboxylate with natural organic matter on hydrous iron oxides as investigated by chemical force microscopy. Colloids Surface-A, 212:249-264, 2003.
• LAIR, G. J. et al. Phosphorus sorption desorption in alluvial soils a young wethering sequence at the Danube River. Geoderma, 149:39-44, 2009.
• LEHMANN, J. A. A handful of carbon. Nature, 447:143-144, 2007.
• LEWIS, D. G.; QUIRK, J. P. Phosphate diffusion in soil and uptake by plants. Plant and Soil, 26:99-118, 1967.
• LIN, Y. et al. Migration of dissolved organic carbon in biochars and biochar mineral complexes. Pesquisa Agropecuária Brasileira, 47:677-686, 2012.
• LINDSAY, W. L.; VLEK, P. L. G.; CHIEN, S. H. Phosphate minerals. In: DIXON, J. B.; WEED, S. B. Minerals in soil environment, 2nd ed. Madison: Soil Science Society of America., 1989. p. 1089-1130.
• LIPTZIN, D.; SILVER, W. L. Effects of carbon additions on iron reduction and phosphorus availability in a humid tropical forest soil. Soil Biology and Biochemistry, 41:1696-1702, 2009.
• LIU, F.; HE, J.; COLOMBO, C. Competitive adsorption of sulfate and oxalate on goethite in the absence or presence of phosphate. Soil Science, 164:180-189, 1999.
• MARTINAZZO, R. et al. Fósforo microbiano do solo sob sistema plantio direto em resposta à adição de fosfato solúvel. Revista Brasileira de Ciência do Solo, 31:563-570, 2007.
• MESQUITA FILHO, M. V.; TORRENT, J. Phosphate sorption as related to mineralogy of a hydrosequence of soils from the Cerrado region (Brazil). Geoderma, 58:107-123, 1993.
• METSON, G. S.; BENNETT, E. M.; ELSER, J. J. The role of diet in phosphorus demand. Environmental Research Letters, 7:044043, 2012.
• MICHEL, F. M. et al. Ordered ferrimagnetic form of ferrihydrite reveals links among structure, composition, and magnetism. Proceedings of the National Academy of Sciences - PNAS, 107:2787-2792, 2010.
• MIKUTTA, R. et al. Stabilization of soil organic matter: association with minerals or chemical recalcitrance? Biogeochemistry, 77:25-56, 2006.
• NOVAIS, R. F.; SMYTH, T. J. Fósforo em solo e planta em condições tropicais. Viçosa: Universidade Federal de Viçosa, 1999. 399p.
• PARFITT, R. L. Phosphate reactions with natural allophane, ferrihydrite and goethite. Journal of Soils Science, 40:359-369, 1989.
• PAVINATO, P. S.; MERLIN, A.; ROSOLEM, C. A. Organic compounds from plant extracts and their effect on soil phosphorus availability. Pesquisa Agropecuária Brasileira, 43:1379-1388, 2008.
• PINTO, F. A. et al. P-sorption and desorption in savanna Brazilian soils as a support for phosphorus fertilizer management. Ciência e Agrotecnologia, 37(6):521-530, 2013.
• RANNO, S. K. et al. Phosphorus adsorption capacity in lowland soils of Rio Grande do Sul state. Revista Brasileira de Ciência do Solo, 24:21-28, 2007.
• REDEL, Y. D. et al. Phosphorus bioavailability affected by tillage and crop rotation on a Chilean volcanic derived Ultisol. Geoderma, 139:388-396, 2007.
• RHEINHEIMER, D. S.; ANGHINONI, I.; CONTE, E. Sorção de fósforo em função do teor inicial e de sistemas de manejo de solos. Revista Brasileira de Ciência do Solo, 27:41-49, 2003.
• RUSSEL, J. D. et al. Surface structures of gibbsite, goethite and phosphate goethite. Nature, 248:220-221, 1974.
• SACHS, J. et al. Monitoring the world's agriculture. Nature, 466:558-560, 2010.
• SANTOS, D. R.; GATIBONI, L. C.; KAMINSKI, J. Fatores que afetam a disponibilidade do fósforo e o manejo da adubação fosfatada em solos sob sistema de plantio direto. Ciência Rural, 38:576-586, 2008.
• SCHAEFER, C. E. G. R.; FABRIS, J. D.; KER, J. C. Minerals in the clay fraction of Brazilian Latosols (Oxisols): a review. Clay Minerals, 43:137-154, 2008.
• SCHWERTMANN, U.; KODAMA, H.; FISCHER, W. R. Mutual interactions between organic and iron oxides. In: HUANG, P. M.; SCHNITZER, M. Interactions of soil minerals with natural organics and microbes. Madison: Soil Science Society of America, 1986. p.223-250.
• SCHWERTMANN, U.; TAYLOR, R. M. Iron Oxides. In: DIXON, J. B.; WEED, S. B. Minerals in soil environments. 2.ed. Madison: Soil Science Society of America, 1989. p. 379-438.
• SHEN, J. et al. Phosphorus dynamics: From soil to plant. Plant Physiology, 156:997-1005, 2011
• SIBANDA, H. M.; YOUNG, S. D. Competitive adsorption of humus acids and phosphate on goethite, gibbsite and two tropical soils. Journal Soil Science, 37:197-204, 1986.
• SOUZA, E. D. et al. Soil quality indicators in a Rhodic Paleudult under long-term tillage systems. Soil and Tillage Research,139:28-36, 2014.
• SOUZA, I. G. et al. Mineralogia e susceptibilidade magnética dos óxidos de ferro do horizonte B de solos do Estado do Paraná. Ciência Rural, 40:513-519, 2010.
• SPARKS, D. L. Environmental Soil Chemistry. San Diego: Elsevier Academic Press, 2003. 352p.
• SPOSITO, G. The chemistry of soils. New York: Oxford University Press. 2008. 321p.
• STUMM, W. Chemistry of the solid-water interface. New York: John Wiley & Sons, 1992. 428p
• TENKORANG, F.; LOWENBERG-DEBOER, J. Forecasting long-term global fertilizer demand. Nutrient Cycling Agroecosystems, 83, 233-247, 2008.
• TIECHER, T. et al. Forms of inorganic phosphorus in soil under different long-term soil tillage systems and winter crops. Revista Brasileira de Ciência do Solo, 36:271-281, 2012.
• TIESSEN, H.; STEWART, J. W. B.; COLE, C. V. Pathways of phosphorus transformations in soils of differing pedogenesis. Soil Science Society of American Journal, 48:853-858, 1984.
• TOLLEFESON, J. How to feed a hungry world. Nature, 466:531-532, 2010.
• TORRENT, J.; BARRÓN, V.; SCHWERTMANN, U. Phosphate adsorption and desorption by goethites differing in crystal morphology. Soil Science Society of American Journal, 54:1007-1012, 1990.
• TORRENT, J.; SCHWERTMANN, U.; BARRÓN, V. Phosphate sorption by natural hematites. European Journal of Soil Science, 45:45-51, 1994.
• TORRENT, J.; SCHWERTMANN, U.; BARRON, V. Fast and slow phosphate sorption by goethite-rich natural materials. Clays and Clay Minerals, 40:14-21, 1992.
• VACCARI, D. A. Phosphorus, a looming crisis. Scientific American, 42-47, 2009.
• VALLADARES, G. S.; PEREIRA, M. G.; ANJOS, L. H. C. Adsorção de fósforo em solos de argila de atividade baixa. Bragantia, 62:111-118, 2003.
• WANG, X. et al. Characteristics of Phosphate Adsorption-Desorption Onto Ferrihydrite. Soil Science, 178:1-11, 2013.
• WILLIAMS, E. H.; REITH, J. W. S. Residual effects of phosphate and relative effectiveness on annual and rotational dressing. In: Residual value of applied nutrients. Londres: Min. of Agric. Fisheries and Food. Tech. Bull. 20:16-33, 1971.
• WORSTALL, T. Mineral demands: A shortage of fertilizer resources? Nature, 493:163-163, 2013.
• XU, G. et al. Biochar had effects on phosphorus sorption and desorption in three soils with differing acidity. Ecological Engineering, 62:54-60, 2014.
• YAGHI, N.; HARTIKAINEN, H. Enhancement of phosphorus sorption onto light expanded clay aggregates by means of aluminum and iron oxide coatings. Chemosphere, 9:1879-1886, 2013.
• YAN, J. et al. Preliminary investigation of phosphorus adsorption onto two types of iron oxide-organic matter complexes. Journal of Environmental Science, 42:152-162, 2015.
• YAO, Y. et al. Effect of biochar amendment on sorption and leaching of nitrate, ammonium, and phosphate in a sandy soil. Chemosphere, 89:1467-1471, 2012.
• ZAMUNER, E. C.; PICONE, L. I.; ECHEVERRIA, H. E. Organic and inorganic phosphorus in Mollisol soil under different tillage practices. Soil Tillage Research , 99:131-138, 2008.

Publication Dates

• Publication in this collection
  Jul-Aug 2016

History

• Received
  09 June 2016
• Accepted
  15 July 2016