The evolution of science, particularly in the past century, has clearly demonstrated the significance of P for all animal and plant life on earth. The process of the unfolding of the knowledge we have today regarding the
many chemical, biological, and management aspects of P has been tantalizing for scientists. The history of P research has been documented in countless articles that emanated from both developed and, increasingly, developing countries. The various reviews of P in the past half century have documented milestones in research achievements (e.g., Dalal, 1977;
Khasawnehet al., 1980; Larsen, 1967; Sims and Sharpley, 2005; Syerset al., 2008). The course of P research has undergone a paradigm shift from how we use P as a driver of crop production, as well as with implications for animal and human health, to concerns about the environmental implications of excess P use. Thus, in the following section, we have expanded on the importance of this vital element for terrestrial aquatic life and elaborated on the changing emphasis from agriculture to the environment, highlighting distinctions that exist depending on the status of countries economic development.
2.1. Phosphorus: An essential element for terrestrial life
Phosphorus is a ubiquitous and relatively abundant element in the Earth’s crust (11th most abundant), the average concentration of 1.18 g kg–1 (Donatello et al., 2010) being much higher than the average P content in soils, that is, 0.5 g kg–1in the top 50 cm (Smil, 2000). This concentration partly results from the non-uniform distribution of P on the Earth’s surface, where a limited number of deposits of phosphate rock (essentially, poorly soluble calcium phosphates) account for a significant portion of total P in the lithosphere. The abundance of P in the Earth’s crust is not matched by its relative content and a disproportionate but essential role in living organ- isms, including plants (Vance et al., 2003). Phosphorus, in the form of phosphate or its esters, is involved in many biological processes, including relevant structural functions as part of nucleic acids or phospholipids in membranes (Richardson, 2009; Yang and Finnegan, 2010). Phosphoesters have a key role in metabolic reactions, particularly those involved in energy transfer, a role that is underlined by the classical statement that of “photo- synthesis would be a fruitless tour de force if it were not followed by the phosphorylation of the sugar produced” (Deevey, 1970).
Under a non-limiting N supply in terrestrial and aquatic systems, P is usually the limiting nutrient for biomass development, mainly because the P in soil and water, ultimately derived from rock weathering, becomes bound with time in stable forms (Lagerstro¨m et al., 2009; Turner et al., 2007;
Vitousek et al., 2010; Wardle et al., 2004). This transformation from one chemical state (unstable) to another (stable) explains why, despite the fact that the total P content in soil is high compared to plant uptake, its low availability generally limits plant growth (Smil, 2000; Yang and Finnegan, 2010). Before the advent of inorganic P fertilizers, crop production relied on native soil P and the addition of locally available organic matter, mainly
animal manures (Cordellet al., 2009). Where manures were not available, the slow weathering of soils to produce plant-available P put a ceiling on crop growth and productivity.
The advent of chemical fertilizers represented an inflection point in global food production and consequently world population. Application of soluble P fertilizers, obtained by treating insoluble phosphate rock with acid, has been a common agricultural practice since the mid-19th century and has been a major contributor to expanded world food production since then (Delgado and Scalenghe, 2008; Keyzer, 2010; Richardson, 2009;
Stewart et al., 2005). However, only in the middle of the 20th century, the amount of P applied to the soil in the form of inorganic fertilizers exceeded the amount applied as manure and other organic residues at a global scale (Cordellet al., 2009; Smil, 2000). Increased crop yields, at least partially related to P fertilizer supply, have indicated that P uptake by crops increased by two to three times relative to that before 1950 (Pierzynski and Logan, 1993; Smil, 1999), with a global P extraction by crops around 12 Tg yr1(Smil, 2000). The transition from deficiency to excess with respect to the crop’s need for P was conditioned by various factors, in particular policies that promoted the low prices for fertilizers through subsidization and to some extent the absence of precise criteria for fertilizer application.
Fertilizer P application practices generally ignored the unique phenomenon of available P buildup in soils, with increased residual value for subsequent crops, an aspect that is later discussed in this review.
2.2. Agronomic and environmental considerations
As soils are inherently low or deficient in plant-available P, observations following the application of P fertilizer to soil in the mid 19th century indicated dramatic crop growth responses. The first P fertilizer experiments were conducted in Europe in the second half of that century (Delgado and Scalenghe, 2008; Merbachet al., 2000). The reactions that explain the long- term scarcity of available P in ecosystems also affect P that is applied as inorganic fertilizers: adsorption on the sorbing surfaces and precipitation in the form of metal phosphates (Frossardet al., 1995a,b). Only a fraction of the P applied to the soil remains phyto-available, its magnitude being difficult to predict in most cases. Uncertainty about the effectiveness of P fertilizers, low fertilizer prices, and incentives (subsidies) to maximize pro- duction in developed countries after the Second World War resulted in the application of fertilizer P far exceeding the crop’s needs (Delgado and Scalenghe, 2008). Consequently, the available P content in many agricul- tural soils of developed countries exceeded the critical values for P fertilizer response (MacDonald and Bennet, 2009; Torrentet al., 2007; Tunneyet al., 2003; Witherset al., 2001). Phosphorus loss from over-fertilized soils then became an extended environmental problem that contributed to water
eutrophication in the past few decades (Pierzynski and Logan, 1993;
Sharpleyet al., 1994, 2005; Tunney et al., 1997). This new phenomenon was particularly apparent in the intensive agriculture of Western Europe and in the eastern part of the USA.
The issues related to diffuse P loss from agricultural soils in developed countries have given rise to global research activity and scientific output as a basis for mitigation and corrective action. Thus, from 2000 to 2008, the European Research Framework Program has invested more than 6 million euros to fund P-related projects, most of which deal with the study of the P environmental question (Delgado and Scalenghe, 2008). The study of P loss processes at the profile and small-plot scale since the 1990s, and the descrip- tion and control of P losses at field and catchments scales since 2000, have been key topics in the ensuing research papers (Delgado and Scalenghe, 2008). In contrast, despite the overuse of P in developed countries, P is still a limiting factor for crop yield on more than 30% of the world’s arable land (Vanceet al., 2003), mostly in the less developed countries. This dichotomy is all the starker since most of the world’s population growth is in less developed countries where the need for enhancing food production through fertilizer use is greatest.
Thus, based on the number of people affected in the world, P is more an agronomic problem affecting food production than an environmental one (Roy et al., 2006). Inadequate P use has an indirect negative impact on human health and wellbeing. While the world’s undernourished people, mainly located in developing countries, account for about 15% of the global population (IFPRI, 2010), the population in these countries is expected to increase by 1800 million people from 1995 to 2020, an increase 40 times greater than that in developed countries (Keyzer, 2010; Roy et al., 2006).
Unfortunately, the obvious need to increase agricultural productivity in the less developed countries is not reflected in the amount of ongoing P research that focuses on agronomic or food-related issues; the paradigm shift is now solidly toward P-related environmental issues.
The problems derived from the low soil-P contents and the reduced P fertilizer inputs in many developing countries are often aggravated by the high P-fixing capacity of the soils, in particular in tropical and subtropical areas (Delgado and Scalenghe, 2008; Smil, 2000; Tiessen, 2005). Paradoxi- cally, some developing countries with low agricultural P inputs are rich in phosphate rock: Morocco, which has about one third of the mineable world P reserves (IFA, 2011), has an annual deficit of 8 kg P ha–1 in the cereal- growing areas; for example, 11.5 kg P ha1 uptake versus 3.5 kg P ha–1 applied on average (FAO, 2006). At a larger scale, 60% of the world’s phosphate rock reserves, and the largest exports of this product, are located in Africa, the continent with the most acute food shortage (Jasinski, 2010).
Many technical and economic and policy factors have contributed to this anomaly, beside limitations in the advisory service. Despite a trend for
removal of subsidies and trade barriers promoted by the World Bank, unsub- sidized agriculture in developing countries cannot sustain rational rates of P fertilizer use to increase agricultural productivity, especially so if logistic problems make the fertilizer much more expensive than in developed countries, for example, two to six times more expensive (Runge-Metzger, 1995). Nevertheless, a gradual political awareness is now gaining momentum regarding the importance of P supplies as a factor in mitigating world hunger.
2.3. Future phosphorus supplies for food production
Phosphorus is a nonrenewable resource. As with other natural resources such as oil and coal, assessment of reserves1 is fraught with uncertainty.
Estimation of world P reserves in high-grade phosphate rock ranges from 1.8 to 3.6 Pg2 P (Smil, 2000; Jasinski, 2010, and other sources cited by Van Vuurenet al., 2010). It has been suggested that these reserves may be depleted in less than 100 years at the current P consumption rate (Cordell et al., 2009; Smil, 2000; Van Vuuren et al., 2010; Vance et al., 2003).
A recent report by the International Fertilizer Development Center (IFDC;Van Kauwenbergh, 2010) estimated the P rock reserves (comprising various grades) to amount to 60 Pg or 8.1 Pg P (assuming that phosphate- rocks contain 30.9% P2O5), that is, about two to four times higher than values given by Van Vuurenet al.(2010). The study also highlighted the uncertainties involved in predicting duration of P supply, giving a conser- vative estimate of 300–400 years.
In 2009, according to data from theUSBM/USGS Mineral Commodities Summary (2011) 166 Tg3 of phosphate rock were produced worldwide (Fig. 1). China, USA, Morocco and Western Sahara, and Russia are the dominant producers of world phosphate rock. These countries contributed 72% to the overall production in 2009.
Most of the mined phosphate rock (around 80%) is used in fertilizer production (Stewartet al., 2005). The finiteness of this essential resource has now begun to dawn on society (Cramer, 2010). The consumption of P fertilizers increased from only 1 Tg P yr1during the late 1930s to a peak of 16.5 Tg P yr1 in 1988, followed by a 25% decline by 1993 due to decreasing fertilizer application rates in developed countries and to the sharp drop in fertilizer use in the post-Communist economies (Smil, 2000). Since then, consumption has increased to around 15 Tg P in 2009 and a further increase in the use of P fertilizer is expected in the coming
1 Commonlyreservesare distinguished fromresources. Reserves comprise phosphate rock that can be produced economically at the time when the assessment is done. Resources, on the other hand, comprise phosphate rock of any grade including stocks of which exploration is currently economically not viable.
2 1 Pgẳ1015g or 109tons.
3 1 Tgẳ1012g or 106tons.
decades (Cordell et al., 2009; Jasinski, 2010;Fig. 2) to eventually reach 20 Tg P yr1by 2030, further increasing to more than 28 Tg P yr1by 2100 (Tenkorang and Lowenberg-DeBoer, 2009; Van Vuurenet al., 2010).
China, India, Brazil, and the United States lead the top 10 list of the major P fertilizer-consuming countries, together using 68% of the world P fertilizer (Fig. 3). China alone accounts for 31%. Even though P fertilizer consumption of the developing countries increased almost linearly from 1961 to 2006—driven by the fast developing major consumer China and India—in the developing countries in the Mediterranean region, consump- tion peaked already in the early 1980s and since then remained more or less stable. This is illustrated for Turkey, Egypt, Morocco, and Syria (Fig. 4).
0 50 100 150 200
1994 1998 2002 2006 2010
Production (Tg yr–1) World total
China Other countries USA
Morocco and Western Sahara Russia
Figure 1 World phosphate rock production in 1994–2010 (USBM/USGS Mineral Commodities Summary, 1996–2011); 2010 data are estimates; phosphate rock by standard definition is assumed to contain 30.9% P2O5.
0 5 10 15 20
1960 1970 1980 1990 2000 2010 Consumption (Tg P yr–1)
World total Developing countries Developed countries
Figure 2 Developing and developed countries’ and world’s total phosphate fertilizer consumption (Tg P yr1) from 1961–2008 (IFADATA, 2011 recalculated from original data expressed in P2O5).
The depletion of P resources and its consequences for mankind is receiving increasing interest (Cramer, 2010), particularly after the rapid increase in fertilizer prices in 2007 and 2008 (Bouwman et al., 2009;
Cordell et al., 2009, Gilbert, 2009; Van Vuuren et al., 2010). However, this scarcity has been noted some decades ago, first gaining prominence in the seventies, but it has so far not elicited much action so far (Keyzer, 2010).
Nevertheless, the implications of world P reserves have recently been highlighted by the public media; in his thought-provoking book in “The Coming Famine,” Cribb (2010) added “peak” P to the list of vanishing resources such as oil, land, and water. Although different reasons have been
0%
8%
16%
24%
32%
40%
0 1 2 3 4 5
Consumption (Tg P)
China India Brazil USA
AustraliaPakistanViet NamCanadaRussia Argentina Consumption
Percent of world total (right axis)
Figure 3 Consumption of phosphate fertilizer (Tg P) in 2008 of the 10 major con- suming countries and percent of world total consumption (IFADATA, 2011 recalcu- lated from original data expressed in P2O5).
0 0.2 0.4 0.6 0.8
1960 1970 1980 1990 2000 2010 Consumption (Tg P yr–1)
Turkey Egypt Morocco Syria
Figure 4 Total phosphate fertilizer consumption (Gg P yr1) from 1961–2008 for Turkey, Egypt, Morocco and Syria (IFADATA, 2011 recalculated from original data expressed in P2O5).
given for the spike in fertilizer prices in 2007–2008, together with increased meat consumption in growing economies and bioethanol production (Cordell et al., 2009), restrictions in phosphate rock exports from China (Van Vuurenet al., 2010), which was the main phosphate rock producer in the world in 2008 (Jasinski, 2010; Vaccari, 2009), are probably a major reason for such increases. These developments underline the strategic character of this resource; United States, China, Morocco, and South Africa account for more than 80% of world’s P reserves (Jasinski, 2010; Vaccari, 2009) and its availability at a global scale can be influenced by political questions.
Under a scenario of no-trade barriers, relatively high P demand, and medium resource estimates, a major P depletion crisis in the next few decades is not likely to occur; however, P resources scarcity will probably manifest itself seriously at the end of the century (Van Vuurenet al., 2010).
The future demand for P will strongly depend on the type of agricultural practices (Vitouseket al., 2009); the expected depletion of reserves can be delayed in a scenario of highly efficient use of P resources (Bouwmanet al., 2009; Cordellet al., 2009). In any case, an increasing demand for P fertilizers is expected in the short run, mainly related to the increasing P fertilizer use in P-deficient countries, the need to increase food production due to the rapid population growth (mainly in developing countries), and the increas- ing consumption of meat and dairy products that indirectly require more P fertilizer in growing economies (Cordellet al., 2009; Keyzer, 2010; Stewart et al., 2005, Van Vuurenet al., 2010; Vitouseket al., 2009).
The increasing demand of fertilizers will coincide with an increased price of P fertilizers due to the progressive depletion of reserves; this will impact more negatively in developing countries than in developed countries where the demand has stabilized or in decreasing by agronomic (high P status of soils), environmental, or policy questions (including, changes in the subsidy policy adopted in Europe in early 1990s). In the developed countries, a rational administration of P stocks in agricultural soils (e.g., recycling P in animal and plant residues, and decreasing P loss from soil) and P recovery from different wastes (Szogiet al., 2010), particularly those of urban origin (Cordellet al., 2009; Donatelloet al., 2010; Nesetet al., 2009), is imperative.
In less developed countries it is unclear whether the need for an increased access to P fertilizers will be satisfied in a scenario of high fertilizer prices.
Therefore, future research on P should envision: (i) how to increase fertilizer efficiency, particularly in high P-fixing soils, (ii) how to produce more food with less P supply via increasing biological efficiency in soil P uptake (through crop selection, plant breeding, and the use of P mobilizing microorganisms), and (iii) the use of recycling strategies for all potential P sources, such as animal and human excreta, and crop residues. Besides investment in research, training, advisory and extension services should make a substantial contribution to more efficient use of fertilizers and increasing agricultural productivity in developing countries.
From the previous discussion, it is apparent that the world is divided into two categories with respect to P fertilizers: developed countries (e.g., North America, Europe, Australia and New Zealand) that have been characterized by excessive use, with harmful environmental implications, and developing resource-poor countries where fertilizer P use is nonexistent or so low as to restrict economic crop yields. An area of the world that is typical of the latter condition is the vast mainly arid and semi-arid region south and east of the Mediterranean, that is, West Asia and North Africa. While Mediterranean climatic conditions are found in other parts of the world, for example, southern Europe, California, Western Australia, and the southern tip of South Africa, the WANA region is unique in the sense of it largely being less developed economically.