RESEARCH AND ANALYSIS Global Flows and Environmental Impacts from a Consumption Perspective

Yi Liu, Gara Villalba, Robert U. Ayres, and Hans Schroder

Keywords: Summary cropland Human activities have significantly intensified natural phospho- rus cycles, which has resulted in some serious environmental problems that modern societies face today. This article at- substance flow analysis (SFA) tempts to quantify the global phosphorus flows associated waste management with present day mining, farming, animal feeding, and house- hold consumption. Various physical characteristics of the re- Supplementary material is available lated phosphorus fluxes as well as their environmental impacts on JIE Web site in different economies, including the United States, European countries, and China, are examined. Particular attention is given to the global phosphorus budget in cropland and the movement and transformation of phosphorus in soil, because these phosphorus flows, in association with the farming sec- tor, constitute major fluxes that dominate the anthropogenic phosphorus cycle. The results show that the global input of phosphorus to cropland, in both inorganic and organic forms from various sources, cannot compensate for the removal in harvests and in the losses by erosion and runoff. A net loss of phosphorus from the world’s cropland is estimated at about 10.5 million metric tons (MMT) phosphorus each year, nearly one half of the phosphorus extracted yearly.

Address correspondence to: Yi Liu Division of Environmental System Analysis Department of Environmental Science and Engineering Tsinghua University Beijing 100084, P.R. China [email protected]

c 2008 by Yale University DOI: 10.1111/j.1530-9290.2008.00025.x

Volume 12, Number 2 www.blackwellpublishing.com/jie Journal of Industrial Ecology 229 RESEARCH AND ANALYSIS

to algae becoming the dominant form of life in Introduction water. This, in turn, shapes one of today’s chal- The root of the deep conflicts between mod- lenges: responding to the increasing demand for ern society and the environment derives from food and agriculture’s growing need of nutrients anthropic interventions in material flows. It has without exhausting mineral resources been argued that human-induced material flows and threatening surface water quality. in modern economies are much more intensive This study analyzes and characterizes global than those in natural cycles (Klee and Graedel phosphorus flows. We examine both the natural 2004). Moreover, the paths and transformations cycle and the societal cycle, by using a statis- of the societal processing of materials are far more tical substance flow analysis method, which has complicated. Because rapid economic develop- been widely applied to quantitatively describe the ment is not yet in harmony with natural ecosys- physical profiles of modern societies (e.g., Klee tems, the underlying conflict between them has and Graedel 2004). In doing so, we give spe- become one of the most important factors influ- cial attention to phosphorus movement in the encing an increase in social welfare. To recon- soil system, which constitutes the largest phos- cile economy and ecology, it is essential to sys- phorus pool (reservoir) within our economy and tematically reflect on the societal mechanism of contributes to the majority of phosphorus losses material flows, thus ecologizing the economy by into the environment. The related environmen- shifting production and consumption paradigms tal issues caused by irrational, inappropriate, or to improve the overall efficiency of material inefficient phosphorus uses are subsequently dis- throughput (Liu 2005). cussed. The article closes with a discussion on Phosphorus is one of the most common ele- the ecological shifting of the societal phosphorus ments on earth and is essential to all living organ- flows. isms. A nonrenewable mineral, phosphorus re- serves exist only at the earth’s crust in the form of phosphate rock, which is currently being mined. The Human-Intensified In nature, phosphorus flows can be defined as a Phosphorus Cycles series of biogeochemical processes involving both The Natural Cycle mechanical transference and physical, chemical, and biological transformations. The natural phos- Inorganic Cycle phorus flows occur very slowly (one single loop Phosphorus circulates through the environ- of the natural cycle can take place over 1 mil- ment in three natural cycles. The first of these is lion years), remain relatively constant in quan- the inorganic cycle, which relates to phosphorus tity, and contribute to a stable closed loop. The in the crust of the earth. Over millions of years, situation has been significantly changed by hu- phosphorus has moved through the inorganic cy- man activities, however, in particular since in- cle, starting with the rocks, which slowly weather dustrialization. Historically, as one of the main to form soil, from which the phosphorus is gradu- plant nutrients, phosphorus was recycled in agri- ally leached from the land into rivers and onward cultural communities: Food was consumed close to the sea, where it eventually forms insoluble to its place of production, and the resulting an- and sinks to the sea floor as imal and human manures were applied to the sediment (Follmi 1996). There it remains until it same land. The growth of cities and the inten- is converted to new sedimentary rocks as a result sification of agriculture have depleted soil nutri- of geological pressure. On a timescale of hundreds ents, which has increased the need for synthetic of millions of years, these sediments are uplifted phosphorus . This has broken open the to form new dry land, and the rocks are sub- originally closed loop of the phosphorus nutri- ject to , completing the global cycle ent and has caused an increase in phosphorus (Schlesinger 1991). In addition, some phospho- in human societies. As a consequence, the nat- rus can be transferred back from the to the ural balance of production and consumption in land by fish-eating birds, whose droppings have the food chain is disturbed, which usually leads built up sizable deposits of phosphate as guano on

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Figure 1 The human-intensified global phosphorus cycles. Sources: modified from Liu et al. 2004a; Richey 1983; Smil 2000.

Pacific coastal regions and islands, and by ocean form each year (Emsley 2000). This amount currents that convey phosphorus from the seawa- cannot offset the annual losses of phosphorus ter to these regions. A simplified schematic of the from the land, however. If we take into account global phosphorus cycle is presented in figure 1. all four forms of phosphorus (dissolved and partic- The global cycle of phosphorus is unique ulate, organic and inorganic), the global annual among the cycles of the major biogeochemical phosphorus losses from the lithosphere into fresh- elements in having no significant gaseous com- waters are estimated at 18.7 to 31.4 MMT P/yr pounds. The biospheric phosphorus flows have (Compton et al. 2000). no atmospheric link from ocean to land. A small The uncertainty in the estimate is mainly due quantity of phosphorus does get into the at- to a lack of knowledge of the biogeochemical mosphere as dust or sea spray, accounting for processes of the particulate inorganic phosphorus 4.3 million metric tons1 of phosphorus per year (PIP), which constitutes the major component (MMT P/yr) and 0.3 MMT P/yr (Richey 1983), in the total loss. Not all of the eroding phos- respectively, but the amounts are several orders phorus can eventually reach the ocean. About less important than other transfers in the global 3.0 MMT P/yr is carried away by wind into the phosphorus cycle. The amount of 4.6 MMT P/yr atmosphere, and at least 25% of that is rede- of atmospheric phosphorus deposition, being bal- posited on adjacent cropland and grassland or anced by the phosphorus carried by the wind and on more distant alluvia (Smil 2000). Conse- the sea spray, cannot offset the endless drain of quently, the amount of phosphorus transported this element from the land due to erosion and by freshwaters into the ocean is probably in the river transport (Schlesinger 1991). Fortunately, range of 12 to 21 MMT P/yr. This result agrees increased anthropogenic mobilization of the ele- with the most likely value of 17 to 22 MMT ment has no direct atmospheric consequences. P/yr given by some previous estimates (Emsley Nearly all the phosphorus on land is originally 1980; Meybeck 1982; Richey 1983; Sposito 1989; derived from the weathering of calcium phos- Howarth et al. 1995). The riverborne transport of phate minerals, especially [Ca5(PO4)3 phosphorus constitutes the main flux of the global OH]. Around 13 MMT P/yr of this is released to phosphorus cycle. The loss, as a result of erosion,

Liu et al., Global Phosphorus Flows from Cansumption 231 RESEARCH AND ANALYSIS , and runoff, must be consider- (see the companion article on phosphorus pro- ably higher than it was in prehuman times. It can duction by Villalba et al. [2008]). The phospho- be argued that the human-intensified phosphorus ric acid is further processed to produce fertilizers, flux caused by wind and water erosion is at least food-grade and feed-grade additives, and deter- double (Compton et al. 2000) or even three times gents. Other marginal applications include metal (Smil 2000) its prehistoric level.2 surface treatment, corrosion inhibition, flame re- tardants, water treatment, and ceramic produc- Organic Cycles tion. Despite such widespread use, the latter ap- Imposed on the inorganic cycle are two or- plications represented only about 3% of the total ganic cycles that move phosphorus through liv- consumption of various in the 1990s ing organisms as part of the food chain. These (CEEP 1997). are a land-based phosphorus cycle that transfers The global consumption of all phosphate fer- it from soil to plants, to animals, and back to soil tilizers surpassed 1 MMT P/yr during the late again and a water-based organic cycle that circu- 1930s. After reaching 14 MMT P/yr in 1980, lates it among the creatures living in rivers, lakes, the world consumption of phosphate fertilizers and seas. The land-based cycle takes a year, on has been relatively stable. It was 14.8 MMT P average, and the water-based organic cycle only (34 MMT P2O5) in statistical year 2002–2003, weeks. The amount of phosphorus in these two and it slightly decreased to 13.8 MMT P (31.5 cycles governs the of living forms that MMT P2O5) in statistical year 2003–2004 (FAO land and sea can sustain. 2005) roughly accounting for 78% of the global The amount of phosphorus in the world’s soils production of phosphorus from phosphate rock. is roughly 90 × 103 to 200 × 103 MMT P, accord- As the top fertilizer-processing country, China ing to various estimates (Emsley 1980; Meybeck contributed 22% and 28%, respectively, to the 1982; Richey 1983; Filippelli 2002). Although world production and consumption; the top three the total phosphorus content of soils is large, only economies (China, United States, and India) ac- a small fraction is available to biota in most soils. counted for one half of the world consumption. This constitutes an available phosphorus pool The area of the world’s current cropland is about containing 1,805 to 3,000 MMT P (Grove 1992), 1.4 billion hectares3 (FAO 2005), which implies most likely 2,000 to 2,600 MMT P (Emsley 1980; that the global fertilizer application intensity av- Richey 1983). A larger amount, in the range of erages 10 kg P/ha. The application rate varies sig- 27 × 106 to 840 × 106 MMT P, can be found in nificantly among continents, ranging from about the . The sea water contains 80 × 103 to 3 kg P/ha in Africa to over 25 kg P/ha in Europe. 120 × 103 MMT P, and the rest is accumulated Among western European countries, application in sediments (Emsley 1980; Richey 1983; Grove levels range from 8.7 kg P/ha in Denmark and 1992; Filippelli 2002; Smil 2002). Sweden to 34 kg P/ha in Ireland (Johnston and The ocean water loses phosphorus continu- Steen 2000). ally in a steady drizzle of detritus to the bottom, where it builds up in the sediments as insolu- Crop Harvests ble calcium phosphate. Despite the geological re- The use of phosphates to nourish agricultural mobilization, there is a net annual loss of mil- soils aims to replenish the removal of phosphorus lions of tons of phosphate a year from the marine from soil by harvests and erosion losses. Adopt- . Thus, the ocean sediments are by far ing the average phosphorus contents in crops and the largest stock in the biogeochemical cycles of the harvest index (Smil 1999), the global crop phosphorus. production harvested 12.7 MMT P from soils in 2005, as shown in table 1, on the basis of the world agricultural production database (FAO 2006a). A The Societal Cycle study of Chinese phosphorus flows suggested that Global Phosphate Consumption the national harvest in 2000 removed 3.4 MMT Phosphate rock is initially converted to phos- P from croplands, on the basis of a set of domestic phoric acid (P2O5) by reaction with sulfuric acid data for the phosphorus contents and the harvest

232 Journal of Industrial Ecology RESEARCH AND ANALYSIS

Ta bl e 1 Allocation of phosphorus in world harvest in 2005 Harvested crops Crop residues

Fresh Dry P in grains Residues P in straws Total P Crop weight (MMT) matter (MMT) (MMT P) (MMT) (MMT P) uptake (MMT P) Cereals 2,239 1,968 5.9 2,947 2.9 8.9 Sugar crops 1,534 476 0.5 370 0.7 1.2 Roots and tubers 713 143 0.1 219 0.2 0.4 Vegetables 882 88 0.1 147 0.1 0.2 Fruit 505 76 0.1 126 0.1 0.2 Pulses 61 58 0.3 61 0.1 0.4 Oil crops 139 102 0.1 92 0.1 0.2 Other 100 80 0.1 200 0.2 0.3 Forages 500 1.0 0 0.0 1.0 Total 6,173 3,491 8.2 4,163 4.5 12.7

Sources: Harvest data are derived from FAO (2006a); conversion coefficients are adopted from Smil (1999). Note: MMT = million metric tons; P = phosphorus.

index (Liu 2005). These two estimates agree that the United States, beef cattle, dairy cattle, swine, (1) cereals accounted for a major part of the har- and poultry produced 1.7 MMT P contained in vested phosphorus (i.e., 70% at the global level animal manures in 1997, of which about half and/or 68% in China) and (2) about two-thirds of was produced by confined animals (Kellogg et al. the annually harvested phosphorus is contained 2000). The livestock population in the United in grains, and the rest is contained in straw and States accounted for 7% of the world total in other agricultural waste. 1997, and the proportion has remained fairly con- Given that natural weathering and atmo- stant. On this basis, the global production of an- spheric deposition, as discussed elsewhere, can- imal wastes would be 24.0 MMT P/yr. However, not compensate for the amount of phosphorus the real figure may be somewhat smaller, because uptake from soils, application of phosphates, in the animals in United States are exceptionally both inorganic and organic forms, becomes es- well fed. For this reason, Smil’s (2000) estimate sential to sustain today’s harvests. Although most of global production of 16 to 20 MMT P/yr in inorganic phosphates applied to soils come from animal wastes, obtained by applying an average chemical fertilizers, the means of organic phos- concentration of 0.8% to 1% of phosphorus for phorus reuse are diverse. The most direct means both confined and unconfined animal wastes, is is to recycle crop residues in situ. If we assume that probably more accurate. roughly half of the annual output of crop residues Only the phosphorus in wastes from con- (mostly cereal straw) is not removed from fields, fined animals is considered to be recyclable for the amount of the direct reuse of crop residues is croplands, whereas unconfined animal wastes about 2.2 MMT P/yr. mainly return to pastures. If we assume that an- imal biomass remains relatively constant, the Livestock and Animal Wastes amount of phosphorus in animal wastes is equal Animal wastes have been applied as organic to the consumption of phosphorus contained in manure in traditional farming and remain a rela- all kinds of feeds. According to the global Food tive large source of recyclable phosphorus in mod- Balance Sheet (FBS) in 2003, livestock con- ern agriculture. A rough estimate of global pro- sumed 36% of the harvested cereals (exclud- duction of animal wastes is needed, because de- ing the amount of cereals processed for beer), tailed inventories of nutrient budget of livestock 21% of the harvested starchy roots, and 20% husbandry are not available for most countries. of the harvested pulses (FAO 2006b). Conse- According to the latest national survey data from quently, the annual livestock consumption of

Liu et al., Global Phosphorus Flows from Cansumption 233 RESEARCH AND ANALYSIS phosphorus in the harvests accounted for about If we assume that the world human body mass 2.9 MMT P/yr. averages 45 kg/capita (reflecting a higher propor- Some part of crop residues is used as an- tion of children in the total population of low- imal fodder. The reuse ratio of crop residues income countries) and phosphorus content in as fodder varies considerably, however. For in- the human body averages 470 g P/capita, this im- stance, it was reported that the percentage of plies a global anthropomass (i.e., aggregate mass crop residues—mostly the straws of rice, wheat, of humankind) that contains approximately 3.0 and corn (maize)—used as fodder ranged from MMT P. The typical daily consumption is about 3.6% in Shanghai to 42.8% in Gansu province in 1,500 mg P/capita for adults (CEEP 1997). This 2000 in China, depending on crop and livestock is well above the dietary reference intake (DRI), species, farming and feeding traditions, and local the amount a human individual should take in economic profiles, and averaged 22.6% across the each day, as recommended by the Food and Nu- nation (Gao et al. 2002; Han et al. 2002). Given trition Board of the Institute of Medicine, a part that over 70% of world livestock are raised in de- of the U.S. National Academy of Science. The veloping countries, where commercial feeds are U.S. recommended intakes are 700 mg/capita for less used, the global rate of crop straws adults over 18 years of age, 1,250 mg/capita for as fodder is probably about 25%, leading to an young adults between 9 and 18 years of age, and absolute quantity of 1.1 MMT P/yr. 500 mg/capita for children. Another major source of animal daily phos- A similar estimate for China is derived from phorus intake is via feed additives. Around 6% of the PHOSFLOW model (a static phosphorus flow the global yield of phosphoric acid has been pro- balance based on a substance flow analysis ap- cessed as animal feed-grade additives since 2000 proach): The individual daily intake of phospho- (Brasnett 2002; PotashCorp 2004). This consti- rus was 1,400 mg P/capita for urban residents and tutes an annual phosphorus flux of 1.0 MMT P/yr 1,470 mg P/capita for rural residents in 2000 (Liu input to livestock husbandry. 2005). This exceeds the DRI of 1,000 mg/capita If we add all three sources above, the global recommended by the Chinese Nutrient Society. livestock consumption of phosphorus amounts to In addition, livestock products provided 30% of about 5.0 MMT P each year. When we take into the daily phosphorus intake for Chinese urban account the recycling of various industrial by- residents and 14% of that for the rural popula- products and kitchen organic wastes (which is tion (Liu 2005). prevalent in rural family-based farms in devel- Although the phosphorus content of anthro- oping countries), this figure could be as much pomass is marginal in comparison with that of soil as 20% higher, resulting in a total of 6.0 MMT biota or ocean biota, the environmental conse- P/yr. Of course, the phosphorus flux to livestock quences can still be significant. Given the annual of 6.0 MMT P/yr is mainly consumed by animals growth of 78.4 million since in confined facilities, whereas the world’s culti- 2000 (UN 2004), the net accumulation of phos- vated and natural pastures provide a major source phorus in the global anthropomass is around 0.04 of phosphorus for unconfined animals. If we as- MMT P/yr. Compared with the global consump- sume that 1.0 MMT P/yr goes to unconfined ani- tion of phosphorus in foods, the slight increase of mals in pastures, about 5.0 MMT P/yr consumed phosphorus in the anthropomass stock implies a by confined animals gives an approximation for low assimilation rate of about 0.5%. If we as- the maximum potential of recoverable phospho- sume a global average dietary consumption of rus for croplands. If one half of the organic phos- 1,400 mg P/capita, human excreta contains about phorus in confined animal wastes is subject to 3.3 MMT P/yr, of which urban and rural popula- recycling, animal manure is responsible for about tions generate 1.6 MMT P/yr and 1.7 MMT P/yr, 2.5 MMT P/yr returns to global croplands. respectively. Application of human excreta as organic fer- Food Consumption and Human Wastes tilizer is common both in Asia and in Europe The third source of organic phosphorus avail- but less prevalent elsewhere in the world. The able, in principle, for cropland is human waste. nutrient linkage between farmers and croplands

234 Journal of Industrial Ecology RESEARCH AND ANALYSIS has been relatively stable, but the human wastes The primary source of phosphorus taken up by in urban areas are less recycled than in rural ar- plants and is dissolved in water eas. In China, less than 30% of human waste (soil solution). The equilibrium concentration of in urban areas was recycled for agricultural uses phosphate present in soil solution is commonly in the late 1990s (Chen 2002). This percentage very low, below 5 μMol (Condron and Tiessen dramatically decreased from 90% in 1980 (Chen 2005). At any given time, soil water contains only and Tang 1998). In contrast, about 94% of hu- about 1% of the phosphorus required to sustain man wastes in rural areas were returned to crop- normal plant growth for a season (Emsley 2000). lands in the 1990s (Pan et al. 1995). In European Thus, phosphates removed by plant and micro- countries, the recycling rate of urban sewage av- bial uptake must be continually replenished from eraged about 50% over the 1990s (EEA 1997; the inorganic, organic, and microbial phospho- Farmer 1999). Globally, it could be appropriate rus pools in the soil. These continuous processes to assume that about 20% of urban human wastes dominate contemporary agricultural production and about 70% of rural human wastes are recy- to remove about 8.2 kg P/ha from cropland each cled at present. Therefore, recycled human wastes year on a world average (based on our own esti- amount to 1.5 MMT P/yr. mate) and commonly 30 kg P/ha from the U.S. When we add the quantities of the phospho- and European fertile agricultural soils (Johnston rus recycled as crop residues, animal manures, and Steen 2000). and human wastes, the total organic fertilizers ap- Each phosphate mineral has a characteris- plied to croplands amount to 6.2 MMT P/yr. This tic solubility under defined conditions (Burke is equivalent to 45% of the amount applied in et al. 2004). The solubility of many compounds the form of inorganic fertilizers. Thus, the global is a function of acidity (pH). A typical solubil- input of phosphorus to croplands is probably ity diagram that illustrates phosphate solubility 20 MMT P/yr in total, or 1.6 times the amount of against pH is shown in figure 2. An increase in the phosphorus removed from the soil by harvest- pH can release sediment-bound phosphorus by ing. This leads to a net accumulation of 7.3 MMT increasing the charge of iron and aluminum hy- P/yr or 4.7 kg P/ha/yr in global soils, disregarding drous oxides and therefore increasing the compe- erosion and runoff losses. tition between hydroxide and phosphate anions for sorption sites. Also, organic acids can inhibit Phosphates in Soil and Losses Phosphates in Soil The distribution, dynamics, and availability of phosphorus in soil are controlled by a com- bination of biological, chemical, and physical processes. These processes deserve special atten- tion, as a considerable proportion of the applied phosphate is transformed into insoluble calcium, iron, or aluminum phosphates. On average, only a small proportion, perhaps 15% to 20% of the total amount of phosphorus in the plant, comes directly from the fertilizer applied to the crop. The remainder comes from soil reserves (John- ston and Steen 2000). For most of the 20th cen- tury, farmers in western countries were advised to add more than double the amount of phosphate Figure 2 The solubility of phosphorus in the soil required by a crop, because these immobilized solution as a function of pH. The thick line indicates calcium, iron, and aluminum phosphates had the minimum boundary of the solubility of been assumed to be permanently unavailable to phosphorus given a certain pH. plants. Source: adapted from Schlesinger 1991.

Liu et al., Global Phosphorus Flows from Cansumption 235 RESEARCH AND ANALYSIS

At later stages of soil development, phospho- rus is progressively transformed into less-soluble iron- and aluminum-associated forms, and or- ganic phosphorus contents of the soil decline (Tiessen and Stewart 1985). At this stage, almost all available phosphorus is found in a biogeo- chemical cycle in the upper soil profile, whereas phosphorus in lower depths is primarily involved in geochemical reactions with secondary sedi- ments (Schlesinger 1991). When the dissolved phosphates supply to growing biomass is abundant, a net immobi- lization of inorganic phosphorus into organic Figure 3 Phosphates in the soil vary with soil forms will occur. Conversely, inadequate inor- development. ganic phosphorus supply will stimulate the pro- Source: adapted from Emsley 1980. duction of and the mineralization of labile organic forms of phosphorus for microbial uptake (Tiessen and Stewart 1985). A continu- the crystallization of aluminum and iron hydrous ous drain on the soil phosphorus pools by cultiva- oxides, reducing the rate of phosphorus occlu- tion and crop removal will rapidly deplete both sion (Schlesinger 1991). The production and re- labile inorganic and organic phosphorus in soils. lease of by fungi explains their impor- Allowing soil reserves of readily available tance in maintaining and supplying phosphorus phosphorus to fall below a critical value, deter- to plants. mined by field experiments, can result in a loss The relative sizes of the sources and stocks of of yield. The turnover of available phosphates by phosphate in soil change as a function of soil de- plants in soil solution is determined by rates of velopment, as shown in figure 3. The buildup of releases of phosphorus from insoluble forms to organic phosphates in the soil is the most dra- soluble phosphates. All kinds of soil particles can matic change. As time goes on, this becomes the contribute to this process, and in some cases it chief reservoir of reserve phosphate in the soil. In is not only chemical balance that maintains the most soils, organic phosphates range from 30% supply but the action of microbes and enzymes to 65% of total phosphorus, and they may ac- that release phosphate from organic debris in the count for as much as 90% of the total, especially soil. It is believed that the biogeochemical con- in tropical soils (Condron and Tiessen 2005). trol of phosphorus availability by symbiotic fungi The reasons for this are organic phosphates’ is a precursor to the successful establishment of insolubility and chemical stability. Several au- plants on land (Schlesinger 1991). thors have noted that acidic soils tend to ac- Our existing knowledge, however—briefly cumulate more total organic phosphorus than discussed above—cannot yet provide a compre- do alkaline soils. This is almost certainly be- hensive understanding of the complex move- cause organic phosphates react with iron and alu- ments and transformations of phosphorus, espe- minum under acidic conditions and become in- cially of its organic forms (Turner et al. 2005). soluble (Harrison 1987). Being the salts or metal This hampers the efficient application of phos- complexes of phosphate esters, they release their phate fertilizers and the efficient control of phos- phosphate by hydrolysis, but only very slowly. phorus losses. Phosphate esters can have half-lives of hydrolysis of hundreds of years. This process can be greatly Phosphorus Losses speeded up by the action of enzymes Phosphorus is lost from croplands via erosion in the soil, whose function is to facilitate reac- or runoff. Quantifying phosphorus losses in erod- tion by catalyzing it (Quiquampoix and Mousain ing agricultural soils is particularly uncertain, as 2005). erosion rates vary widely even within a single

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field. Another cause of uncertainty is that few na- Assuming a global erosion rate averaging tions take comprehensive, periodic inventories of 25 t/ha gives the soil loss of 38,500 MMT/yr from their soil erosion. cropland (cf. table 1). Furthermore, most of the The phosphorus loss from croplands can be loss is permanent and may not be replenished by roughly estimated on the basis of the amount of weathering. For instance, the excessive soil loss, topsoil erosion and average phosphorus content. a rate that would impair long-term crop produc- A crop takes up the majority of the nutrients it tivity, was estimated at about 25,400 MMT/yr requires from topsoil. The topsoil is often iden- around 1980 (Brown and Wolf 1984). tified as the “plough layer”—that is, the 20 to Erosion from pastures is commonly less inten- 30 cm depth of soil that is turned over before sive than that from ploughed fields. Soil losses, seedbed preparation. The volume of topsoil in the however, have been greatly increased by over- plough layer is around 2,500 cubic meters4 (m3) , which now affects more than half (i.e., per hectare and weighs approximately 2,000 tons at least 1,720 million hectares) of the world’s per- (Johnston and Steen 2000). A ton of fertile top- manent pastures, with a high erosion rate of soil can contain 0.6 to 3.0 kg of phosphorus, 15 t/ha each year (Smil 2000). This leads to mainly based on U.S. and European agricultural 25,800 MMT/yr of the soil loss from overgrazed practices (Troeh et al. 1991; Johnston and Steen pastures. Together with the amount of soil loss 2000). from cultivated grassland, the world’s permanent It has been estimated that the annual soil pastures lose their topsoil at an annual rate of erosion from agricultural systems of the United 34,400 MMT/yr. When we add the losses from States, China, and India was 3,000 MMT/yr, cropland and pastures, the world soil erosion from 5,500 MMT/yr, and 6,600 MMT/yr, respectively agricultural areas amounts to 72,900 MMT/yr in (Pimentel 2006). As these three countries hold total, or 15 t/ha/yr on average. This is similar to 23% of global agricultural lands, the global soil previous estimates, as discussed above. erosion could reach 66,600 MMT/yr. Some of Allowing for the poor condition of topsoil in the most serious soil erosion takes place in the developing countries, it might be appropriate to agricultural systems of Southeast Asia, Africa, assume that the global phosphorus content in and South America (Yang et al. 2003). Hence, topsoil averages about 0.5 kg P/t, or 1.0 t P/ha. the real global soil erosion loss could be even This gives world phosphorus losses at 19.3 MMT higher, perhaps as much as 75,000 MMT/yr P/yr from cropland and at 17.2 MMT P/yr from (Myers 1992). pastures, respectively, as shown in table 2. The erosion intensity from croplands varies The loss of applied inorganic considerably among countries, ranging from 0.5 phosphate fertilizer varies significantly with a to 400 t/ha-yr (Pimentel et al. 1995). Worldwide, number of agronomic factors. Typical runoff rates soil erosion is highest in Asia, Africa, and South of phosphorus in European countries range from America, averaging 30 to 40 t/ha-yr of soil loss 0.2% to 6.7%, an average of 3.5% (Haygarth (Taddese 2001). Smil (2000) has suggested that 1997; Hart et al. 2004). Worldwide, the maxi- the global average erosion rate is at least 20 t/ha- mum rate can reach 10% under certain soil char- yr. The lowest erosion rates occur in the United acteristics and climatic conditions (Waddell and States and Europe, where they average about Bower 1988). Roughly, the world total phosphate 10 t/ha each year (USDA 2000a, 2000b). It is fertilizer application can lead to a loss of 0.5 MMT evident that soil erosion in the United States has P/yr in surface runoff. been reduced by soil conservation policies: A na- tional survey showed that the total soil erosion Phosphate Balance in Cropland between 1982 and 1992 decreased by 32% (Uri The national phosphorus balance varies sig- 2001). The annual sheet and rill erosion rate in nificantly from one country to another, due to dif- the United States fell from an average of 10 t/ha ferences in the use of mineral fertilizers and ma- in 1982 to 7.7 t/ha in 1992, and the wind erosion nure and differences in animal husbandry prac- rate fell from an average of 8.1 t/ha-yr to 5.9 t/ha- tices. Broadly speaking, in developing countries yr over the same period. soils tend to be deficient in phosphorus, whereas

Liu et al., Global Phosphorus Flows from Cansumption 237 RESEARCH AND ANALYSIS

Ta bl e 2 Global soil erosion and phosphorus losses Ta b l e 3 Phosphorus budget for the world’s from agricultural land (2003) cropland (2004) Permanent pasture Annual fluxes Contents Cropland Overgrazed Ordinary Flows (MMT P) Total area 1,540 1,720 1,720 Inputs 22.9 (million ha) Weathering 1.6 Soil erosion Atmospheric deposition 0.4 Erosion rate 25 15 5 Synthetic fertilizers 14.7 (t/ha/yr) Organic recycling 6.2 Erosion 38,500 25,800 8,600 Crop residues 2.2 quantity Animal wastes 2.5 (MMT/yr) Human wastes 1.5 Phosphorus loss Removals 12.7 Pcontentin 0.5 0.5 0.5 Crops 8.2 topsoil (kg Crop residues 4.5 P/ha) Losses 19.8 P loss (MMT 19.3 12.9 4.3 Erosion 19.3 P/yr) Runoff 0.5 Balance −9.6 Note: MMT = million metric tons; P = phosphorus. Input shares (%) Fertilizer application 64.2 Organic recycling 27.1 in developed countries the phosphorus content Uptake efficiency (%) 64.6 of the soils is adequate or even excessive. If we take into account applications of mineral fertil- izers and manure, the balance for some western flows associated with the farming sector, which European countries is positive, particularly in the is the most intensive and complicated subsystem Netherlands, where it exceeds 39 kg P/ha each of the anthropogenic phosphorus cycle. year. For the majority of western European coun- tries, the phosphorus balance ranges from 8.7 Environmental Impacts of to 17.5 kg P/ha annually (Johnston and Steen Phosphorus Uses 2000). China, one of the largest agricultural sys- tems in transition, also achieved a positive bal- Phosphorus-related fall ance around 1980 at the national level, in parallel into a broad range. Some are caused by inap- with increasing application of synthetic fertiliz- propriate use of the material; some are not. Eu- ers (Wang et al. 1996; Jin and Portch 2001). In trophication, regarded as the most immediate en- 2000, the national surplus of phosphorus in Chi- vironmental consequence of extensive phospho- nese soils was estimated at an average of 16 kg rus usage in contemporary societies, has received P/ha (Liu et al. 2007). wide attention. It is not the whole story, how- To balance the phosphorus budget for the ever, and other issues deserve to be taken into world’s cropland, two natural inflows of phospho- consideration. Here, our discussion is devoted to rus to croplands should be taken into account. On a broad socioeconomic context, focusing on five the basis of the ratio of cropland area to world phosphorus-related environmental issues: min- total land areas, weathering and atmospheric de- eral reserve conservation, soil erosion and degra- position contribute 2.0 MMT P/yr as inputs to dation of soil fertility, animal waste management, world croplands. sewage and detergent use, and . The world phosphorus budget for cropland is summarized in table 3. Although the magnitudes Mineral Conservation of recycling of animal wastes and soil erosion need further verification, the budget provides a com- If the annual mining rate of about 19.5 prehensive overview of the global phosphorus MMT P/yr remains constant, the world’s known

238 Journal of Industrial Ecology RESEARCH AND ANALYSIS phosphate reserves could be exhausted in about sion is induced by human activity, an increase of 120 years. Moreover, it has been projected that 17% since the early 1900s (Yang et al. 2003). the utilization trend is unlikely to decline in the In contrast to the erosion loss, a huge amount next 30 years. It will instead probably increase at of phosphorus has been mobilized in cultivated the rate of 0.7% to 1.3% annually (FAO 2000). soils. Contemporary scientific knowledge can- This strongly suggests that phosphate rock, as a not fully explain the complex transportation of finite, nonrenewable resource, may be exhausted phosphorus between plant roots, soil waters, and in a much shorter time. It has been shown that soil . More complete understanding of the global average phosphorus content in raw these processes might suggest a possibility of con- ores dropped to 29.5% in 1996 from 32.7% in trollable remobilization of soil phosphorus that 1980 and that global reserves can sustain the cur- would benefit the environment via reducing both rent mining intensity for only another 80 years the input of fertilizers and the loss of phosphorus (Isherwood 2000). Some phosphorus-rich de- from soils. posits around the world could be depleted much sooner. China’s phosphorus reserves, for instance, Animal Wastes constitute 26% of the world’s total reserve base, second only to Morocco and the western Sahara Livestock husbandry, in particular large, in- (USGS 2006). With a high intensive extraction tensive feedlots, has become a major problem activity as well as losses incurred during min- both for recycling of organic phosphorus and for ing, the basic reserve of the nation’s phospho- emission of phosphorus pollutants. Worldwide, rus resources (i.e., 4,054 million tons with aver- the structure of animal agriculture has changed age P2O5 content of 17% to 22%) could be ex- as livestock are concentrated in fewer but larger hausted in 64–83 years (Liu 2005). As a result, operations (GAO 1995; EEA 2003a; Ribaudo the Ministry of Land and Resources in China et al. 2003). In the United States, in spite of the counts phosphorus as one of the unsustainable re- loss of nearly a fourth of the livestock operations sources for China’s development in this century. between 1982 and 1997, the total number of an- Certainly, the larger reserve base and probably imal units5 has remained fairly constant at about more reserves to be discovered in the future guar- 91 to 95 million (Kellogg et al. 2000). In China, antee a longer life span of the extraction. Even a large number of intensive feedlots appeared in so, the deposits of phosphorus in the lithosphere suburbs and rural areas during the last decade. Ac- will inevitably be depleted before new igneous or cording to a national investigation, the output of sedimentary rocks to be formed via the biogeo- hogs, meat chickens (broilers), and egg chickens chemical process at the timescale of millions of (layers) produced by intensive feedlots and farms years. accounted for 23%, 48%, and 44% of the national total in 1999, respectively (SEPA 2002). Soil Erosion As livestock operations have become fewer, If our estimates are reasonably accurate, one larger, and more spatially concentrated in specific of the most important results derived from the areas, animal wastes have also become more con- phosphorus budget is that world cropland is los- centrated in those regions. This leads to a con- ing phosphorus at a surprising rate of 9.6 MMT siderable phosphorus surplus in manure, as the P each year. This massive loss from croplands amount of manure nutrients relative to the as- is mainly caused by wind and water erosion similative capacity of land available on farms for of topsoil. Soil erosion has been recognized as application has grown, especially in specific high- one of the most serious environmental crises production areas (Steinfeld et al. 1998; Poulsen challenging the world (Brown and Wolf 1984). et al. 1999; OECD 2001; Gerber et al. 2005). It is estimated that 10 million hectares of crop- Consequently, off-farm manure export require- land are abandoned annually worldwide due to ments are increasing. lack of productivity caused by the soil erosion But because of its bulk, uneven distribution, (Pimentel 2006). Nearly 60% of present soil ero- and the prohibitive cost of transport beyond a

Liu et al., Global Phosphorus Flows from Cansumption 239 RESEARCH AND ANALYSIS limited radius, a large proportion of manure phos- recycling and is permanently lost from the land phorus is now subject to disposal instead of recy- (EEA 1997; USEPA 1999). cling. If construction of necessary infrastructures Proposals for recovery of phosphorus via de- for appropriate disposal of manure lags behind, centralized source-separated strategies have re- animal wastes become a major source of phospho- ceived increasing attention since the mid-1990s rus loads in surface waters. Uncontrolled phos- (Larsen and Gujer 1996; Beck 1997; Otterpohl phorus emission from intensive feedlots and farms et al. 1999; Berndtsson and Hyvonen 2002; in China has escalated in parallel with the grad- Wilsenach and van Loosdrecht 2003; IWA and ual growth in total animal-feeding operations and GTZ 2004).6 This decentralized and downsized the rapid shift in breeding structure (Liu et al. sanitation concept, focused on ecologically sus- 2004b). The emission of China’s livestock was tainable and economically feasible closed-loop estimated at 36% of its national phosphorus load systems rather than on expensive end-of-pipe to aquatic environments in 2000 (Liu et al. 2007). technologies, advances a new philosophy. It de- Thus, livestock husbandry is the most signifi- parts from the one-way flow of excreta from ter- cant source of phosphorus flux to surface wa- restrial to aquatic environments, as introduced ters in China, similar to the situation in Euro- by the conventional flush-and-discharge sewage pean countries in the early 1990s (Morse et al. system. The new alternative separates nutrients 1993). and domestic used water at the source and han- dles both components individually on the basis of material flows approaches. Thus, it avoids the dis- Sewage Treatment advantages of conventional wastewater solutions In the 1960s, many developed countries be- and enables and facilitates nutrient recycling. gan to alleviate the pollution in surface water Although the reinvention and transition of ur- by constructing municipal sewage infrastructures ban wastewater systems poses a major challenge, and implementing phosphorus discharge restric- it does provide a promising prospect for future tions on production sectors (Stauffer 1998; Moss phosphorus recovery and recycling in an ecolog- 2000). The giant infrastructure of centralized ical and economically efficient way (Larsen et al. wastewater treatment has drastically reshaped the 2001; Pahl-Wostl et al. 2003).7 phosphorus cycle within modern cities. Despite high economic costs, its environmental benefits Detergents Use in regard to removal of phosphorus from wastew- ater are far less than satisfactory worldwide. Some The use of sodium tripolyphosphate progress has been achieved in European countries (Na5P3O10; STPP), the most widely used (EEA 2003b; Farmer 2001) and the United States detergent additive, has been identified as a (Litke 1999), however. As the centralized con- significant contributor to eutrophication. STPP trol strategy just removes “pollutants” into sewage was first introduced in the United States in 1946 sludge rather than promoting a recovery and recy- (Emsley 2000). After reaching a peak in the cling of resources, including phosphorus, it does 1960s, global production has finally fallen to not really solve the long-term problem (Beck one half of the peak level, about 1.0 MMT P/yr, 1997; Stauffer 1998). The costly and rigid infras- mainly due to bans on phosphorus-containing tructures have significantly reduced agricultural detergents in developed countries. According reuse of urban human excreta and contributed to the estimate by Villalba and colleagues to a disconnection of nutrient cycles between (2008), the total quantity of STPP production urban areas and croplands (Foster 1999). Un- was 0.86 MMT P in 2004. In the late 1990s, fortunately, no available technologies for stable phosphorus-free detergents accounted for 45%, recovery and recycling of phosphorus are likely 97%, and 100% of all detergents, respectively, to be successfully commercialized in the near fu- in the United States, Japan, and European ture (Driver 1998; Piekema and Roeleveld 2001; countries (Litke 1999; Moss 2000). SCOPE 2001). Hence, most of the phosphorus There has been controversy on the environ- in urban human wastes is not subject to efficient mental impacts of STPP since the middle 1980s

240 Journal of Industrial Ecology RESEARCH AND ANALYSIS

(Lee and Jones 1986; Hoffman and Bishop 1994; sources. It is helpful to discriminate phospho- Morse et al. 1994; Wilson and Jones 1994; Wil- rus loads from different sources. Normally, point son and Jones 1995; Liu et al. 2004a). Today, it sources refer to the discharges from industry is acknowledged that limiting or banning house- and urban wastewater. Diffuse sources (nonpoint hold consumption of phosphorus-containing de- sources) include background losses, losses from tergents would not lead to a significant or a agriculture, losses from scattered dwellings, and perceivable improvement of eutrophication. It atmospheric deposition on water bodies. Appli- would have little impact on the environment cation of area-specific indicators enables a com- and human health compared to other substitute parison of phosphorus loads between different chemicals (sodium carbonates, sodium silicates geographic boundaries (EEA 2005). Figure 4 il- or zeolites A, and sodium nitrilotriacetate), from lustrates a cross-county comparison of the phos- both an environmental and an economic per- phorus loads in European countries and in China spective. In parallel with these discoveries, some to their domestic aquatic environments. Figure 5 Nordic countries eco-labeled STPP as an envi- shows a comparative histogram of the phospho- ronmentally friendly component of detergents in rus loads to some main lakes and river basins in 1997 and have repromoted the production and Europe and China. consumption of STPP since then. The results show that the phosphorus loads range from 0.2 kg P/ha in Sweden to 2.5 kg P/ha in Belgium at the national level. China lies be- Eutrophication tween Germany and Northern Ireland in terms Eutrophication is an unwanted explosion of of the load per unit land area. At the basin living aquatic-based organisms in lakes and es- level, the phosphorus loads of the three rivers tuaries that results in oxygen depletion, which and three lakes8 in China average 1.7 kg P/ha, can destroy an aquatic ecosystem. It has been 1.3 times the average of the selected European regarded as the most important environmental river basins and lakes. These results suggest that problem caused by phosphorus losses. Significant the Chinese economy is, in general, processing eutrophication took place in the 1950s in the phosphorus “wastes” less efficiently than devel- Great Lakes of North America and has been oped countries. It is nearly impossible, however, prevalent in many lakes and estuaries around the to determine a common benchmark (of a de- world (UNEP 1994; ILEC 2003). Phosphorus is sired phosphorus load) to prevent water bodies often the limiting factor responsible for eutroph- from eutrophication. This is because the complex ication, as nitrogen fluxes to water bodies are rel- interrelations between the amount of aquatic atively large. biomass and the phosphorus load are affected by Phosphorus losses from industries, croplands, a number of hydrological, meteorological, and animal farms, and households constitute the main biochemical factors that remain unclear under

Figure 4 Comparison of phosphorus loads to aquatic environments by country in 2000 (unit: kg P/ha). Sources: EEA 2005; Liu 2005.

Liu et al., Global Phosphorus Flows from Cansumption 241 RESEARCH AND ANALYSIS

Figure 5 Comparison of phosphorus loads to aquatic environments by river basin in 2000 (unit: kg P/ha). Date for Chinese river basins refers to 2001. Sources: EEA 2005; Liu 2005; Zhang and Chen 2003. current knowledge. Nevertheless, the compari- latory measures focus on the reduction of vari- son of area-specific phosphorus loads serves as a ous phosphorus losses to the water body, aiming valuable analysis tool for decision making. to mitigate extensive eutrophication. Neverthe- less, management of the phosphorus in soils and recovery and recycling of phosphorus in various Regulating the Societal wastes, which are vitally important to reconstruct Phosphorus Flows the societal phosphorus flows as a whole, are com- paratively disregarded. Phosphorous, intensively extracted from the The ecological restructuring of the cur- natural sink in the lithosphere and processed rent once-through mode of societal phospho- through various production–consumption cycles, rus metabolism is thus desired, leading to ultimately deposits in soil or reaches a water body a sound structural shift in the societal pro- by different pathways. The societal phosphorus duction and consumption of phosphorus. The flows are characterized by complicated physi- ecologically rational switch, differing from the cal interconnections in high intensities among current eutrophication-driven regulatory regime, a number of production and consumption sec- can contribute to sustained phosphorus uses and tors. Hence, it is vitally important to connect a substantial reduction of phosphorus emissions, the phosphorus flows with environmental regu- by minimizing phosphorus input and maximiz- lations intended to intervene in social practices ing phosphorus recycling. Given that ecologiz- and human behaviors. ing the phosphorus flows only succeeds when Instead of continuously trying to limit the measures are institutionalized into the economy growth of phosphorus use (e.g., the bans of deter- and society as a whole, this process will most gent phosphorus), there is a great need to recon- likely be a gradual one rather than a radical struct the physical structure of phosphorus flows, revolution. in particular by redirecting the crucial phospho- rus flows with highly negative environmental im- pacts. The most remarkable feature of the societal Notes phosphorus flows is that, on the one hand, the 1. One million metric tons (106 t) = 1 teragram current global reserves may sustain the current (Tg) = 109 kilograms (kg, SI) ≈ 1.102 × 106 short mining intensity for perhaps less than 1 century. tons. All tons mentioned in this article refer to On the other hand, massive losses of phospho- metric tons. rus from the economies take place annually, and 2. Some authors disagree. Schlesinger (1991), for in- only a few of them have been subject to recy- stance, assumed that this flux may be only slightly cling.9 Currently, most of the phosphorus regu- higher than in prehistoric time.

242 Journal of Industrial Ecology RESEARCH AND ANALYSIS

3. One square kilometer (km2,SI)= 100 hectares for a longer period. For instance, as discussed else- (ha) ≈ 0.386 square miles ≈ 247 acres. where in this article, the phosphorus that has been 4. One cubic meter (m3,SI)≈ 1.31 cubic yards (yd3). mobilized in soils over time, especially after indus- 5. We apply the term animal unit acknowledging that trialization of chemical fertilizer production and ap- animals are considerably different in manure pro- plication, forms a tremendous source for remining. duction. It serves as a common unit for aggregating Due to significant uncertainties in technological animals across farms and across animal types and trajectories as well as market mechanisms, how- thus provides a measurable basis for environmental ever, it is almost impossible to predict exact de- regulation. One calculates animal units by multi- pletion times of a certain resource. Our estimation plying the number of animals by an equivalency provides a baseline scenario for phosphorus deple- factor based on nitrogen or phosphorus emission. tion. The result warns us that if we do nothing on 6. Such systems (e.g., dual-flush toilets) separate nu- investments in advanced technologies for phospho- trients and domestic used water at the source and rus (re-)mining and recycling today, we will suffer handle all components individually on the basis very soon. of material flows approaches. The holistic alterna- tives, which avoid the disadvantages of conven- tional wastewater solutions, allow the segregation References of urine and feces in plumbing and thus ultimately enable and facilitate nutrient recycling. Moreover, Beck, M. B. 1997. Applying systems analysis in man- by decentralizing and downsizing the entire urban aging the water environment: Towards a new wastewater infrastructure, this approach does not agenda. Water Science and Technology 36(5): 1– favor specific technologies and meanwhile does not 17. cause hygiene or odor problems. Berndtsson, J. C. and I. Hyvonen. 2002. Are there 7. Detailed studies are essential as a first step, inter alia, sustainable alternatives to water-based sanitation of technological, organizational, economic, and so- system? Practical illustrations and policy issues. cial aspects. In addition, the involvement of multi- Water Policy 4(6): 515–530. stakeholders, such as residents, building owners, Brasnett, R. 2002. Feed phosphates: Their role in an- farmers, politicians, officials, and other interested imal feeding and prospects for demand growth. parties, from the start seems essential. All these Paper presented at 2003 Fertilizer Outlook Con- problems cannot be solved overnight, as the so- ference, 14–14 November, Arlington, VA. lution requires nothing less than a paradigmatic Brown, L. R. and E. C. Wolf. 1984. Soil erosion: Quiet change of a large sociotechnical system. crisis in the world economy. Worldwatch paper 60. 8. Three rivers refers the Huai River, Hai River, and Washington, DC: Worldwatch Institute. Liao River, and the three lakes include Taihu Lake, Burke, S., L. Heathwaite, and N. Preedy. 2004. Transfer Chaohu Lake, and Dianchi Lake. All of them are re- of phosphorus to surface waters; eutrophication. garded as national key areas for water environmen- In Phosphorus in environmental technology: Princi- tal protection. These six watersheds were upgraded ples and applications, edited by E. Valsami-Jones, as the national key environmental protection areas p. 120–146. London: IWA Publishing. at the Fourth National Environmental Protection CEEP (Centre European d’Etudes des Polyphosphates Conference in 1996. [the West European Phosphate Industry’s Joint 9. The estimation of the depletion times of phospho- Research Association]). 1997. Phosphate. Brus- rus reserves on the basis of the ratio of current re- sels: CEEP. serves to current usage rates is controversial. Re- Chen, F., ed. 2002. Agricultural ecology. Beijing, China: serves are defined as the resources economically China Agricultural University Press. In Chinese available to extract given current prices and tech- Chen, Z. L. and Y. Z. Tang. 1998. Study on develop- nology. It is argued that when reserves become ment and drawbacks of urban night-soil treatment scarce, the market prices tend to rise, and a va- and disposal system in China. Environment and riety of societal responses (e.g., substitution, more Hygiene Engineering 6(3): 125–131. In Chinese. efficient use, increased exploration, investment in Compton, J. S., D. J. Mallinson, C. R. Glenn, G. Filip- improvements in extraction technology) could oc- pelli, K. Follmi, G. Shields, and Y. Zanin. 2000. cur. Because there is definitely no substitute for Variations in the global phosphorus cycle. 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Journal of Environmental Management 47(3): 283– About the Authors 296. Wilsenach, J. and M. van Loosdrecht. 2003. Impact of Yi Liu is a lecturer in the Institute of separate urine collection on wastewater treatment Environmental System Analysis, Department systems. Water Science and Technology 48(1): 103– of Environmental Science and Engineering at 110. Wilson, B. and B. Jones. 1994. The phosphate report. Tsinghua University in Beijing, China. Gara London: Landbank Environmental Research & Villalba is a postdoctoral fellow in the Insti- Consulting. tut de Ciencia` I Tecnologia Ambientals at Uni- Wilson, B. and B. Jones. 1995. The Swedish phosphate re- versitat Autonoma` de Barcelona in Barcelona, port. London: Landbank Environmental Research Spain. Robert U. Ayres is Emeritus Professor of and Consulting. Economics and Political Science and Technol- Yang, D., S. Kanae, T. Oki, T. Koike, and K. Musiake. ogy Management at INSEAD in Fontainebleau, 2003. Global potential soil erosion with reference France, and Institute Scholar at the International to and climate changes. Hydrological Pro- Institute for Applied Systems Analysis in Lax- cesses 17(14): 2913–2928. enburg, Austria. Hans Schroder is a consultant Zhang, D. and J. Chen. 2003. Investigation and estimation in Vedbaek, Denmark specializing in graphical of non-point sources in China. Technical report. Beijing, China: SEPA. input-output analysis.

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