Changing Urban Phosphorus Metabolism: Evidence from Longyan City, China

Science of the Total Environment 536 (2015) 924–932

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Science of the Total Environment

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Changing urban phosphorus metabolism: Evidence from Longyan City, China

Shenghui Cui a,b,⁎,SuXua,b, Wei Huang a,b, Xuemei Bai c, Yunfeng Huang d,GuilinLia,b a Key Lab of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China b Xiamen Key Lab of Urban Metabolism, Xiamen 361021, China c Fenner School of Environment and Society, College of Medicine, Biology and Environment, Australian National University, Canberra 0200, Australia d School of Biotechnology Engineering, Jimei University, Xiamen 361021, China

HIGHLIGHTS GRAPHICAL ABSTRACT

• Both input P and output P increased sig- niﬁcantly from 1985 to 2010. • The agricultural subsystem contributed 85% of total P input. • The share of P input lost to the environment increased from 66% to 72%. • Food production efﬁciency decreased from 48% to 29%. • Per capita P input shows different curves with HDI, urbanization rate, and income.

Phosphorus flow of Longyan in 1985(a) and 2010(b) (Unit: t P). Arrows are sized relative to the magnitude of the flow; red arrows are P input flows; blue arrows are P output flows; orange arrows are P flows internal to the system; green arrows are P recycling flows internal to the system. The percentages are used to express the ratio of the input, output or stock categories to the total P input. article info abstract

Article history: Rapid worldwide urbanization calls for a better understanding of phosphorus (P) metabolism and the interaction Received 8 March 2015 of the physical, ecological and social drivers of P cycling in urban systems. We quantified the P metabolism in Received in revised form 16 May 2015 Longyan, a city with a major agricultural economy, and analyzed its long-term trends over the rapid urbanization Accepted 19 June 2015 period of 1985–2010. Both input P (from 4811 t P to 14,296 t P) and output P (from 4565 t P to 13,509 t P) Available online 2 July 2015 increased significantly. The agricultural subsystem contributed most to the P metabolism, accounting for 85% Editor: D. Barcelo of total P input. The share of P input lost to the environment, i.e. discharge to water, accumulation in the soil and landfill, increased from 66% to 72%, while food production efficiency decreased from 48% to 29%. Per capita Keywords: P input showed linear relationships with the Human Development Index (HDI), S-curve relationship with the Phosphorus urbanization rate, and logistic curve relationship with per capita disposable income. A more meat-based diet Substance flow analysis shift both in Longyan and surrounding cities greatly affected Longyan's food production structure. Our results Urban metabolism demonstrate that P metabolic quantity, configuration, and efficiency in production systems can change drastically Urbanization in response to changes in consumer and producer behavior as well as in socioeconomic structure. A larger China regional scale should be considered in urban P management, when trying to mitigate the increase in P use.

⁎ Corresponding author at: Institute of Urban Environment, Xiamen, China. E-mail address: [email protected] (S. Cui).

1. Introduction static P metabolism analysis; very few have presented any long term trends of the city phosphorus budget. Consequently, the underlying Phosphorus (P) is an essential nutritional element for all living drivers of such trends are poorly understood. In this study, we aim to beings (Smil, 2000) and a critical resource for agricultural production. address these challenges by taking Longyan City, China as a case Because most soils contain only low concentrations of this nutrient study. We established a phosphorus metabolism model in Longyan (Cordell et al., 2011; Matsubae et al., 2011), phosphate fertilizer, made City to identify and quantify the P flow, aim to answer the following from phosphate rock, is a key component of high-yield agriculture questions: (1) How has the P flow changed between 1985 and 2010, (Tilman et al., 2001, 2002). It is estimated that 20 million tonnes of and do these changes differ in various subsystems in the city? phosphorus is mined annually around the world (Bennett et al., 2001; (2) How important are changing P metabolism, especially shifts in Mackenzie et al., 2002). However, at the current rate of mining, world food production efficiency, in explaining changes in environmental P phosphorus reserves will be depleted in the next 50 to 100 years loss? (3) What are the key socioeconomic drivers of changing urban P (Gilbert, 2009). Furthermore, the quantity of P flowing into the oceans metabolism? The study adds a rather unique empirical evidence of has crossed to the planetary boundary and at high risk (Rockstrom city P metabolism, where urban system shows a high throughput in- et al., 2009; Steffen et al., 2015). In China, a major phosphorus producer cluding high ratio of P export in agricultural product. as well as a consumer of phosphate fertilizers (Chen et al., 2008; Cooper et al., 2011; Van Kauwenbergh, 2010), it is predicted that phosphate ore 2. Materials and methods can only be exploited for about 70 more years, and that no more than 20% of the phosphate ores in China have a sufficiently high content of 2.1. Description of study area phosphorus (N30% P2O5)(NBSC, National Bureau of Statistics of China, 2011). To counteract such environment problems and issues of scarcity The study area is within the administrative boundaries of Longyan of P, serious attention should be paid by all sections of the community. City (24°23′N – 26°02′N, 115°51′–117°45′E), which is located in Many studies have estimated how phosphorus use proceeds at the west of Fujian Province, China (Figure S1) and covers an area of different geographical scales. Metson et al. have found, through 1.9 × 104 km2, including the built up area of 45 km2. Between the global-scale research, that dietary choices have a large influence on years 1985 and 2010, the GDP of Longyan experienced a significant the demand for P, and that the global per capita P footprint increased growth, from approximately 1 billion Yuan (Yuan = Chinese Yuan 38% between 1961 and 2007 (Metson et al., 2012a). Urban systems [RMB], 1 Chinese Yuan ≈ 0.164 USD in 2014) to 99 billion Yuan and have been playing a major role in changing biogeochemical cycles at the urbanization rate increased from 27% to 45% (LSB, Longyan different scales (Cui et al., 2013; Grimm et al., 2008; Kaye et al., 2006), Statistics Burean and NBSC, National Bureau of Statistics of China, including the increased movement of P from mineral deposits to rivers 1986–2011), indicating that more than 50% of the population were and oceans, leading to eutrophication of aquatic ecosystems (Cordell still engaged in agricultural activities. But the agricultural industry et al., 2009; Wang et al., 2015). Such increases are principally due to only contributes 12% of the GDP of Longyan City in 2010. The local live- three changes in the systems: increases in population, which require stock industry contributed 40% of local total agricultural output value an overall increase in food production (Cordell et al., 2009); changes (Wu, 2009), and produced 26% of the pigs slaughtered in the entire in diet to more P intensive products (Schmid Neset et al., 2008); and province (Ruan et al., 2011). The discharge of pig excreta can greatly structural composition of P intensive industries (Liu et al., 2007). For ex- affect downstream areas, especially since Longyan is located at the ample, in cities where agriculture is the main economic component, river source area of the Minjiang, Jiulong and Ting rivers, which are changes in P use efficiency, including intensification of fertilizer inputs the three principal rivers of Fujian Province. The concentrations of nitro- to increase yields, and in P recovery efficiency (Cordell et al., 2013; gen and phosphorus in the river were blamed for the recent algal bloom Schroder et al., 2011; Godfray et al., 2010) alter overall P metabolic char- incidents in one of the rivers (Li et al., 2011). acteristics. Urban P metabolism analysis— an approach to identifying the P flow pathways and quantifying them at the city scale, has been 2.2. The P metabolism model and calculation processing conducted in many cities (Dokulil et al., 2000; Han et al., 2011; Li et al., 2010; Metson et al., 2012b; Nyenje et al., 2010; Qiao et al., 2011; In this study, considering the actual situation, data availability and Yuan et al., 2011b). P flows have changed dramatically during the past theoretical assumptions, we firstly present a model used in this study few decades, with more variation in key phosphorus flows, largely to map the P metabolism of the socioeconomic system of Longyan City because they represent specific characteristics of the urban system, in- (Fig. 1). And then, we divided the socio-economic system related to P cluding size, industry type, infrastructure and stage of development metabolism into four subsystems: the crop production subsystem, the (Cordell et al., 2012). Many of these studies show that the “upstream” livestock subsystem, the human consumption subsystem and the indus- urban P nutrient demand, the “downstream” urban P waste increase, trial subsystem. After that, we collected data to calculate every subsys- and the cycle of P within the city itself often show unidirectional flow. tem, compared temporal variation of P metabolism and discussed the The studies related to China or Chinese cities indicate that the P cycle reasons and strategies of P management. The crop production subsys- here shows highly intensive input but low use efficiency and low recov- tem includes the agricultural soil and crops. The livestock subsystem in- ery (Fan et al., 2009; Li et al., 2012; Liu and Chen, 2006; Ma et al., 2011). cludes livestock and poultry. The human consumption subsystem Promoting urbanization is one of the top policy agendas of the includes both the urban population in, and the rural population Chinese government, and according to its recently released national surrounding the city. The industrial subsystem refers to factories that strategy, the process will increasingly spread into inland and western produce and process P products, and industrial raw materials includes regions (Bai et al., 2014; Deng and Bai, 2014). In order to understand the raw materials (sodium tripolyphosphate, phosphoric acid, etc.) and effectively manage P flows, it is important to establish the behavior used to produce phosphorus-containing industrial products (such as of P flows over a long time period, especially in rapidly urbanizing coun- detergents). tries like China, where many cities will emerge and grow over the next In this study, phosphorus analysis was based on the P metabolism several decades. However, most of the studies have focused mainly on model and the SFA (substance flow analysis) method, a systematical 926 S. Cui et al. / Science of the Total Environment 536 (2015) 924–932

Fig. 1. Phosphorus metabolism model for Longyan City. Central dashed box is subsystem in the city. Arrows are flows into and out of the Longyan socioeconomic system or between subsystems; red arrows are P input flows; blue arrows are P output flows; orange arrows are P internal flows between subsystems; and green arrows are P recycling flows between subsystems. method for analyzing the metabolism of an objective substance (Yuan We also interviewed about 30 farmers who were engaged in livestock et al., 2011a,b). The boundary for the SFA was defined as the geographic and poultry cultivation to obtain parameters such as culture cycle and boundary of Longyan City. We also combined the SFA with the time 5 persons who worked in the local sewage treatment plant. series method to analyze the temporal dynamics of the P flows of the All P inputs to and outputs from the Longyan socioeconomic system socio-economic system. For the food production process, four indices were calculated based on the law of mass conservation. We estimated P were defined (Table 1 and see Supplementary materials for more infor- flows using the following equation: mation) to demonstrate the evolution of different subsystems' production efficiency. And, we finally used a curve fitting method to analyze Pflow ¼ massof material Pconcentrationof material: ð1Þ the relationship between P metabolism and key indicators. The calculation process was based on four assumptions: (1) local products were We estimated P accumulation from the system or subsystem using assumed to primarily meet the demand of local residents, and then the following equation: the excess was exported to other cities; (2) aquatic products were all X X ¼ ‐ : ð Þ imported from outside the city because Longyan is an inland city and Paccumulation Pinputs P outputs 2 the main consumed aquatic products are marine products; (3) because socio-economic P metabolism was dominated by the anthropogenic P In the crop production subsystem, 8 types of products (rice, wheat, cycle, some small natural flows were not considered (e.g., P input maize, beans, tubers, vegetable oil crops, vegetables and fruits) were in- through atmospheric deposition and the rivers); (4) P accumulation in cluded in the calculation of P flows. For the livestock subsystem, four the human body was ignored and P inputs and outputs of the human kinds of common livestock (pigs, cattle, sheep and poultry) were con- consumption subsystem reached equilibrium in one year. sidered. Data for the required amount of feed and the livestock-raising Data for this study were mainly collected from official statistical cycle were obtained from interviewing local farmers. In the industrial yearbooks, published literatures and local investigation (see Supple- subsystem, only detergents and fuel were considered and we did not mentary material for more details). Official statistical yearbooks includ- calculate industrial products output because of data constraints. In the ed the Longyan Statistics Yearbook 1986–2011 (LSB, Longyan Statistics human consumption subsystem, 14 types of commonly consumed Burean and NBSC, National Bureau of Statistics of China, 1986–2011) foods (cereals, vegetables, vegetable oil, pork, beef, poultry meat, eggs, and the Fujian Statistical Yearbook 1986–2011 (FSB, Fujian Statistics aquatic products, milk products, sugar, wine, fruits, potato tubers and Bureau and NBSC, National Bureau of Statistics of China, 1986–2011). soybeans) were chosen to calculate P food consumption per capita by both urban and rural populations. The formula is as follows:

Table 1 Xn fi fi ¼ γ ð Þ De nition of ef ciency in food production system. qp iqi 3 i¼1 Efficiency indices Definition

Crop production subsystem The ratio of crop P (plant-based foods P + green where qp is the P consumption per capita per annum; yi is the P concen- efficiency fodder P) to P input to crop production subsystem tration of food i, and its value refers to the average P concentration of Livestock subsystem The ratio of animal-based food P to P input to food i in China (Yang et al., 2009); q is the consumption amount of efficiency livestock subsystem i Food production system The ratio of P in desired outputs (crops for the food, food i;andn is the number of types of food. Since the data sources efficiency meat and poultry, and green fodder P,and so on) to and computing methods were the same for all the years between total P inputs to food production system 1985 and 2010, we show only the data and detailed description of the P recycling efficiency The ratio of P recycling from livestock and human calculation process for the year 2010 as an example (see supplementary consumption subsystem to fertilization P Tables S1 and S2 for more details). S. Cui et al. / Science of the Total Environment 536 (2015) 924–932 927

3. Results Compared to the year 1985, the total P input had a huge growth, associated with a greater proportion of P (from 65% to 73%) loss to the 3.1. Structure and trends of P metabolism environment in 2010. This indicated the P use efficiency of the system had decreased. The categories of P inputs and outputs from 1985 to As shown in Fig. 2(a), in 1985 the total P inputs to the Longyan City 2010 are presented in Fig. 3. Fertilizer P and feed P had growth multi- amounted to 4811 t P (t = ton(s), 1 t = 1000 kg), of which the agricul- pliers of 1.5 and 8.8, respectively. Although fuel P input took up the tural subsystem (including crop and livestock production) accounted least proportion of total P inputs in 1985 (fuel 2.2%, phosphates for 81% (75% + 6%), and the industrial subsystem only 15%. Another 12.8%), it had the fastest growth rate, with a compounded annual 4% (217 t P) of the total P inputs were imported food consumed by growth rate of 12% (from 108 t P to 1863 t P). There were upward trends local inhabitants. About 65% (28% + 20% + 17%, 3163 t P) of P input in phosphorus of the categories of soil accumulation, landfill, water and was lost to the environment, 29% (1402 t P) was exported as food and exported animal-based food P, increasing from 1378, 830, 955 and 5 t P 6% (4% + 2%, 246 t P) remained in the system, in 1985. to 3940, 3434, 2960 and 410 t P, respectively, while exported plant- The total P input skyrocketed to 14,296 t in 2010 (Fig. 2(b)). The based food P presented a downward trend from the year 1999 onward percentage of the total P input of the agricultural subsystem, industrial (Fig. 3(b)). Between 1985 and 1999, exported plant-based food P grew subsystems, and the imported food, constituted 82%, 15% and 3%, re- from 1397 t P to 3790 t P, then decreased to 2765 t P by the year 2010. spectively. This similar percentage distribution of inputs between 1985 and 2010 indicates that the inputs structure is relatively stable 3.2. P metabolism of different subsystems with the increase of total quantity of P input. 73% (28% + 21% + 24%, 10,334 t P) of P input was lost to the environment in 2010. Food exports From the year 1985 to 2010, the P flow in the identified subsystems and P accumulation in the system accounted for 23% (3175 t P) and 6% in 2010 changed dramatically (Table 2). For the crop production subsys- (1% + 5%, 787 t P), respectively. tem, in 1985 the total P input was 4579 t P, including 78% (3591 t

Fig. 2. Phosphorus flow of Longyan in 1985(a) and 2010(b) (Unit: t P). Arrows are sized relative to the magnitude of the flow; red arrows are P input flows; blue arrows are P output flows; orange arrows are P flows internal to the system; and green arrows are P recycling flows internal to the system. The percentages are used to express the ratio of the input, output or stock categories to the total P input. 928 S. Cui et al. / Science of the Total Environment 536 (2015) 924–932

bodies) in the livestock subsystem (from 56 t P to 699 t P) was mainly due to the growth in the livestock population. The food production subsystem (including both crop production and livestock subsystems) played a principal role in phosphorus metabolism of Longyan City. Our study suggested that during 1985 to 2010, about 84%–91% of P inputs were used to meet the food demand (local food consumption and food exports) in Longyan City. Total P input to the food production system was 3893 t P in 1985 and 11,751 t P in 2010, with 1957 t P (51%) of the input and 7233 t P (62%) of the input, respectively, lost to the environment, through soil accumulation, straw loss, livestock excreta and loss in food processing (Fig. 3 and Table 2). And 988 t P, 4047 t P was recycled as biological fertilizer, while 1402 t P (in 1985) and 3174 t P (in 2010) were output as food products. Between 1985 and 2010, the pattern of P production efficiency in Longyan changed. We chose four indices to evaluate P production efficiency in the food production cascade, including crop production, livestock production, food production and P recycling efficiency (Table 1 and Figure S2). The four indices showed different variations. Crop production efficiency fluctuated between 55% and 65%. Livestock production efficiency remained at about the 11% level. However, food production efficiency decreased from 55% to 34%, meaning that we could gain 1 t food P by inputting 1.8 t P to the food production system in 1985, but needed to input 2.9 t P to obtain 1 t food P in 2010. The main reason for the difference was that in order to meet the development of the livestock industry, a great amount of green fodder was used for raising local livestock and poultry instead of exporting outside the city. The crop recycling efficiency showed a gentle upward trend (about 1.6% annual growth rate) from 1985 to 2010, due primarily to an increase in the application of manure. For the human consumption subsystem, total P input increased from1,123 t P to 1306 t P. Consumption of meat and poultry rose significantly, from 92 t P to 315 t P, while the amounts for consumed plant- based foods decreased from 805 t P to 626 t P, indicating a shift in die- Fig. 3. Categories and trends of phosphorus inputs (a) and outputs (b) of Longyan from tary choice. It is worth noting that between 1985 and 2010 the amount 1985 to 2010. of recycled P from the human consumption subsystem to the crop production subsystem decreased from 609 t P (only excreta) to 386 t P P) from fertilizer, seed and pesticides, 13% (609 t P) from human excreta (sludge 230 t + excreta 156 t), while the P content in garbage increased recovery, and 9% (379 t P) from livestock manure reuse. However, in from 431 t to 623 t. The input of the industrial subsystem also rose, from 2010 the total P input peaked to 12,837 t P, mainly due to the increased 701 t P to 2194 t P. The industrial subsystem generated more P discharge amount of fertilizer application (67%, 8599 t P) and livestock manure in the form of waste and sludge in 2010 than in 1985. reuse (28%, 3661 t P). Over the same period, the total P output increased from 4389 t P to 12,749 t P, with the P accumulation (standing crops) 3.3. P loss to the water environment decreasing from 199 t P to 88 t P. P output through plant-based food exports, soil accumulation, straw and food processing loss grew twofold, During 1985 to 2010, the total water P load increased from 955 t to threefold and ninefold, respectively. 2960 t, a rise of 210% (Fig. 4). But between 2005 and 2007, there was For the livestock subsystem, the total P input increased to 7538 t P a obvious decline, due mainly to the decrease of marketable fattened in 2010, about ninefold that in 1985 (795 t P) owing to the heavy P stock of poultry because of the influence of avian influenza. P release application to feed and more fodder from the crop production subsys- from the livestock subsystem grew from 243 t P to 2373 t P during the tem. At the P output end, with the total output increasing from 739 t P period. Meanwhile, the contribution of livestock excreta in the total to 6839 t P, meat and poultry exports and livestock manure reuse water P also peaked to about 80%, especially from live pig excreta. In both experienced large increases, to 410 t P and 3661 t P, respectively. 2010, P emitted by live pigs accounted for 71% of the total P discharge The increase of P accumulation (P retention in livestock and poultry from the livestock subsystem to water.

Table 2 P ﬂows in each subsystem in 1985 and 2010 (Unit: t P per year).

Subsystem Input (external input) Accumulation Exported Output to downstream subsystems (human) Discharge to environment (landﬁll) Recycled

P ﬂows in 1985 Crop production 4579 (3591) 190 1397 1298 (805) 1694 (66) – Livestock 795 (302) 56 5 92 (92) 263 (20) 379 Human consumption 1123 (217) 0 –– 514 (431) 609 Industry 701 (701) 0 – 9 (9) 692 (313) –

P ﬂows in 2010 Crop production 12,837 (8790) 88 2765 5204 (626) 4780 (594) – Livestock 7538 (2960) 699 410 315 (315) 2453 (80) 3661 Human consumption 1306 (352) 0 –– 920 (623) 386 Industry 2194 (2194) 0 – 13 (13) 2181 (2137) – S. Cui et al. / Science of the Total Environment 536 (2015) 924–932 929

The other sources of water P were from industry, soil erosion and capita P input (Fig. 5(c)), likely because increases in HDI are associated human consumption. These three items accounted for 75% of the total with a more meat-intensive diet. This result is similar to the relationship P load to the water environment in 1985, while the proportion de- between HDI and P footprint at the global scale (Metson et al., 2012a). creased to only 20% in 2010. P discharge by industry saw the biggest drop, from 379 t P (40%) to 44 t P (1.5%). However, the amount of P dis- 4.2. Drivers for P metabolism changes in Longyan City charge by human consumption increased greatly, from 83 t P to 300 t P, although the proportion in total P load looked stable compared to that of During the rapid urbanization of 1985 to 2010, the metabolic quan- livestock. P discharge through soil erosion was quite stable and its pro- tity, configuration, destinations and efficiency of P have changed drasti- portion was decreasing, which was probably because we only calculated cally in the production systems of Longyan City. Our results confirm that the soil erosion through agricultural land and did not consider other these changes of P metabolism were in response to the changes in the land use patterns. complex dynamics of urban socio-economic system (Bai et al., 2010; Bai and Schandl, 2011): (1) the large population growth brought 4. Discussion about by urbanization; (2) the dietary choice shift from a plant-based diet to a more meat-based diet; (3) the industrial structure changes, 4.1. Relationship between P input to the city and urbanization e.g., the increase in food exports, especially meat and poultry, and the development of manufacturing industries; (4) producer behavior To further understand the relationship between urbanization and P e.g., greater fertilizer use in agriculture and the discharge of industrial input, we chose per capita disposable income, urbanization rate and sewage. the Human Development Index (HDI) to fit with per capita P input; As mentioned above, the population of the city increased from 2.3 the results are presented in Fig. 5. million to 2.9 million during these 25 years. The greater population, In Fig. 5(a), per capita P input responds in a logistic curve, as per the greater the demand for food. In addition to Longyan, the population capita disposable income of residents rises. It indicated that when per of surrounding cities (such as Fuzhou, Xiamen and so on) also rose dra- capita income exceeds 9000 Yuan, per capita P input approached or matically. These cities imported a large amount of food from Longyan, reached saturation. This was different from the result that the total in- creating a food export challenge for Longyan; population growth in flow of dietary P into the socio-economic systems increases with per the local surrounding cities was an important driving factor for P metab- capita disposable income at the national scale when doing cross-city olism in Longyan. comparisons (Li et al., 2012). One reason for this difference might be Many studies have shown that dietary choices, especially those that Longyan was a food-production-dominated city and P input to related to meat and poultry consumption, have a large influence on the industrial subsystem was much less than to the agricultural subsys- the demand for P (Cordell et al., 2009). Our results showed that the tem. The other reason was more uncertainty about the influencing ratio between local plant-based foods P consumption and local meat factors at the national scale, such as the international food trade. In and poultry P consumption changed from 8.8:1 to 2:1 (Fig. 2), shifting Fig. 5(b), the relationship between per capita P input and urbanization from a more plant-based diet to a more meat-based diet. In the food rate fits the S-curve, indicating that urbanization is an important driver production system, the ratio between plant-based food P production for the growth of P input when the urbanization rates are between 0.3 and meat and poultry P production also changed, from 25.6:1 to 4.8:1, and 0.4. There was also a positive correlation between HDI and per indicating that the dietary choices of surrounding cities also greatly affected Longyan's food production structure. These results indicate that sustainable P management should consider the larger regional scale, when trying to mitigate the increase in P use. The urbanization process caused not only population growth and dietary changes, but also changes in the industrial structure. The P input increased significantly, in order to satisfy two objectives: food demand and fuel consumption. On the food side, we found that local food P consumption increased by only 16%, while P food exports, especially meat and poultry products, grew by 126% (an eightfold increase). These increases in food production profoundly changed the P metabolism in Longyan. On the fuel consumption side, the energy embedded P became the main proportion of P input for manufacturing. From the calculation results of energy P, with the rapid development of the manufacturing industry and urbanization, the input of fuel P bears witness to the fastest growth rate. Compared to other studies, such as Hefei (Li et al., 2010), Chaohu (Yuan et al., 2011b) and Lujiang (Yuan et al., 2011a), the P metabolism of Longyan showed distinctive characteristics. The largest P flows for these other three cities were raw materials imported to the product manufacturing sector (3700 t P, 4748 t P, and 5699 t P, accounting for 47%, 56% and 69%, respectively). The urbanization rate of Hefei was higher than Longyan (nearly 60%). A higher urbanization rate meant fewer citizens who engaged in agricultural activity. Therefore, compared to Longyan, food production took less proportion in Hefei. The urbanization rate of Chaohu and Lujiang was similar to that of Longyan, but there were more enterprises related to phosphorus in Chaohu and Lujiang. That was the reason why crop production system and livestock production system constituted a higher proportion in Longyan. On the other hand, Longyan was very similar to some counties with lower urbanization rate, such as Feixi (Wu et al., 2012)andWuwei(Bi Fig. 4. Sources of phosphorus load in the water environment. et al., 2013). In Feixi and Wuwei counties, P input to the agricultural 930 S. Cui et al. / Science of the Total Environment 536 (2015) 924–932

Fig. 5. Relationship between per capita P input and income (a), urbanization rate (b), HDI (c). production subsystems accounted for 88% and 98% of the total, Anthropogenic distortion of P flows caused excessive nutrient in respectively. All of them had high P input to the crop production subsys- water, resulting in anoxic events and turbid water (Rockstrom et al., tem (fertilizer) and the livestock subsystem (feed). These cases indicate 2009). In Longyan, P discharge from livestock had become the primary that city P metabolism was strongly influenced by local industrial source of water pollution. The Longyan municipal government had structure. also become aware of the serious water pollution caused by the pig There is a long tradition of using organic fertilizer from both live- breeding industry. Many pig farms were compulsorily shut down stock and humans in China (Gao et al., 2003). During the research in order to solve the problem (LMPG Longyan Municipal Peoples period, livestock manure recycling experienced a huge increase owing Government, 2013). But because many farmers raised pigs for a living, to the increase in the number of livestock, while the decrease in eliminating the pig farms meant a significant decrease in per capita in- human excreta recycling was mainly due to the decrease of the rural come and an increase in unemployment. Furthermore, the rapid urban- population and the consequent reduction in the proportion of human ization, with its consequent increase in a livestock-based diet and excreta recycling. Sludge recycling appeared after the year 2000, when improved nutritional intake, increased the demand for pork. Hence, the first waste water treatment plants were constructed. However, the the promotion of livestock waste product recycling and reuse is a big development of the chemical fertilizer industry caused large increases challenge in Longyan City. in fertilizer use, because the fertilizer had a high content of active com- The characters of P metabolism in Longyan call for new socio- ponents, was convenient transport and highly effective, compared to economic strategies and integrated nutrient management (Wu and organic fertilizer (Rautaray et al., 2003). Additionally, most farmers Ma, 2015). Firstly, in the production sector, integrated P management over-fertilized, erroneously believing that more fertilizer would result was important for agricultural subsystem. For example, increasing the in a better harvest; they also applied the fertilizers as early in the season reuse amount of animal wastes, human excreta and sludge could signif- as possible because of the short product guarantee periods (Yuan et al., icantly decrease the application of chemical fertilizer. Secondly, agricul- 2011a,b). The excess fertilizer application caused higher P accumulation ture production structure should be adjusted. The government had the in the agricultural soils. During the research period, soil accumulation P responsibility to guide livestock cultivators to shift to other job, such increased nearly threefold, causing a possible long-term threat to the as beekeeping (According to our investigation, a small number of freshwater ecosystem. cultivators had successfully shifted to the bee keepers). Thirdly, in the The decrease in the P discharge by industry was due mainly to the consumer sector, public need to choose a less animal based diet and re- implementation of relevant laws and regulations and the construc- duce their food wastes. In addition, Long-term goals for P management tion of sewage treatment plants. The significant changes in P config- should be clarified with consensus among concerned agencies, planners uration reflected industrial structural changes as well as industrial from all cities (Longyan, Zhangzou and Xiamen) along with the water environmental regulations. Through the waste disposal system, shed and relevant stakeholders. most P in wastewater was transferred to sludge for landfills. Com- pared with industrial wastewater disposal, the livestock sector was 4.3. Limitation relatively under-regulated. And there was lack of management mechanisms to collect and treat livestock manure, as well as of rele- At the city scale, uncertainty of quantification is inevitable for SFA vant laws. (Daniels and Moore, 2001). Because our budgets were made using S. Cui et al. / Science of the Total Environment 536 (2015) 924–932 931 many parameters from multiple data sources and much of the statistical countries. This study has indicated that city P metabolism research data is determined through analogy to other cities or the nation, our re- requires a system-wide, cross-setor and cross-boundary approach, sults contained a substantial degree of uncertainty. For example, when which is also critical for sustainable P management. calculating the amount of P consumed by humans through food, we used the data for the average quantity of P consumed by all Chinese in- Acknowledgments stead of the data for the average quantity of P consumed by residents in Longyan. In addition, some data from local investigation (including This study was supported by Ministry of Science & Technology of fi questionnaire and eld observations) had comparatively higher uncer- China (2011DFB91710), the Science and Technology Projects of Xiamen, fl tainty. And in this study, we only considered main P ows in the city, China (3502Z20130037) and the Key Laboratory of Urban Environment fl fi ignoring some ows that were dif cult to quantify such as the calcula- and Health, Institute of Urban Environment, Chinese Academy of tion of various industrial products and P loss at plant-based food pro- Sciences (KLUEH201108). cessing stage. Although the above uncertainty existed, the data in this article were Appendix A. Supplementary data used with relatively high credibility. Most data had been proved to be authorized and professional related and the uncertain P flows only Supplementary data to this article can be found online at http://dx. accounted for a small portion of the whole system. doi.org/10.1016/j.scitotenv.2015.06.073. Harmful algal blooms (HAB) and eutrophication have become the primary environmental concerns in Jiulong River watershed where Longyan city locates in the upstream. Continued N and P enrichment References and the decline of N: P ratio has been observed in this river, which Bai, X., McAllister, R.RJ., Beaty, R.M., Taylor, B., 2010. Urban policy and governance in a have increased the risk of nutrient-enhanced algal bloom (Chen global environment: complex systems, scale mismatches and public participation. et al., 2013). According to the findings and current understandings Curr. Opin. Environ. Sustain. 2, 129–135. Bai, X., Schandl, H., 2011. 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