How China's nitrogen footprint of food has changed from 1961 to 2010

The calculation of the N footprint of food production and consumption in China (hereafter 'N footprint') is based on a modified version of the N-Calculator (Leach et al 2012). The N-Calculator approach is modified in three ways with respect to the food component. First, we did not consider the energy consumption of food production and consumption in the N footprint calculation because it contributes in general a very small proportion to the total N footprint (Leach et al 2012). Second, we used a separate model (NUFER) to calculate virtual N factors, which are explained in more detail below. Third, we did not consider fossil fuel combustion associated with heating, electricity, transportation and production of goods and services.

'Food' is a generalized definition in this study, which does not distinguish different existing forms of food products before and after food processing. For example, wheat grain after harvest is the primary food commodity, bread, cake and noodles are different food products after processing. We use 'wheat' to represent all these food products originated from wheat as a whole. The N footprint of food is the sum of the N losses related to food production and consumption. The food consumption N footprint is the quantity of food N actually consumed by human beings based on the assumption that adults excrete the equivalent N contained in the food they eat (i.e. no net N retention). The food production N footprint represents all the N losses along the chain of food production to food consumption (Leach et al 2012). Here we chose 13 different food items, including seven plant-derived (wheat, maize, rice, soybeans, vegetables, fruits and roots), and six animal-derived (pig meat, beef, chicken meat, eggs, milk and fish & seafood) food items. The total per capita food N footprint in China is the sum of the per capita food consumption N footprint and food production N footprint of the 13 selected food types.

We used food protein supply data from the Food and Agricultural Organization of the United Nations Statistical Database (FAOSTAT) for the period 1961 to 2010 to calculate the food consumption N footprint in China (FAOstat 2016). Data and information about food losses and wastes that occurs at the retailer, food services and consumer were derived from literature (supplementary table S4, available at stacks.iop.org/ERL/12/104006/mmedia). Food production data were derived from the NUFER model and data on N fertilizer application for different crops were derived from literature and statistical data (tables S2 to S5).

The following equation shows the calculation method of the total per capita N footprint of food (NF_food):

$$\begin{equation} \begin{array}{*{20}c} {{\rm NF}_{{\rm food}} } \, &=& \, {\sum\limits_{i = 1}^n {{\rm NF}_{{\rm food}\;i} } } \\ {} &=& {\sum\limits_{i = 1}^n {({\rm NF}_{{\rm consumption }i} + {\rm NF}_{{\rm production }i} )} } \\ \end{array} \end{equation} \tag{ 1 }$$

where NF_consumption represents the food consumption N footprint; NF_production represents the food production N footprint; and i represents the different types of food (n = 13). The results will be shown as the average value per decade, for example, NF_food in the 1960s is the average value from 1961 to 1970.

The average per capita food consumption N footprint (NF_consumption) of a certain food type in a certain year followed the definition by Leach et al (2012), as follows:

$$\begin{equation} {\rm NF}_{{\rm consumption }i} = {\rm S}_{{\rm protein }i} \times {\rm NC}_{{\rm protein }i} - W_{{\rm food}\;i} \end{equation} \tag{ 2 }$$

where S_protein is the per capita protein supply of a certain food item, as derived from FAOSTAT (FAOstat 2016); NC_protein is the N content of protein (16%); and W_food is the per capita food waste related to consumption (at the retailer, food service, and consumer levels). We assumed that the average adults do not accumulate nitrogen, meaning that all N consumed enters the sewage stream. Sewage treatment with N removal technology was not considered in this study because of the low application rate and efficiency in China (Gong 2000). Therefore, all N consumed is considered to be released to the environment as human waste. It should be noted that this assumption is likely an overestimate because of recycling pathways (e.g. human waste used as fertilizer) and denitrification that occurs without sewage treatment.

Virtual nitrogen is defined here as N that was used in the food production process and is not contained in the food product that is consumed. It includes fertilizer volatilization and runoff, losses during food harvest and processing, animal manure losses, and food waste (Galloway et al 2014, Leach et al 2012). The N released to the environment in the process of food production to consumption per unit of N consumed is described by virtual nitrogen factors (VNFs). The average per capita food production N footprint (NF_production) of a certain food type in a certain year is calculated as

$$\begin{equation} {\rm NF}_{{\rm consumption }i} = {\rm NF}_{{\rm consumption }i} \times {\rm VNF}_{{\rm food}\;i} \end{equation} \tag{ 3 }$$

where VNF_food is the virtual N factor of a certain food item, representing the amount of Nr lost to the environment per unit N consumed (Leach et al 2012).

Similar to the description by Leach et al (2012), we assume that N flows between production and consumption of plant-derived food to have the following five steps: 1) input of new N, 2) crop production, 3) crop harvesting, 4) plant-derived food processing, and 5) food consumption. Nitrogen flows between production and consumption of animal-derived food can be captured in the following seven steps: 1) input of new N, 2) feed production, 3) feed processing, 4) animal production, 5) animal slaughtering, 6) animal-derived food processing, and 7) food consumption. Figure S1 conceptualizes the different stages of plant-derived and animal-derived food production and consumption.

During crop and animal production, N may be lost to the environment in four ways: ammonia (NH₃) emission, nitrous oxide (N₂O) emission, dinitrogen (N₂) emission and N losses to water (including N losses through surface runoff, leaching and erosion). Unlike other nitrogen species, N₂ emission does not cause environmental problems. Here we use emission factors derived from the NUFER model (Ma et al 2012) to calculate N losses in different forms that occur during food production. Calculation methods are presented in the supplementary information; detailed information on emission factors is presented in table S5.

To calculate VNFs, Leach et al (2012) use two indicators at each step of the food production process: N that continues to the next step (N uptake or % of previous) and N that is recycled (N recycled or % recycled). In this study, we rename these two indicators as NUE and nitrogen recycling efficiency (NRE), respectively, and use the same calculation methods to calculate VNFs of 13 major food items for China. However, as noted earlier, nutrient flows of food production and consumption in China are largely different from the US, thus it is very important to calculate local NUE and NRE for China. We use the NUFER model to provide the detailed information for the data points to calculate the NUE and NRE of 13 kinds of food items, which is described in the supplementary information. Results for the NUE and NRE at different stages used in the calculations of VNFs are presented in tables S6–S15. The NUFER model also enabled the N footprint to be reported by N species, which is a new addition to the N footprint approach (table S1).

According to the methods used by Shibata et al (2014), the virtual N factors considering food trade (VNF_T) are estimated as follows:

$$\begin{equation} \begin{array}{*{20}c} {{\rm VNF}_{\rm T} } \, &=& {{\rm SSR*VNF}_{{\rm NT}} } \\ {} &&+ \, {(1 - {\rm SSR})*{\rm VNF}_{{\rm import}} } \\ \end{array} \end{equation} \tag{ 4 }$$

where VNF_NT is the VNF without considering food trade; VNF_import was based on the VNF of the food items from the US, one of China's main agricultural trading partners; and SSR is the self-sufficiency rate of a specific food item, which describes how much food produced in-country contributes to total food supply (table S2).

There are large differences among food items when examining VNF changes between 1961 and 2010 (table 1). VNFs of vegetables, fruits and roots (potatoes and sweet potatoes) increased continuously over the past five decades. Roots had the highest increase (198-fold), followed by vegetables (70-fold). The high rate of increase is due in part to the very low VNFs in the 1960s. VNFs of wheat, maize and rice increased from the 1960s to the 1990s, and then tended to decrease. In contrast, VNFs of soybeans decreased from 4.6 in the 1960s to 1.3 in the 2000s. Most meat items showed increasing VNFs from 1961–2010. VNFs of pig meat, beef and chicken increased throughout the whole period, while VNFs of eggs and milk decreased around the 1970s and the 1980s, but increased thereafter (table 1).

The per capita food N footprint increased from 4.7 kg N capita⁻¹ yr⁻¹ in the 1960s to 21.3 kg N capita⁻¹ yr⁻¹ in the 2000s (figure 1). For plant-derived food, the per capita N footprint increased over the last five decades for all crops except for maize and soybeans. Due to the dramatic decreases in per capita protein supply quantity of maize (29-fold) (table S2) and the VNF of soybeans (3.5-fold) (table 1), the per capita N footprint of maize and soybeans decreased from 0.9 to 0.03 kg N capita⁻¹ yr⁻¹ and from 1.1 to 0.4 kg N capita⁻¹ yr⁻¹, respectively. The most dramatic increase occurred with roots, vegetables and fruits: the per capita food N footprint increased by 12, 33 and 82-fold, respectively. For animal-derived food, the per capita food N footprint increased continuously and significantly during the past five decades. Pig meat contributed 21% to the per capita N footprint in China in the 2000s, a seven-fold increase compared to the 1960s. The per capita N footprint of beef and chicken increased from 0.01 to 0.5 kg N capita⁻¹ yr⁻¹ (38-fold) and from 0.1 to 1.2 kg N capita⁻¹ yr⁻¹ (15-fold), respectively (figure 1).

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The national food N footprint in China increased eight-fold during the past five decades, from 3.4 to 28.2 metric tons (MT) N yr⁻¹ (figure 2). The increasing rate of the national food N footprint in China started to accelerate after the 1970s, and had the highest increase in the 1990s. The N footprint of plant-derived food increased from 2.2 MT N yr⁻¹ in the 1960s to 13 MT N yr⁻¹ in the 2000s. The N footprint of animal-derived food increased from 1.3 MT N yr⁻¹ in the 1960s to 15.1 MT N yr⁻¹ in the 2000s, and overtook the N footprint of plant-derived food in the 1990s. In the 2000s, animal-derived food contributed 54% to the national food N footprint.

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The national N losses from food production increased from 3.0 MT N yr⁻¹ to 27.2 MT N yr⁻¹ over the past five decades. Emissions of NH₃ and N₂ are the main loss items, NH₃ emissions increased from 1.3 MT N yr⁻¹ in the 1960s to 9.6 MT N yr⁻¹ in the 2000s. However, the contribution of NH₃ emissions decreased from 42% to 35%. Due to increasing fertilizer application and biological nitrogen fixation (BNF) during the past five decades, N₂O emissions and N₂ emissions increased from 0.04 MT N yr⁻¹ to 0.3 MT N yr⁻¹ and from 1.2 MT N yr⁻¹ to 10.3 MT N yr⁻¹, respectively. The contributions of N₂O and N₂ emissions were relatively stable in the past five decades, accounting for nearly 1.5% and 38% of the total losses respectively. N losses to water increased from 0.5 MT N yr⁻¹ in the 1960s to 6.9 MT N yr⁻¹ in the 2000s. The contribution of N losses to water increased from 17% to 25% (figure 3).

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The increases in the per capita N footprint (by 4.5-fold) (figure 1) and population (by 1.8-fold) (NBSC 2015) between 1961 and 2010 have both contributed to the increase in the national food N footprint (by 8.3-fold) (figure 2). The per capita food consumption N footprint increased from 1.8 to 3.3 kg N capita⁻¹ yr⁻¹ (1.8-fold); however, its contribution to the total food N footprint decreased from 38% in the 1960s to 16% in the 2000s. The per capita food production N footprint increased from 2.9 to 18.0 kg N capita⁻¹ yr⁻¹ (six-fold); its contribution to the total food N footprint increased from 62% in the 1960s to 84% in the 2000s (figure S2). The contributions of the food production N footprint to the N footprint of plant-derived food increased from 48% in the 1960s to 82% in the 2000s. The food production N footprint contributed a relatively stable share of nearly 85% to the N footprint of animal-derived food in the past five decades (figure 2).

The main reason for the increase in the per capita food consumption N footprint was the increase in consumption of animal-derived food (figure S3). The food consumption N footprint of animal-derived food did not change much during the 1960s and 1970s, mainly because of the poor economic conditions in China at that time (Naughton 2007). At the beginning of the 1980s, along with the 'reform and opening-up' national policy, the average income increased quickly, the urban population increased from 18% in 1978 to more than 40% in the 2000s (NBSC 2015), and crop and animal production started to rise quickly (Zhang et al 2012, Ju et al 2009). These favorable conditions promoted the consumption of animal-derived food and increased the food consumption N footprint (figure S3).

The larger increase in the food production N footprint compared to the food consumption N footprint (six-fold versus two-fold) (figures S3 and S4) is because the VNFs increased substantially over the past five decades. Increased fertilizer N inputs in crop production, increased animal production and a low recycling rate of animal manure N were the main drivers of the increasing VNFs (Zhang et al 2012, Ma et al 2012, Zhang et al 2008, Bai et al 2016).

Not all food items had increasing VNFs. For example, the VNF of wheat increased from the 1960s to the 1990s, but then stabilized as the slight increase in fertilizer N input was compensated by an increase in harvested yield. Similar trends were observed for maize (table 1). Interestingly, the VNF of soybeans decreased over time for a number of reasons. First, due to the rapid development of breeding programs since the founding of new China, many new cultivars with better productivity and quality have been released, which has stimulated the dramatic increase of soybean yield over the past five decades (Xue 2013, Liu et al 2008). Second, the increase of fertilizer N inputs was small relative to the increase of the soybean yield. Third, soybean imports have increased over the past two decades, and the VNF of soybeans is lower in exporting countries (including the US) than in China. The decrease of the eggs VNF in the 1980s and 1990s and the decrease of the milk VNF in the 1980s were also due to relatively large increases in yield and productivity (table S2).

Some food items with an increasing N footprint do not contribute a large proportion to the overall N footprint. For example, the per capita N footprint of fruits accounts for less than 4% of the per capita N footprint in China in the 2000s, but it increased 82-fold from the 1960s and the 2000s (figure 1). Pig meat contributed 21% to the per capita N footprint in China in the 2000s, but its increase (seven-fold) was relatively modest (figure 1).

The national N losses associated with plant-derived and animal-derived food production increased from 2.4 to 19.6 MT N yr⁻¹ and from 0.6 to 7.5 MT N yr⁻¹, respectively. The contribution of N losses associated with animal-derived food production increased from 21% in the 1960s to 28% in the 2000s. Increased fertilizer use and consumption of animal-derived food have become main drivers of the growing environmental costs of food systems (Tilman and Clark 2014, Xue and Landis 2010). N losses during feed crop production are merged into the total N losses of animal-derived food production. However, the total N losses were still dominated by plant-derived food production, which contributed 72% in the 2000s (table S16). This proportion is similar to the estimate provided in the study of Ma et al (2010).

The results of this study show that NH₃ emission and N losses to water are the main N loss pathways of animal production in China (table S16), similar to the results of Ma et al (2010) and Bai et al (2016). Ma et al (2010) estimated the N losses from food production in 2005 at 38.5 MT N yr⁻¹, which is much higher than the result of this study (27.2 MT N yr⁻¹) for the 2000s. This difference is mainly related to the difference in years and the numbers of food items; Ma et al (2010) included ten more plant-derived food items and five more animal-derived food items in their study compared to this study. Bai et al (2016) estimated total N losses from livestock production (including manure excretion, housing and storage) at 14.4 MT N yr⁻¹ in 2010, which is much larger than the result of this study (7.5 MT N yr⁻¹ in the 2000s) (table S16). This difference is related to the fact that our estimate is the average value from 2001–2010, while Bai et al (2016) estimated the N losses for 2010 (which are much higher than those in 2000). Also, Bai et al (2016) included sheep and goats, which are not included in this study.

N losses associated with vegetables, fruits and pig meat production increased after the 1980s, and accounted for 32%, 15% and 13% of the total N losses in China in the 2000s, respectively (table S17). N losses associated with the production of wheat, maize and rice reached a peak in the 1980s and then started to decrease. N losses associated with soybeans steadily decreased over the past five decades. N losses related to roots and animal-derived food items increased during the past five decades. Pig meat is the largest contributor to the N losses from animal-derived food (table S17).

Most papers about N footprints are also based on the N-Calculator methodology (Galloway et al 2014, Leach et al 2012, Pierer et al 2014, Shibata et al 2014, Stevens et al 2014, Liang et al 2016, Shibata et al 2017, Hutton et al 2017), which facilitate comparison. Here, we compare only the N footprint of food, as we did not consider the N footprint related to energy consumption.

The per capita food N footprint in China was 21.3 kg N capita⁻¹ yr⁻¹ with food trade and 21.5 kg N capita⁻¹ yr⁻¹ without food trade in the 2000s (figure 4). This is higher than the food N footprint of Tanzania, Austria and Germany, close to that of the Netherlands, but lower than those of the UK, the US, Japan and Australia. The proportion of the food production N footprint to the food N footprint ranged from 77% in Tanzania to 95% in the Netherlands, which is mainly related to the amount of food N consumption and the level of sewage treatment (figure 4). The N footprint of plant-derived food is much higher in China than in some other developed countries, regardless of whether the total per capita food N footprint was higher in those countries. The US food N footprint is dominated by meat based animal-derived food items and that of the Netherlands is dominated by non-meat animal-derived food items (i.e. dairy, eggs and fish) (figure S5).

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The VNFs indicate how much Nr is lost to the environment per unit of N in a food item consumed. The Chinese VNFs are generally higher than those of other countries, except for Japan. Japanese VNFs are especially high for meat products (pig meat, beef and poultry meat) (table 2), this is mainly related to the relatively low N use efficiency for feed crops and low feed conversion ratio for animals in Japan (Shibata et al 2014). A high chemical N fertilizer input and poor manure management in China caused a low NUE of crop and animal food production to consumption chain (Ma et al 2010, Zhang et al 2008, Yan et al 2014), which lead to high VNFs of food in China. For example, the average apparent recovery efficiency of applied nitrogen (RE_N) for Chinese cereal (i.e. wheat, rice and maize) production was 26%–28% from 2001 to 2005, much lower than the global average value of 40%–60% (Zhang et al 2008). The N use efficiency of crop production in China was only 26% in 2005 (Ma et al 2010, which was much lower than the average level of Europe and the United States (Dobermann 2007, Oenema et al 2009, Howarth et al 2002). A low recycling rate of animal manure is the main driver of low NUE in animal production in China. Only 33% of the amount of N excreted in animal manure was recycled, which is much lower than in the US (75%) (Doering et al 2011)and the European Union (80%) (Leip et al 2011). The NUE of animal production in China was 11% in 2005 (Ma et al 2010), which is also lower than the world average level of 15% according to Zhang et al (2008).

In this study, we did not take energy consumption during food production into consideration when calculating the food N footprint. Developing a database of energy consumption related to food production and consumption should be included in future calculation in China, especially for food items which are highly dependent on international trade. However, previous studies in other countries have found that the energy portion of the food N footprint is very small (Leach et al 2012, Liang et al 2016, Shibata et al 2014).

We used the American VNF of fish & seafood data for China and assumed no temporal changes during the past five decades. Additionally, we used the VNFs for the US as representative for all countries exporting food to China because the US VNFs were the only ones available for major exporters to China. However, Brazil is one of the most important soybean exporting country for China. The application of N footprint methods to more countries would benefit the estimation of the global N footprint.

We assumed there were no N losses from producing 'other feed products' (feed products except for maize and soybeans) because many of them are waste products (e.g. crop residue), this assumption underestimates the N footprint of animal-derived food items in China. We did not consider temporal changes in emission factors of N losses during plant-derived food production, which may cause uncertainties in food production N footprint and N losses results. Expanding the application of the N footprint methodology to a wider range of different specific food types and building a more complete emission factors database would also help to conduct a more accurate estimation of the N footprint and N losses of the food system in China.