Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Network resilience of phosphorus cycling in China has shifted by natural flows, fertilizer use and dietary transitions between 1600 and 2012

Abstract

The resilience of the phosphorus (P) cycling network is critical to ecosystem functioning and human activities. Although P cycling pathways have been previously mapped, a knowledge gap remains in evaluating the P network’s ability to withstand shocks or disturbances. Applying principles of mass balance and ecological network analysis, we examine the network resilience of P cycling in China from 1600 to 2012. The results show that changes in network resilience have shifted from being driven by natural P flows for food production to being driven by industrial P flows for chemical fertilizer production. Urbanization has intensified the one-way journey of P, further deteriorating network resilience. Over 2000–2012, the network resilience of P cycling has decreased by 11% owing to dietary changes towards more animal-based foods. A trade-off between network resilience improvement and increasing food trade is also observed. These findings can support policy decisions for enhanced P cycling network resilience in China.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: The evolution of resilience, α, and efficiency and redundancy of the P cycling network in China during 1600–2012.
Fig. 2: Relative contributions of changes in efficiency and redundancy to changes in the resilience of the P cycling network in China.
Fig. 3: Relative contributions of changes in the concentration degree of P flows, node inter-dependency and node inter-independency to changes in efficiency, redundancy and resilience of the P cycling network in China during 1600–2012.
Fig. 4: Critical links and nodes influencing the resilience of the P cycling network in China during 2000–2012.
Fig. 5: The P cycling network of China in 2012.

Similar content being viewed by others

Data availability

Calculations to generate 149-node P flow networks used data from Liu et al.12. All data used in this study are available from the corresponding authors upon reasonable request. Source data are provided with this paper.

Code availability

All computer codes generated in MATLAB 2019a and R version 3.6.1 for this study are available from the corresponding authors upon reasonable request.

References

  1. Cordell, D., Drangert, J.-O. & White, S. The story of phosphorus: global food security and food for thought. Glob. Environ. Change 19, 292–305 (2009).

    Article  Google Scholar 

  2. Elser, J. & Bennett, E. Phosphorus cycle: a broken biogeochemical cycle. Nature 478, 29–31 (2011).

    Article  ADS  CAS  Google Scholar 

  3. Scholz, R. W. & Wellmer, F.-W. Although there is no physical short-term scarcity of phosphorus, its resource efficiency should be improved. J. Ind. Ecol. 23, 313–318 (2019).

    Article  Google Scholar 

  4. Ulanowicz, R. E. The dual nature of ecosystem dynamics. Ecol. Model. 220, 1886–1892 (2009).

    Article  Google Scholar 

  5. Carpenter, S. R. & Bennett, E. M. Reconsideration of the planetary boundary for phosphorus. Environ. Res. Lett. 6, 014009 (2011).

    Article  ADS  Google Scholar 

  6. Steffen, W. et al. Planetary boundaries: guiding human development on a changing planet. Science 347, 1259855 (2015).

  7. Chen, M. & Graedel, T. A half-century of global phosphorus flows, stocks, production, consumption, recycling, and environmental impacts. Glob. Environ. Change 36, 139–152 (2016).

  8. Chowdhury, R. B., Moore, G. A., Weatherley, A. J. & Arora, M. A review of recent substance flow analyses of phosphorus to identify priority management areas at different geographical scales. Resour. Conserv. Recycl. 83, 213–228 (2014).

    Article  Google Scholar 

  9. Reinhard, C. T. et al. Evolution of the global phosphorus cycle. Nature 541, 386–389 (2017).

    Article  ADS  CAS  Google Scholar 

  10. Yuan, Z. et al. Human perturbation of the global phosphorus cycle: changes and consequences. Environ. Sci. Technol. 52, 2438–2450 (2018).

    Article  ADS  CAS  Google Scholar 

  11. Smil, V. Phosphorus in the environment: natural flows and human interferences. Annu. Rev. Energy Env. 25, 53–88 (2000).

    Article  Google Scholar 

  12. Liu, X. et al. Intensification of phosphorus cycling in China since the 1600s. Proc. Natl Acad. Sci. USA 113, 2609–2614 (2016).

    Article  ADS  CAS  Google Scholar 

  13. MacDonald, G. K. et al. Guiding phosphorus stewardship for multiple ecosystem services. Ecosyst. Health Sustain. 2, e01251 (2016).

    Article  Google Scholar 

  14. Sattari, S. Z., van Ittersum, M. K., Giller, K. E., Zhang, F. & Bouwman, A. F. Key role of China and its agriculture in global sustainable phosphorus management. Environ. Res. Lett. 9, 054003 (2014).

    Article  ADS  Google Scholar 

  15. Chen, M., Sun, F., Xia, X. & Chen, J. The phosphorus flow in China: a revisit from the perspective of production. Glob. Environ. Res. 19, 19–25 (2015).

    Google Scholar 

  16. Cui, S. et al. Changing urban phosphorus metabolism: evidence from Longyan City, China. Sci. Total Environ. 536, 924–932 (2015).

    Article  ADS  CAS  Google Scholar 

  17. Li, G.-L., Bai, X., Yu, S., Zhang, H. & Zhu, Y.-G. Urban phosphorus metabolism through food consumption: the case of China. J. Ind. Ecol. 16, 588–599 (2012).

    Article  CAS  Google Scholar 

  18. Li, S., Yuan, Z., Bi, J. & Wu, H. Anthropogenic phosphorus flow analysis of Hefei City, China. Sci. Total Environ. 408, 5715–5722 (2010).

    Article  ADS  CAS  Google Scholar 

  19. Ma, L. et al. Nitrogen and phosphorus use efficiencies and losses in the food chain in China at regional scales in 1980 and 2005. Sci. Total Environ. 434, 51–61 (2012).

    Article  ADS  CAS  Google Scholar 

  20. Qiao, M., Zheng, Y.-M. & Zhu, Y.-G. Material flow analysis of phosphorus through food consumption in two megacities in northern China. Chemosphere 84, 773–778 (2011).

    Article  ADS  CAS  Google Scholar 

  21. Yuan, Z., Liu, X., Wu, H., Zhang, L. & Bi, J. Anthropogenic phosphorus flow analysis of Lujiang County, Anhui Province, Central China. Ecol. Model. 222, 1534–1543 (2011).

    Article  CAS  Google Scholar 

  22. Yuan, Z., Sun, L., Bi, J., Wu, H. & Zhang, L. Phosphorus flow analysis of the socioeconomic ecosystem of Shucheng County, China. Ecol. Appl. 21, 2822–2832 (2011).

    Article  Google Scholar 

  23. Bi, J., Chen, Q., Zhang, L. & Yuan, Z. Quantifying phosphorus flow pathways through socioeconomic systems at the county level in China. J. Ind. Ecol. 17, 452–460 (2013).

    Article  Google Scholar 

  24. Jiang, S. & Yuan, Z. Phosphorus flow patterns in the Chaohu watershed from 1978 to 2012. Environ. Sci. Technol. 49, 13973–13982 (2015).

    Article  ADS  CAS  Google Scholar 

  25. Yuan, Z., Shi, J., Wu, H., Zhang, L. & Bi, J. Understanding the anthropogenic phosphorus pathway with substance flow analysis at the city level. J. Environ. Manag. 92, 2021–2028 (2011).

    Article  CAS  Google Scholar 

  26. Bai, Z. et al. Changes in phosphorus use and losses in the food chain of China during 1950–2010 and forecasts for 2030. Nutr. Cycl. Agroecosyst. 104, 361–372 (2016).

    Article  Google Scholar 

  27. Li, G. et al. Identifying potential strategies in the key sectors of China’s food chain to implement sustainable phosphorus management: a review. Nutr. Cycl. Agroecosyst. 104, 341–359 (2016).

    Article  Google Scholar 

  28. Ma, D., Hu, S., Chen, D. & Li, Y. Substance flow analysis as a tool for the elucidation of anthropogenic phosphorus metabolism in China. J. Clean. Prod. 29–30, 188–198 (2012).

    Article  Google Scholar 

  29. Ma, D., Hu, S., Chen, D. & Li, Y. The temporal evolution of anthropogenic phosphorus consumption in China and its environmental implications. J. Ind. Ecol. 17, 566–577 (2013).

    Article  Google Scholar 

  30. Wang, F. et al. The phosphorus footprint of China’s food chain: implications for food security, natural resource management, and environmental quality. J. Environ. Qual. 40, 1081–1089 (2011).

    Article  CAS  Google Scholar 

  31. Ma, L. et al. Modeling nutrient flows in the food chain of China. J. Environ. Qual. 39, 1279 (2010).

    Article  CAS  Google Scholar 

  32. Ulanowicz, R. E. Growth and Development: Ecosystems Phenomenology (Springer, 1986).

  33. Kharrazi, A., Rovenskaya, E. & Fath, B. D. Network structure impacts global commodity trade growth and resilience. PLoS ONE 12, e0171184 (2017).

    Article  Google Scholar 

  34. Goerner, S. J., Lietaer, B. & Ulanowicz, R. E. Quantifying economic sustainability: implications for free-enterprise theory, policy and practice. Ecol. Econ. 69, 76–81 (2009).

    Article  Google Scholar 

  35. Helin, J. & Weikard, H.-P. A model for estimating phosphorus requirements of world food production. Agric. Syst. 176, 102666 (2019).

    Article  Google Scholar 

  36. World Urbanization Prospects: The 2018 Revision; https://population.un.org/wup/country-profiles/ (United Nations, 2018).

  37. Global Food Losses and Food Waste – Extent, Causes and Prevention (FAO, 2011).

  38. Zhang, W. et al. Efficiency, economics, and environmental implications of phosphorus resource use and the fertilizer industry in China. Nutr. Cycl. Agroecosyst. 80, 131–144 (2008).

    Article  Google Scholar 

  39. Liu, G. Food Losses and Food Waste in China: A First Estimate OECD Food, Agriculture and Fisheries Papers No. 66 (OECD, 2014).

  40. Roy, R. N., Finck, A., Blair, G. J. & Tandon, H. L. S. Plant Nutrition for Food Security. A Guide for Integrated Nutrient Management (FAO, 2006).

  41. Cieślik, B. & Konieczka, P. A review of phosphorus recovery methods at various steps of wastewater treatment and sewage sludge management. The concept of “no solid waste generation” and analytical methods. J. Clean. Prod. 142, 1728–1740 (2017).

    Article  Google Scholar 

  42. Yokoyama, K. et al. Separation and recovery of phosphorus from steelmaking slags with the aid of a strong magnetic field. ISIJ Int. 47, 1541–1548 (2007).

    Article  CAS  Google Scholar 

  43. Action Plan for Zero Increase in Fertilizer Use by 2020 (Ministry of Agriculture, 2015); http://jiuban.moa.gov.cn/zwllm/tzgg/tz/201503/t20150318_4444765.htm

  44. UN Environment Programme, International Resource Panel (2018); http://www.resourcepanel.org

  45. Chen, S. & Chen, B. Urban energy–water nexus: a network perspective. Appl. Energy 184, 905–914 (2016).

    Article  CAS  Google Scholar 

  46. Fath, B. D. Quantifying economic and ecological sustainability. Ocean Coast. Manag. 108, 13–19 (2015).

    Article  Google Scholar 

  47. Panyam, V., Huang, H., Davis, K. & Layton, A. Bio-inspired design for robust power grid networks. Appl. Energy 251, 113349 (2019).

    Article  Google Scholar 

  48. Kharrazi, A. & Fath, B. D. Measuring global oil trade dependencies: an application of the point-wise mutual information method. Energy Policy 88, 271–277 (2016).

    Article  Google Scholar 

  49. Ang, B. W. & Zhang, F. Q. A survey of index decomposition analysis in energy and environmental studies. Energy 25, 1149–1176 (2000).

    Article  CAS  Google Scholar 

  50. Weik, M. H. in Computer Science and Communications Dictionary (ed. Weik, M. H.) 1074–1074 (Springer, 2001).

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (71874014, 51721093, 71704055, 71704015 and 41661144023), the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement CIFTRESS no. 840205, Natural Science Funds for Distinguished Young Scholar of Guangdong Province, China (2018B030306032) and the Fundamental Research Funds for the Central Universities.

Author information

Authors and Affiliations

Authors

Contributions

S.L., Y.Y., A.K. and Z.M. designed the study. S.L. and Y.Y. collected data and conducted calculations. S.L., Y.Y., A.K., B.D.F., G.T.D. and S.C. led the analysis. S.L., Y.Y., A.K., B.D.F., C.F., G.T.D., S.C., T.M., B.Z., Z.M. and Z.Y. contributed to the writing.

Corresponding authors

Correspondence to Sai Liang, Yadong Yu or Zhifu Mi.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Distribution of values for the resilience of the P cycling network in China during 1600–2012.

The resilience values of the P cycling network during 1600–2012 are distributed in the curve of the theoretical relationship between resilience and α.

Source data

Extended Data Fig. 2 Changes of human P demand in China during 1950–2012.

The contribution of each category of P demand to the total P demand is shown in a different colour.

Source data

Extended Data Fig. 3 Changes of food structure in China during 1950–2012.

Food structure is calculated as the sum of P content in all foods except for grain divided by P content in grain.

Source data

Extended Data Fig. 4 Uncertainties in the efficiency, redundancy, α, and resilience of the P cycling network in China during 1600–2012.

Uncertainties are calculated by Monte Carlo simulation sampling 10,000 times. The upper boundary of the range indicates maximum values; the lower boundary of the range represents minimum values; and the solid line stands for average values.

Source data

Extended Data Fig. 5 Comparisons of α values between the 149-node and 16-node networks.

The overly efficient area is separated from the overly redundant area by the line where α = 0.3679 in the figure.

Source data

Extended Data Fig. 6 Comparisons of network resilience between the 149-node and 16-node networks.

The maximum value of resilience is 0.3679 in the figure.

Source data

Supplementary information

Supplementary Information

Supplementary Table 1 title and caption, Tables 2–11, notes, methods, discussion and references.

Reporting Summary

Supplementary Table 1

The list of nodes in the Chinese P cycling network.

Source data

Source Data Fig. 1

Resilience, α, and efficiency and redundancy of the P cycling network in China during 1600–2012.

Source Data Fig. 2

Relative contributions of changes in efficiency and redundancy to changes in the resilience of the P cycling network in China during 1600–2012.

Source Data Fig. 3

Relative contributions of changes in concentration degree of P flows, node inter-dependency and node inter-independency to changes in efficiency, redundancy, and resilience of the P cycling network in China during 1600–2012.

Source Data Fig. 4

Contributions of changes in links and nodes to changes in the resilience of the P cycling network in China during 2000–2012.

Source Data Fig. 5

The P flow network of China in 2012.

Source Data Extended Data Fig. 1

α and resilience of the P cycling network in China during 1600–2012.

Source Data Extended Data Fig. 2

Human P demand in China during 1950–2012.

Source Data Extended Data Fig. 3

Food structure in China during 1950–2012.

Source Data Extended Data Fig. 4

Uncertainties in the efficiency, redundancy, α, and resilience of the P cycling network in China during 1600–2012.

Source Data Extended Data Fig. 5

α values for the 149-node and 16-node P cycling networks in China during 1600–2012.

Source Data Extended Data Fig. 6

Network resilience for the 149-node and 16-node P cycling networks in China during 1600–2012.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liang, S., Yu, Y., Kharrazi, A. et al. Network resilience of phosphorus cycling in China has shifted by natural flows, fertilizer use and dietary transitions between 1600 and 2012. Nat Food 1, 365–375 (2020). https://doi.org/10.1038/s43016-020-0098-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s43016-020-0098-6

This article is cited by

Search

Quick links

Nature Briefing Anthropocene

Sign up for the Nature Briefing: Anthropocene newsletter — what matters in anthropocene research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Anthropocene