Advertisement

Biogeochemistry

, Volume 144, Issue 3, pp 273–290 | Cite as

Decreased buffering capacity and increased recovery time for legacy phosphorus in a typical watershed in eastern China between 1960 and 2010

  • Dingjiang ChenEmail author
  • Yufu Zhang
  • Hong Shen
  • Mengya Yao
  • Minpeng Hu
  • Randy A. Dahlgren
Article

Abstract

Legacy phosphorus (P) accumulated in watersheds from excessive historical P inputs is recognized as an important component of water pollution control and sustainable P management in watersheds worldwide. However, little is known about how watershed P buffering capacity responds to legacy P pressures over time and how long it takes for riverine P concentrations to recover to a target level, especially in developing countries. This study examined long-term (1960–2010) accumulated legacy P stock, P buffering capacity and riverine TP flux dynamics to predict riverine P-reduction recovery times in the Yongan watershed of eastern China. Due to a growing legacy P stock coupled with changes in land use and climate, estimated short- and long-term buffering metrics (i.e., watershed ability to retain current year and historically accumulated surplus P, respectively) decreased by 65% and 36%, respectively, resulting in a 15-fold increase of riverine P flux between 1980 and 2010. An empirical model incorporating accumulated legacy P stock and annual precipitation was developed (R2 = 0.99) and used to estimate a critical legacy P stock of 22.2 ton P km−2 (95% CI 19.4–25.3 ton P km−2) that would prevent exceedance of a target riverine TP concentration of 0.05 mg P L−1. Using an exponential decay model, the recovery time for depleting the estimated legacy P stock in 2010 (29.3 ton P km−2) to the critical level (22.2 ton P km−2) via riverine flux was 456 years (95% CI 353–560 years), 159 years (95% CI 57–262 years) and 318 years (95% CI 238–400 years) under scenarios of a 4% reduction in annual P inputs, total cessation of P inputs, and 4% reduction of annual P inputs with a 10% increase in average annual precipitation, respectively. Given the lower P buffering capacity and lengthening recovery time, strategies to reduce P inputs and utilize soil legacy P for crop production are necessary to effectively control riverine P pollution and conserve global rock P resources. A long-term perspective that incorporates both contemporary and historical information is required for developing sustainable P management strategies to optimize both agronomic and environmental benefits at the watershed scale.

Keywords

Phosphorus Legacy nutrients Watershed Phosphorus buffering capacity Eutrophication Lag time 

Notes

Acknowledgements

We thank local government departments for providing data critical for this investigation. This work was supported by the National Natural Science Foundation of China (51679210 and 41877465), National Key Research and Development Program of China (2017YFD0800101) and Zhejiang Provincial Natural Science Foundation of China (LR19D010002).

Compliance with ethical standards

Conflict of interest

This study has no conflict of interest with any persons or affiliations.

References

  1. Abbott BW, Moatar F, Gauthier O, Fovet O, Antoine V, Ragueneau O (2018) Trends and seasonality of river nutrients in agricultural catchments: 18 years of weekly citizen science in France. Sci Total Environ 624:845–858.  https://doi.org/10.1016/j.scitotenv.2017.12.176 CrossRefGoogle Scholar
  2. Agricultural Bureau of Xianju County (2011) Agricultural Ecological Environment Quality Assessment in the Yongan River Watershed. http://www.xjlsncp.com/html/main/nyqhView/2011-12/6533.html. Accessed Oct 2014
  3. Borbor-Cordova MJ, Boyer EW, McDowell WH, Hall CA (2006) Nitrogen and phosphorus budgets for a tropical watershed impacted by agricultural land use: Guayas, Ecuador. Biogeochemistry 79:135–161.  https://doi.org/10.1007/s10533-006-9009-7 CrossRefGoogle Scholar
  4. Carpenter SR (2005) Eutrophication of aquatic ecosystems: bistability and soil phosphorus. Proc Natl Acad Sci 102:10002–10005.  https://doi.org/10.1073/pnas.0503959102 CrossRefGoogle Scholar
  5. Carpenter SR (2008) Phosphorus control is critical to mitigating eutrophication. Proc Natl Acad Sci 105:11039–11040.  https://doi.org/10.1073/pnas.0806112105 CrossRefGoogle Scholar
  6. Chen DJ, Hu MP, Guo Y, Dahlgren RA (2015a) Influence of legacy phosphorus, land use, and climate change on anthropogenic phosphorus inputs and riverine export dynamics. Biogeochemistry 123:99–116.  https://doi.org/10.1007/s10533-014-0055-2 CrossRefGoogle Scholar
  7. Chen DJ, Hu MP, Guo Y, Dahlgren RA (2015b) Reconstructing historical changes in phosphorus inputs to rivers from point and nonpoint sources in a rapidly developing watershed in eastern China, 1980–2010. Sci Total Environ 533:196–204.  https://doi.org/10.1016/j.scitotenv.2015.06.079 CrossRefGoogle Scholar
  8. Chen DJ, Hu MP, Wang JH, Dahlgren RA (2016) Factors controlling phosphorus export from agricultural/forest and residential systems to rivers in eastern China, 1980–2011. J Hydrol 533:53–61.  https://doi.org/10.1016/j.jhydrol.2015.11.043 CrossRefGoogle Scholar
  9. Chen DJ, Hu MP, Guo Y (2017) Long-term (1980–2010) changes in cropland phosphorus budgets, use efficiency and legacy pools across townships in the Yongan watershed, eastern China. Agric Ecosyst Environ 236:166–176.  https://doi.org/10.1016/j.agee.2016.12.003 CrossRefGoogle Scholar
  10. Chen DJ, Shen H, Hu MP, Wang JH, Zhang YF, Dahlgren RA (2018) Legacy nutrient dynamics at the watershed scale: principles, modeling, and implications. Adv Agron 149:237–313.  https://doi.org/10.1016/bs.agron.2018.01.003 CrossRefGoogle Scholar
  11. Conley DJ, Paerl HW, Howarth RW, Boesch DF, Seitzinger SP, Havens KE, Lancelot C, Likens GE (2009) Controlling eutrophication: nitrogen and phosphorus. Science 323:1014–1015.  https://doi.org/10.1126/science.1167755 CrossRefGoogle Scholar
  12. Cui SH, Xu S, Huang W, Bai XM, Huang YF, Li GL (2015) Changing urban phosphorus metabolism: evidence from Longyan City, China. Sci Total Environ 536:924–932.  https://doi.org/10.1016/j.scitotenv.2015.06.073 CrossRefGoogle Scholar
  13. Doody DG, Withers PJA, Dils RM, McDowell RW, Smith V, McElarney YR, Dunbar M, Daly D (2016) Optimising land use for the delivery of catchment ecosystem services. Front Ecol Environ 14:325–332.  https://doi.org/10.1002/fee.1296 CrossRefGoogle Scholar
  14. Dubus IG, Becquer T (2001) Phosphorus sorption and desorption in oxide-rich Ferralsols of New Caledonia. Soil Res 39:403–414.  https://doi.org/10.1071/SR00003 CrossRefGoogle Scholar
  15. Gaba S, Lescourret F, Boudsocq S, Enjalbert J, Hinsinger P, Journet E-P, Navas M-L, Wery J, Louarn G, Malézieux E, Pelzer E, Prudent M, Ozier- Lafontaine H (2014) Multiple cropping systems as drivers for providing multiple ecosystem services: from concepts to design. Agron Sustain Dev 35:607–623.  https://doi.org/10.1007/s13593-014-0272-z CrossRefGoogle Scholar
  16. Gao C, Zhang TL (2010) Eutrophication in a Chinese context: understanding various physical and socio-economic aspects. Ambio 39:385–393.  https://doi.org/10.1007/s13280-010-0040-5 CrossRefGoogle Scholar
  17. Gentry LE, David MB, Royer TV, Mitchell CA, Starks KM (2007) Phosphorus transport pathways to streams in tile-drained agricultural watersheds. J Environ Qual 36:408–415.  https://doi.org/10.2134/jeq2006.0098 CrossRefGoogle Scholar
  18. Goyette JO, Bennett EM, Howarth RW, Maranger R (2016) Changes in anthropogenic nitrogen and phosphorus inputs to the St. Lawrence sub-basin over 110 years and impacts on riverine export. Glob Biogeochem Cycl 30:1000–1014.  https://doi.org/10.1002/2016GB005384 CrossRefGoogle Scholar
  19. Goyette JO, Bennett EM, Maranger R (2018) Low buffering capacity and slow recovery of anthropogenic phosphorus pollution in watersheds. Nat Geosci 11:921–925.  https://doi.org/10.1038/s41561-018-0238-x CrossRefGoogle Scholar
  20. Gu S, Gruau G, Dupas R, Petitjean P, Li Q, Pinay G (2019) Respective roles of Fe-oxyhydroxide dissolution, pH changes and sediment inputs in dissolved phosphorus release from wetland soils under anoxic conditions. Geoderma 338:365–374.  https://doi.org/10.1016/j.geoderma.2018.12.034 CrossRefGoogle Scholar
  21. Hamilton JD (1994) Time series analysis. Princeton University Press, PrincetonGoogle Scholar
  22. Hamilton SK (2012) Biogeochemical time lags may delay responses of streams to ecological restoration. Freshwater Biol 57:43–57.  https://doi.org/10.1111/j.1365-2427.2011.02685.x CrossRefGoogle Scholar
  23. Han H, Bosch N, Allan JD (2011) Spatial and temporal variation in phosphorus budgets for 24 watersheds in the Lake Erie and Lake Michigan basins. Biogeochemistry 102:45–58.  https://doi.org/10.1007/s10533-010-9420-y CrossRefGoogle Scholar
  24. Han H, Allan JD, Bosch NS (2012) Historical pattern of phosphorus loading to Lake Erie watersheds. J Great Lakes Res 38:289–298.  https://doi.org/10.1016/j.jglr.2012.03.004 CrossRefGoogle Scholar
  25. Han YG, Yu XX, Wang XX, Wang YQ, Tian JX, Xu L, Wang CZ (2013) Net anthropogenic phosphorus inputs (NAPI) index application in Mainland China. Chemosphere 90:329–337.  https://doi.org/10.1016/j.chemosphere.2012.07.023 CrossRefGoogle Scholar
  26. Han YG, Fan YT, Yang PL, Wang XX, Wang YJ, Tian JX, Xu L, Wang CZ (2014) Net anthropogenic nitrogen inputs (NANI) index application in Mainland China. Geoderma 213:87–94.  https://doi.org/10.1016/j.geoderma.2013.07.019 CrossRefGoogle Scholar
  27. Haygarth PM, Jarvie HP, Powers SM, Sharpley AN, Elser JJ, Shen JB, Peterson HM, Chan NI, Howden NJK, Burt T, Worrall F, Zhang FS, Liu XJ (2014) Sustainable phosphorus management and the need for a long-term perspective: the legacy hypothesis. Environ Sci Technol.  https://doi.org/10.1021/es502852 Google Scholar
  28. Hong B, Swaney DP, Mörth C-M, Smedberg E, Hägg EH, Humborg C, Howarth RW, Bouraoui F (2012) Evaluating regional variation of net anthropogenic nitrogen and phosphorus inputs (NANI/NAPI), major drivers, nutrient retention pattern and management implications in the multinational areas of Baltic Sea basin. Ecol Model 227:117–135.  https://doi.org/10.1016/j.ecolmodel.2011.12.002 CrossRefGoogle Scholar
  29. Hou Y, Ma L, Gao ZL, Wang FH, Sims JT, Ma WQ, Zhang FS (2013) The driving forces for nitrogen and phosphorus flows in the food chain of China, 1980 to 2010. J Environ Qual 42:962–971.  https://doi.org/10.2134/jeq2012.0489 CrossRefGoogle Scholar
  30. Howarth R, Chan F, Conley DJ, Garnier J, Doney SC, Marino R, Billen G (2011) Coupled biogeochemical cycles: eutrophication and hypoxia in temperate estuaries and coastal marine ecosystems. Front Ecol Environ 9:18–26.  https://doi.org/10.1890/100008 CrossRefGoogle Scholar
  31. Hu MP, Liu YM, Wang JH, Dahlgren RA, Chen DJ (2018) A modification of the regional nutrient management model (ReNuMa) to identify long-term changes in riverine nitrogen sources. J Hydrol 561:31–42.  https://doi.org/10.1016/j.jhydrol.2018.03.068 CrossRefGoogle Scholar
  32. Jarvie HP, Sharpley AN, Withers PJA, Scott JT, Haggard BE, Neal C (2013) Phosphorus mitigation to control river eutrophication: murky waters, inconvenient truths and ‘post-normal’ science. J Environ Qual 42:295–304.  https://doi.org/10.2134/jeq2012.0085 CrossRefGoogle Scholar
  33. Jarvie HP, Sharpley AN, Brahana V, Simmons T, Price A, Neal C, Lawlor AJ, Sleep D, Thacker S, Haggard BE (2014) Phosphorus retention and remobilization along hydrological pathways in Karst Terrain. Environ Sci Technol 48:4860–4868.  https://doi.org/10.1021/es405585b CrossRefGoogle Scholar
  34. Jiang SY, Yuan ZW (2015) Phosphorus flow patterns in the Chaohu watershed from 1978 to 2012. Environ Sci Technol 49:13973–13982.  https://doi.org/10.1021/acs.est.5b03202 CrossRefGoogle Scholar
  35. Kang LL (2008) Prediction of future climate change scenarios in Zhejiang Province. Annual meeting of the Chinese meteorological society: climate change parallel sessions. Yantai City, Shangdong Province, China (in Chinese)Google Scholar
  36. Kleinman PJA, Sharpley AN, McDowell RW, Flaten DN, Buda AR, Tao L, Bergstrom L, Zhu Q (2011) Managing agricultural phosphorus for water quality protection: principles for progress. Plant Soil 349:169–182.  https://doi.org/10.1007/s11104-011-0832-9 CrossRefGoogle Scholar
  37. Kolbe T, Marçais J, Thomas Z, Abbott BW, de Dreuzy JR, Rousseau-Gueutin P, Aquilina L, Labasque T, Pinay G (2016) Coupling 3D groundwater modeling with CFC-based age dating to classify local groundwater circulation in an unconfined crystalline aquifer. J Hydrol 543:31–46.  https://doi.org/10.1016/j.jhydrol.2016.05.020 CrossRefGoogle Scholar
  38. Kolbe T, de Dreuzy JR, Abbott BW, Aquilina L, Babey T, Green CT, Fleckenstein JH, Labasque T, Laverman AM, Marçais J, Peiffer S, Thomas Z, Pinay G (2019) Stratification of reactivity determines nitrate removal in groundwater. Proc Natl Acad Sci 116:2494–2499.  https://doi.org/10.1073/pnas.1816892116 CrossRefGoogle Scholar
  39. Kusmer AS, Goyette JO, MacDonald GK, Bennett EM, Maranger R, Withers PJA (2018) Watershed buffering of legacy phosphorus pressure at a regional scale: a comparison across space and time. Ecosystems 22:91–109.  https://doi.org/10.1007/s10021-018-0255-z CrossRefGoogle Scholar
  40. Li ZW, Yuan J, Bi H, Wu J (2010) Anthropogenic phosphorus flow analysis of Hefei City, China. Sci Total Environ 408:5715–5722.  https://doi.org/10.1016/j.scitotenv.2010.08.052 CrossRefGoogle Scholar
  41. Liu XJ, Vitousek P, Chang YH, Zhang WF, Matson P, Zhang FS (2016) Evidence for a historic change occurring in China. Environ Sci Technol 50:505–506.  https://doi.org/10.1021/acs.est.5b05972 CrossRefGoogle Scholar
  42. MacDonald GK, Bennett EM, Potter PA, Ramankutty N (2011) Agronomic phosphorus imbalances across the world’s croplands. Proc Natl Acad Sci 108:3086–3091.  https://doi.org/10.1073/pnas.1010808108 CrossRefGoogle Scholar
  43. Macintosh KA, Doody DG, Withers PJ, McDowell RW, Smith DR, Johnson LT, Bruulsema TW, O’Flaherty V, McGrath JW (2019) Transforming soil phosphorus fertility management strategies to support the delivery of multiple ecosystem services from agricultural systems. Sci Total Environ 649:90–98.  https://doi.org/10.1016/j.scitotenv.2018.08.272 CrossRefGoogle Scholar
  44. Marçais J, Gauvain A, Labasque T, Abbott BW, Pinay G, Aquilina L, Chabaux F, Viville D, de Dreuzy JR (2018) Dating groundwater with dissolved silica and CFC concentrations in crystalline aquifers. Sci Total Environ 636:260–272.  https://doi.org/10.1016/j.scitotenv.2018.04.196 CrossRefGoogle Scholar
  45. McCrackin ML, Muller-Karulis B, Gustafsson BG, Howarth RW, Humborg C, Svanbäck A, Swaney D (2018) A century of legacy phosphorus dynamics in a large drainage basin. Glob Biogeochem Cycle 32:1107–1122.  https://doi.org/10.1029/2018GB005914 CrossRefGoogle Scholar
  46. Meals DW, Dressing SA, Davenport TE (2010) Lag time in water quality response to best management practices: a review. J Environ Qual 39:85–96.  https://doi.org/10.2134/jeq2009.0108 CrossRefGoogle Scholar
  47. Metson GS, Lin JJ, Harrison JA, Compton JE (2017) Linking terrestrial phosphorus inputs to riverine export across the United States. Water Res 124:177–191.  https://doi.org/10.1016/j.watres.2017.07.037 CrossRefGoogle Scholar
  48. Moriasi DN, Arnold JG, Van Liew MW, Bingner RL, Harmel RD, Veith TL (2007) Model evaluation guidelines for systematic quantification of accuracy in watershed simulations. Trans ASABE 50:885–900.  https://doi.org/10.13031/2013.23153 CrossRefGoogle Scholar
  49. Morse NB, Wollheim WM (2014) Climate variability masks the impacts of land use change on nutrient export in a suburbanizing watershed. Biogeochemistry 121:45–59.  https://doi.org/10.1007/s10533-014-9998-6 CrossRefGoogle Scholar
  50. Okajima H, Kubota H, Sakuma T (1983) Hysteresis in the phosphorus sorption and desorption processes of soils. Soil Sci Plant Nutr 29:271–283.  https://doi.org/10.1080/00380768.1983.10434628 CrossRefGoogle Scholar
  51. Pinay G, Bernal S, Abbott BW, Lupon A, Marti E, Sabater F, Krause S (2018) Riparian corridors: a new conceptual framework for assessing nitrogen buffering across biomes. Front Environ Sci.  https://doi.org/10.3389/fenvs.2018.00047 Google Scholar
  52. Powers SM, Bruulsema TW, Burt TP, Chan NI, Elser JJ, Haygarth PM, Howden NJK, Jarvie HP, Lyu Y, Peterson HM, Sharpley AN (2016) Long-term accumulation and transport of anthropogenic phosphorus in three river basins. Nat Geosci 9:353–356.  https://doi.org/10.1038/ngeo2693 CrossRefGoogle Scholar
  53. Qiu JX, Turner MG (2015) Importance of landscape heterogeneity in sustaining hydrologic ecosystem services in an agricultural watershed. Ecosphere 6:1–19.  https://doi.org/10.1890/ES15-00312.1 CrossRefGoogle Scholar
  54. Reed T, Carpenter SR (2002) Comparisons of P-yield, riparian buffer strips, and land cover in six agricultural watersheds. Ecosystems 5:568–577.  https://doi.org/10.1007/s10021-002-0159-8 CrossRefGoogle Scholar
  55. Rowe H, Withers PJA, Baas P, Chan NI, Doody D, Holiman J, Jacobs B, Li HG, MacDonald GK, McDowell R, Sharpley AN, Shen JB, Taheri W, Wallenstein M, Weintraub MN (2016) Integrating legacy soil phosphorus into sustainable nutrient management strategies for future food, bioenergy and water security. Nutr Cycles Agroecosyst 104:393–412.  https://doi.org/10.1007/s10705-015-9726-1 CrossRefGoogle Scholar
  56. Runkel RL, Crawford CG, Cohn TA (2004) Load estimator (Loadest): A Fortran program for estimating constituent loads in streams and rivers. http://pubs.usgs.gov/tm/2005/tm4A5/pdf/508final.pdf. Accessed 26 June 2014
  57. Russell MJ, Weller DE, Jordan TE, Sigwart KJ, Sullivan KJ (2008) Net anthropogenic phosphorus inputs: spatial and temporal variability in the Chesapeake Bay region. Biogeochemistry 88:285–304.  https://doi.org/10.1007/s10533-008-9212-9 CrossRefGoogle Scholar
  58. Sanford WE, Pope JP (2013) Quantifying groundwater’s role in delaying improvements to Chesapeake Bay water quality. Environ Sci Technol 47:13330–13338.  https://doi.org/10.1021/es401334k CrossRefGoogle Scholar
  59. Sattari SZ, Bouwman AF, Giller KE, van Ittersum MK (2012) Residual soil phosphorus as the missing piece in the global phosphorus crisis puzzle. Proc Natl Acad Sci 109:6348–6353.  https://doi.org/10.1073/pnas.1113675109 CrossRefGoogle Scholar
  60. Sebilo M, Mayer B, Nicolardot B, Pinay G, Mariotti A (2013) Long-term fate of nitrate fertilizer in agricultural soils. Proc Natl Acad Sci 110:18185–18189.  https://doi.org/10.1073/pnas.1305372110 CrossRefGoogle Scholar
  61. Sharpley AN, Kleinman PJA, Heathwaite AL, Gburek WJ, Folmar GJ, Schmidt JP (2008) Phosphorus loss from an agricultural watershed as a function of storm size. J Environ Qual 37:362–368.  https://doi.org/10.2134/jeq2007.0366 CrossRefGoogle Scholar
  62. Sharpley AN, Jarvie HP, Buda A, May L, Spears B, Kleinman P (2013) Phosphorus legacy: overcoming the effects of past management practices to mitigate future water quality impairment. J Environ Qual 42:1308–1326.  https://doi.org/10.2134/jeq2013.03.0098 CrossRefGoogle Scholar
  63. Shigaki F, Sharpley A, Prochnow LI (2007) Rainfall intensity and phosphorus source effects on phosphorus transport in surface runoff from soil trays. Sci Total Environ 373:334–343.  https://doi.org/10.1016/j.scitotenv.2006.10.048 CrossRefGoogle Scholar
  64. Sjö B (2008) Testing for unit roots and cointegration. https://pdfs.semanticscholar.org/7ce6/2a0c7f6dab85f264a5403bf9b99a0f20a156.pdf. Accessed July 2019
  65. Sobota DJ, Harrison JA, Dahlgren RA (2011) Linking dissolved and particulate phosphorus export in rivers draining California’s Central Valley with anthropogenic sources at the regional scale. J Environ Qual 40:1290–1302.  https://doi.org/10.2134/jeq2011.0010 CrossRefGoogle Scholar
  66. Ti CP, Pan JJ, Xia YQ, Yan XY (2012) A nitrogen budget of mainland China with spatial and temporal variation. Biogeochemistry 108:381–394.  https://doi.org/10.2307/41410602 CrossRefGoogle Scholar
  67. Uehara G, Gillman G (1981) The mineralogy, chemistry, and physics of tropical soils with variable charge clays. Westview Press, BoulderGoogle Scholar
  68. USEPA (2006) An Approach for Using Load Duration Curves in Developing TMDLs. https://www.epa.gov/sites/production/files/2015-07/documents/2007_08_23_tmdl_duration_curve_guide_aug2007.pdf. US Environmental Protection Agency, Washington, DC. Accessed Feb 2019
  69. Van Meter KJ, Basu NB (2017) Time lags in watershed-scale nutrient transport: an exploration of dominant controls. Environ Res Lett 12:084017.  https://doi.org/10.1088/1748-9326/aa7bf4 CrossRefGoogle Scholar
  70. Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15.  https://doi.org/10.1890/08-0127.1 CrossRefGoogle Scholar
  71. Voss M, Deutsch B, Elmgren R, Humborg C, Kuuppo P, Pastuszak M, Rolff C, Schulte U (2006) Source identification of nitrate by means of isotopic tracers in the Baltic Sea catchments. Biogeosciences 3:663–676.  https://doi.org/10.5194/bg-3-663-2006 CrossRefGoogle Scholar
  72. Withers PJA, Jarvie HP (2008) Delivery and cycling of phosphorus in rivers: a review. Sci Total Environ 400:379–395.  https://doi.org/10.1016/j.scitotenv.2008.08.002 CrossRefGoogle Scholar
  73. Withers PJA, Sylvester-Bradley R, Jones DL, Healey JR, Talboys PJ (2014) Feed the crop not the soil: rethinking phosphorus management in the food chain. Environ Sci Technol 48:6523–6530.  https://doi.org/10.1021/es501670j CrossRefGoogle Scholar
  74. Withers PJA, Rodrigues M, Soltangheisi A, Carvalho TS, Guilherme LRG, Benites VM, Gatiboni LC, Sousa DMG, Nunes RDS, Rosolem CA (2018) Transitions to sustainable management of phosphorus in Brazilian agriculture. Sci Rep 8:2537.  https://doi.org/10.1038/s41598-018-20887-z CrossRefGoogle Scholar
  75. Yan XY, Cai ZC, Yang R, Ti CP, Xia YQ, Li FY, Wang JQ, Ma AJ (2011) Nitrogen budget and riverine nitrogen output in a rice paddy dominated agricultural watershed in eastern China. Biogeochemistry 106:489–501.  https://doi.org/10.1007/s10533-010-9528-0 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Dingjiang Chen
    • 1
    • 2
    Email author
  • Yufu Zhang
    • 1
  • Hong Shen
    • 1
  • Mengya Yao
    • 1
  • Minpeng Hu
    • 1
    • 3
  • Randy A. Dahlgren
    • 4
  1. 1.College of Environmental Science and ResourcesZhejiang UniversityHangzhouChina
  2. 2.Ministry of Education Key Laboratory of Environment Remediation and Ecological HealthZhejiang UniversityHangzhouChina
  3. 3.Zhejiang Provincial Key Laboratory of Subtropical Soil and Plant NutritionZhejiang UniversityHangzhouChina
  4. 4.Department of Land, Air, and Water ResourcesUniversity of CaliforniaDavisUSA

Personalised recommendations