National Center for Water Quality Research (NCWQR)
Published December 21, 2016 | Version v1
Journal article Open

Guiding phosphorus stewardship for multiple ecosystem services

Creators

  • 1. McGill University
  • 2. Centre for Ecology and Hydrology
  • 3. Bangor University
  • 4. Agri-Food and Biosciences Institute
  • 5. University of Minnesota
  • 6. Lancaster University
  • 7. National Center for Water Quality Research
  • 8. Invermay Agricultural Centre and Lincoln University
  • 9. University of Cape Coast
  • 10. Washington State University
  • 11. University of Arkansas
  • 12. China Agricultural University
  • 13. Grassland, Soil and Water Research Laboratory, USDA-ARS
  • 14. University of Toledo
  • 15. Agriculture and Agri-Food Canada

Description

ABSTRACT

The essential role of phosphorus (P) for agriculture and its impact on water quality has received decades of research attention. However, the benefits of sustainable P use and management for society due to its downstream impacts on multiple ecosystem services are rarely acknowledged. We propose a conceptual framework—the “phosphorus-ecosystem services cascade” (PESC) to integrate the key ecosystem processes and functions that moderate the relationship between P released to the environment from human actions and ecosystem services at distinct spatial and temporal scales. Indirect pathways in the cascade via soil and aquatic processes link anthropogenic P to biodiversity and multiple services, including recreation, drinking water provision, and fisheries. As anthropogenic P cascades through catchments, it often shifts from a subsidy to a stressor of ecosystem services. Phosphorus stewardship can have emergent ecosystem service co-benefits due to synergies with other societal or management goals (e.g., recycling of livestock manures and organic wastes could impact soil carbon storage). Applying the PESC framework, we identify key research priorities to align P stewardship with the management of multiple ecosystem services, such as incorporating additional services into agri-environmental P indices, assessing how widespread recycling of organic P sources could differentially impact agricultural yields and water quality, and accounting for shifting baselines in P stewardship due to climate change. Ultimately, P impacts depend on site-specific agricultural and biogeophysical contexts, so greater precision in targeting stewardship strategies to specific locations would help to optimize for ecosystem services and to more effectively internalize the downstream costs of farm nutrient management.

Notes

The PESC framework was developed as part of the Sustainable Phosphorus Initiative, a National Science Foundation (NSF) Research Coordination Network (Science, Engineering, and Education for Sustainability Program, RCN-SEES, award #1230603). We thank all workshop participants for fostering discussion about the PESC, as well as two anonymous reviewers for feedback on the manuscript. Research support for GKM came from the Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants Program, to HPJ and PMH from the Natural Environment Research Council of the UK (NERC), to RWM from the National Science Challenge—Our Land and Water, to JS from the National Natural Science Foundation of China, and to TZ from the Growing Forward-2 Research Program of Agricultural and Agri-Food Canada. Vector graphics used in Fig. 2 were created by Tracey Saxby, Jane Hawkey, Jason C. Fisher, Diana Kleine, and Jane Thomas via the Integration and Application Network, University of Maryland Center for Environmental Science (ian.umces.edu/imagelibrary/).

Files

MacDonald et al 2016 Ecosystem_Health_and_Sustainability.pdf

Files (2.0 MB)

Additional details

References

  • Aktar, M. D., D. Sengupta, and A. Chowdhury. 2009. Impact of pesticides use in agriculture: their benefits and hazards. Interdisciplinary Toxicology 2:1–12.
  • Bai, Z., et al. 2013. The critical soil P levels for crop yield, soil fertility and environmental safety in different soil types. Plant and Soil 372:27–37.
  • Barrow, N. J., and A. Debnath. 2014. Effect of phosphate status on the sorption and desorption properties of some soils of northern India. Plant and Soil 378:383–395.
  • Bender, S. F., and M. G. A. van der Heijden. 2015. Soil biota enhance agricultural sustainability by improving crop yield, nutrient uptake and reducing nitrogen leaching losses. Journal of Applied Ecology 52:228–239.
  • Bennett, E. M., G. D. Peterson, and L. J. Gordon. 2009. Understanding relationships among multiple ecosystem services. Ecology Letters 12:1394–1404.
  • Braat, L. C., and R. de Groot. 2012. The ecosystem services agenda: bridging the worlds of natural science and economics, conservation and development, and public and private policy. Ecosystem Services 1:4–15.
  • Brauman, K. A., G. C. Daily, T. K. E. Duarte, and H. A. Mooney. 2007. The nature and value of ecosystem services: an overview highlighting hydrologic services. Annual Review of Environment and Resources 32:67–98.
  • Burson, A., M. Stomp, L. Akil, C. P. Brussaard, and J. Huisman. 2016. Unbalanced reduction of nutrient loads has created an offshore gradient from phosphorus to nitrogen limitation in the North Sea. Limnology and Oceanography 61: 869–888.
  • Carpenter, S. R. 2005. Eutrophication of aquatic ecosystems: bistability and soil phosphorus. Proceedings of the National Academy of Sciences of the United States of America 102: 10002–10005.
  • Cassidy, R., D. G. Doody, and C. J. Watson. 2016. Impact of legacy soil phosphorus on losses in drainage and overland flow from grazed grassland soils. Science of the Total Environment, in press. http://dx.doi.org/10.1016/j.scitotenv.2016.07.063
  • Ceulemans, T., et al. 2014. Soil phosphorus constrains biodiversity across European grasslands. Global Change Biology 20: 3814–3822.
  • Chagnon, P. L., and R. L. Bradley. 2013. Evidence that soil nutrient stoichiometry controls the competitive abilities of arbuscular mycorrhizal vs. root-borne non-mycorrhizal fungi. Fungal Ecology 6:557–560.
  • Chambers, B. J., F. A. Nicholson, E. Cartmell, and C. Rowlands. 2003. Benefits of biosolids to soil quality and fertility. Water and Environment Journal 17:162–167.
  • Compton, J. E., J. A. Harrison, R. L. Dennis, T. L. Greaver, B. H. Hill, S. J. Jordan, H. Walker, and H. V. Campbell. 2011. Ecosystem services altered by human changes in the nitrogen cycle: a new perspective for US decision making. Ecology Letters 14:804–815.
  • Cordell, D., and S. White. 2014. Life's bottleneck: sustaining the world's phosphorus for a food secure future. Annual Review of Environment and Resources 39:161–188.
  • Dodds, W. K., W. W. Bouska, J. L. Eitzmann, T. J. Pilger, K. L. Pitts, A. J. Riley, J. T. Schloesser, and D. J. Thornbrugh. 2008. Eutrophication of US freshwaters: analysis of potential economic damages. Environmental Science & Technology 43:12–19.
  • Doody, D. G., P. J. A. Withers, R. M. Dils, R. W. McDowell, V. Smith, Y. R. McElarney, M. Dunbar, and D. Daly. 2016. Optimizing land use for the delivery of catchment ecosystem services. Frontiers in Ecology and the Environment 14:325–332.
  • Elser, J. J., M. E. Bracken, E. E. Cleland, D. S. Gruner, W. S. Harpole, H. Hillebrand, J. T. Ngai, E. W. Seabloom, J. B. Shurin, and J. E. Smith. 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology Letters 10:1135–1142.
  • Fornara, D. A., E. A. Wasson, P. Christie, and C. J. Watson. 2016. Long-term nutrient fertilization and the carbon balance of permanent grassland: Any evidence for sustainable intensification? Biogeosciences 13:4975–4984.
  • Fraterrigo, J. M., and J. A. Downing. 2008. The influence of land use on lake nutrients varies with watershed transport capacity. Ecosystems 11:1021–1034.
  • French, R. J., and J. E. Schultz. 1984. Water use efficiency of wheat in a Mediterranean-type environment. II. Some limitations to efficiency. Crop and Pasture Science 35:765–775.
  • Galloway, J. N., J. D. Aber, J. W. Erisman, S. P. Seitzinger, R. W. Howarth, E. B. Cowling, and B. J. Cosby. 2003. The nitrogen cascade. BioScience 53:341–356.
  • Garnier, J., et al. 2015. Phosphorus budget in the water-agro-food system at nested scales in two contrasted regions of the world (ASEAN-8 and EU 27). Global Biogeochemical Cycles 29:1348–1368.
  • Grant, C. A., D. N. Flaten, D. J. Tomasiewicz, and S. C. Sheppard. 2001. The importance of early season phosphorus nutrition. Canadian Journal of Plant Science 81:211–214.
  • Grizzetti, B., F. Bouraoui, and A. Aloe. 2012. Changes of nitrogen and phosphorus loads to European seas. Global Change Biology 18:769–782.
  • Haines-Young, R., and R. Potschin. 2010. The links between biodiversity, ecosystem services and human well-being. Pages 110–139 in D. Raffaelli and C. Frid, editors. Ecosystem ecology: a new synthesis. Cambridge University Press, Cambridge, UK.
  • Hao, X. J., T. Q. Zhang, C. S. Tan, T. Welacky, Y. T. Wang, D. Lawrence, and I. P. Hong. 2015. Crop yield and phosphorus uptake as affected by phosphorus-based swine manure application under long-term corn-soybean rotation. Nutrient Cycling in Agroecosystems 103:217–228.
  • Haygarth, P. M., and K. Ritz. 2009. The future of soils and land use in the UK: soil systems for the provision of land-based ecosystem services. Land Use Policy 26: S187–S197.
  • Haygarth, P., L. Condron, A. Heathwaite, B. Turner, and G. Harris. 2005. The phosphorus transfer continuum: linking source to impact with an interdisciplinary and multi-scaled approach. Science of the Total Environment 344:5–14.
  • Heathwaite, L., A. N. Sharpley, and W. Gburek. 2000. A conceptual approach for integrating phosphorus and nitrogen management at watershed scales. Journal of Environmental Quality 29:158–166.
  • International Plant Nutrition Institute (IPNI). 1999. Phosphorus and water use efficiency. Better Crops with Plant Food 83: 24–27.
  • Jacobson, L. M., M. B. David, and L. E. Drinkwater. 2011. A spatial analysis of phosphorus in the Mississippi River basin. Journal of Environmental Quality 40:931–941.
  • Jarvie, H. P., A. N. Sharpley, B. Spears, A. R. Buda, L. May, and P. J. A. Kleinman. 2013a. Water quality remediation faces unprecedented challenges from 'legacy phosphorus'. Environmental Science & Technology 47:8997–8998.
  • Jarvie, H. P., A. N. Sharpley, P. J. A. Withers, J. T. Scott, B. E. Haggard, and C. Neal. 2013b. Phosphorus mitigation to control river eutrophication: murky waters, inconvenient truths and 'post-normal' science. Journal of Environmental Quality 42: 295–304.
  • Jarvie, H. P., A. N. Sharpley, D. Flaten, P. J. A. Kleinman, A. Jenkins, and T. Simmons. 2015. The pivotal role of phosphorus in a resilient water-energy-food security nexus. Journal of Environmental Quality 44:1049–1062.
  • Keeler, B. L., S. Polasky, K. A. Brauman, K. A. Johnson, J. C. Finlay, A. O'Neill, K. Kovacs, and B. Dalzell. 2012. Linking water quality and well-being for improved assessment and valuation of ecosystem services. Proceedings of the National Academy of Sciences of the United States of America 109:18619–18624.
  • Keeler, B. L., S. A. Wood, S. Polasky, C. Kling, C. T. Filstrup, and J. A. Downing. 2015. Recreational demand for clean water: evidence from geotagged photographs by visitors to lakes. Frontiers in Ecology and the Environment 13:76–81.
  • Li, H., et al. 2011a. Integrated soil and plant phosphorus management for crop and environment in China. A review. Plant and Soil 349:157–167.
  • Li, J. T., X. L. Zhang, F. Wang, and Q. G. Zhao. 2011b. Effect of poultry litter and livestock manure on soil physical and biological indicators in a rice-wheat rotation system. Plant Soil Environment 58:351–356.
  • Liu, K., T. Q. Zhang, and C. S. Tan. 2011. Processing tomato phosphorus utilization and post-harvest soil profile phosphorus as affected by phosphorus and potassium additions and drip irrigation. Canadian Journal of Soil Science 91:417–425.
  • MacDonald, G. K., E. M. Bennett, P. A. Potter, and N. Ramankutty. 2011. Agronomic phosphorus imbalances across the world's croplands. Proceedings of the National Academy of Sciences of the United States of America 108:3086–3091.
  • Mace, G. M., K. Norris, and A. H. Fitter. 2012. Biodiversity and ecosystem services: a multilayered relationship. Trends in Ecology & Evolution 27:19–26.
  • Magliocca, N. R., T. K. Rudel, P. H. Verburg, W. J. McConnell, O. Mertz, K. Gerstner, A. Heinimann, and E. C. Ellis. 2015. Synthesis in land change science: methodological patterns, challenges, and guidelines. Regional Environmental Change 15:211–226.
  • McDowell, R. W., and D. Nash. 2012. A review of the cost-effectiveness and suitability of mitigation strategies to prevent phosphorus loss from dairy farms in New Zealand and Australia. Journal of Environmental Quality 41:680–693.
  • McDowell, R. W., A. N. Sharpley, L. M. Condron, P. M. Haygarth, and P. C. Brookes. 2001. Processes controlling soil phosphorus release to runoff and implications for agricultural management. Nutrient Cycling in Agroecosystems 59:269–284.
  • McDowell, R. W., R. M. Dils, A. L. Collins, K. Flahive, and A. N. Sharpley. 2016. A review of the policies and implementation of practices to decrease water quality impairment by phosphorus in New Zealand, the UK, and the US. Nutrient Cycling in Agroecosystems 104:289–305.
  • Meals, D. W., S. A. Dressing, and T. E. Davenport. 2010. Lag time in water quality response to best management practices: a review. Journal of Environmental Quality 39:85–96.
  • Metson, G. S., D. M. Iwaniec, L. A. Baker, E. M. Bennett, D. L. Childers, D. Cordell, N. B. Grimm, J. M. Grove, D. A. Nidzgorski, and S. White. 2015. Urban phosphorus sustainability: systemically incorporating social, ecological, and technological factors into phosphorus flow analysis. Environmental Science & Policy 47:1–11.
  • Metson, G. S., G. K. MacDonald, D. Haberman, T. Nesme, and E. M. Bennett. 2016. Feeding the corn belt: opportunities for phosphorus recycling in US agriculture. Science of the Total Environment 542:1117–1126.
  • Michalak, A. M. 2016. Study role of climate change in extreme threats to water quality. Nature 535:349–350.
  • Millennium Ecosystem Assessment (MA). 2005. Ecosystems and human well-being: synthesis. Island Press, Washington, D.C., USA.
  • Monteith, J. L. 1986. How do crops manipulate water supply and demand? Philosophical Transactions of the Royal Society of London A316:245–259.
  • Moomaw, W. R., and M. B. Birch. 2005. Cascading costs: an economic nitrogen cycle. Science in China Series C: Life Sciences 48:678–696.
  • Mueller, N. D., J. S. Gerber, M. Johnston, D. K. Ray, N. Ramankutty, and J. A. Foley. 2012. Closing yield gaps through nutrient and water management. Nature 490:254–257.
  • Naiman, R. J., and H. Decamps. 1997. The ecology of interfaces: riparian zones. Annual Review of Ecology and Systematics 28:621–658.
  • Nesme, T., and P. J. A. Withers. 2016. Sustainable strategies towards a phosphorus circular economy. Nutrient Cycling in Agroecosystems 104:259–264.
  • Nesme, T., K. Senthilkumar, A. Mollier, and S. Pellerin. 2015. Effects of crop and livestock segregation on phosphorus resource use: a systematic, regional analysis. European Journal of Agronomy 71:88–95.
  • Nziguheba, G., S. Zingore, J. Kihara, R. Merckx, S. Njoroge, A. Otinga, E. Vandamme, and B. Vanlauwe. 2016. Phosphorus in smallholder farming systems of sub-Saharan Africa: implications for agricultural intensification. Nutrient Cycling in Agroecosystems 104:321–340.
  • Ockenden, M. C., et al. 2016. Changing climate and nutrient transfers: evidence from high temporal resolution concentration-flow dynamics in headwater catchments. Science of the Total Environment 548:325–339.
  • Odum, E. P., J. T. Finn, and E. H. Franz. 1979. Perturbation theory and the subsidy-stress gradient. BioScience 29:349–352.
  • Orgiazzi, A., et al. 2016. Global soil biodiversity atlas. European Commission, Publications Office of the European Union, Luxembourg City, Luxembourg.
  • Osmond, D., et al. 2012. Comparing phosphorus indices from twelve southern US states against monitored phosphorus loads from six prior southern studies. Journal of Environmental Quality 41:1741–1749.
  • Pimentel, D., P. Hepperly, J. Hanson, D. Douds, and R. Seidel. 2005. Environmental, energetic, and economic comparisons of organic and conventional farming systems. BioScience 55: 573–582.
  • Powers, S. M., et al. 2016. Long-term accumulation and transport of anthropogenic phosphorus in three river basins. Nature Geoscience 9:353–356.
  • Rowe, H., et al. 2016. Integrating legacy soil phosphorus into sustainable nutrient management strategies for future food, bioenergy and water security. Nutrient Cycling in Agroecosystems 104:393–412.
  • Schipanski, M. E., and E. M. Bennett. 2012. The influence of agricultural trade and livestock production on the global phosphorus cycle. Ecosystems 15:256–268.
  • Shackleton, C. M., S. Ruwanza, G. S. Sanni, S. Bennett, P. De Lacy, R. Modipa, N. Mtati, M. Sachikonye, and G. Thondhlana. 2016. Unpacking Pandora's box: understanding and categorising ecosystem disservices for environmental management and human wellbeing. Ecosystems 19:587–600.
  • Sharpley, A., D. Beegle, C. Bolster, L. Good, B. Joern, Q. Ketterings, J. Lory, R. Mikkelsen, D. Osmond, and P. Vadas. 2012. Phosphorus indices: Why we need to take stock of how we are doing. Journal of Environmental Quality 41:1711–1719.
  • Sharpley, A., H. P. Jarvie, A. Buda, L. May, B. Spears, and P. J. Kleinman. 2013. Phosphorus legacy: overcoming the effects of past management practices to mitigate future water quality impairment. Journal of Environmental Quality 42:1308–1326.
  • Shen, J., C. Li, G. Mi, L. Li, L. Yuan, R. Jiang, and F. Zhang. 2013. Maximizing root/rhizosphere efficiency to improve crop productivity and nutrient use efficiency in intensive agriculture of China. Journal of Experimental Botany 64: 1181–1192.
  • Shepherd, J. G., R. Kleemann, J. Bahri-Esfahani, L. Hudek, L. Suriyagoda, E. Vandamme, and K. C. van Dijk. 2016. The future of phosphorus in our hands. Nutrient Cycling in Agroecosystems 104:281–287.
  • Smith, V. H., and D. W. Schindler. 2009. Eutrophication science: Where do we go from here? Trends in Ecology & Evolution 24:201–207.
  • Smith, D. R., K. W. King, L. Johnson, W. Francesconi, P. Richards, D. Baker, and A. N. Sharpley. 2015a. Surface runoff and tile drainage transport of phosphorus in the Midwestern United States. Journal of Environmental Quality 44: 495–502.
  • Smith, P., et al. 2015b. Biogeochemical cycles and biodiversity as key drivers of ecosystem services provided by soils. Soil Discussions 2:537–586.
  • Sobota, D. J., J. E. Compton, M. L. McCrackin, and S. Singh. 2015. Cost of reactive nitrogen release from human activities to the environment in the United States. Environmental Research Letters 10:025006.
  • Stockner, J. G., E. Rydin, and P. Hyenstrand. 2000. Cultural oligotrophication: causes and consequences for fisheries resources. Fisheries 25:7–14.
  • Syers, J. K., A. E. Johnston, and D. Curtin. 2008. Efficiency of soil and fertilizer phosphorus use. FAO Fertilizer and Plant Nutrition Bulletin, Food and Agriculture Organization of the United Nations (FAO), Rome, Italy.
  • Taranu, Z. E., et al. 2015. Acceleration of cyanobacterial dominance in north temperate-subarctic lakes during the Anthropocene. Ecology Letters 18:375–384.
  • Teste, F. P., E. Laliberté, H. Lambers, Y. Auer, S. Kramer, and E. Kandeler. 2016. Mycorrhizal fungal biomass and scavenging declines in phosphorus-impoverished soils during ecosystem retrogression. Soil Biology and Biochemistry 92: 119–132.
  • Vörösmarty, C. J., et al. 2010. Global threats to human water security and river biodiversity. Nature 467:555–561.
  • Wilson, M. A., and S. R. Carpenter. 1999. Economic valuation of freshwater ecosystem services in the United States: 1971–1997. Ecological Applications 9:772–783.
  • Withers, P. J. A., and H. P. Jarvie. 2008. Delivery and cycling of phosphorus in rivers: a review. Science of the Total Environment 400:379–395.
  • Withers, P. J. A., K. C. van Dijk, T. S. S. Neset, T. Nesme, O. Oenema, G. H. Rubæk, O. F. Schoumans, B. Smit, and S. Pellerin. 2015. Stewardship to tackle global phosphorus inefficiency: the case of Europe. Ambio 44:193–206.
  • Zhang, T. Q., C. S. Tan, Z. M. Zheng, T. W. Welacky, and W. D. Reynolds. 2015. Impacts of soil conditioners and water management on phosphorus loss in tile drainage from a clay loam soil. Journal of Environmental Quality 44:572–584.
  • Zhang, D. S., C. C. Zhang, X. Y. Tang, H. G. Li, F. S. Zhang, Z. Rengel, W. R. Whalley, W. J. Davies, and J. B. Shen. 2016. Increased soil P availability induced by faba bean root exudation stimulates root growth and P uptake in neighbouring maize. New Phytologist 209:823–831.