Skip to main content

Thank you for visiting 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.

Sustainable intensification of high-diversity biomass production for optimal biofuel benefits


The potential benefits of biofuels depend on the environmental impacts of biomass production. High-diversity mixtures of grassland species grown on abandoned agricultural lands have been proposed as enhancing climate mitigation potential, but can have low yields. Intensification might increase productivity, but might also cause negative environmental impacts. Here, we show that, compared with more intensive treatments, moderate intensification of high-diversity grasslands had as great or greater biomass yields, soil carbon stores and root mass, and had negligible effects on grassland stability, diversity and nitrate leaching. In particular, compared with untreated plots, the moderate treatment of irrigation and addition of 70 kgN ha−1 yr−1 resulted in 89% more yield, 61% more root carbon, 187% more soil carbon storage and, if biomass were used for bioenergy, twice the greenhouse gas reductions. Irrigation and 140 kgN ha−1 yr−1 had 32% lower greenhouse gas benefits, 10 times greater nitrate leaching and 121% greater loss of plant diversity than the moderate treatment. These results suggest that optimizing multiple environmental benefits requires sustainable intensification practices appropriate for the soils, climate and plant species of a region.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Fig. 1: Aboveground biomass and root production.
Fig. 2: Soil carbon stores in the upper 20 cm of soil from 2010 to 2017.
Fig. 3: Annual life-cycle GHG impacts (as CO2 equivalents).
Fig. 4: Effect of nitrogen addition and irrigation on species richness, temporal stability of the yield and nitrate leaching.

Data availability

The data used in this study—experiment e248 of the Cedar Creek Long-Term Ecological Research programme—are available at For data collected before the start of the irrigation and nitrogen fertilization treatments in the 32-species treatment plots, see pre-2002 data for the experiment e120.


  1. 1.

    Tilman, D., Hill, J. & Lehman, C. Carbon-negative biofuels from low-input high-diversity grassland biomass. Science 314, 1598–1600 (2006).

    CAS  Article  Google Scholar 

  2. 2.

    Robertson, G. P. et al. Cellulosic biofuel contributions to a sustainable energy future: choices and outcomes. Science 356, eaal2324 (2017).

    Article  Google Scholar 

  3. 3.

    Searchinger, T. et al. Use of US croplands for biofuels increases greenhouse gases through emissions from land-use change. Science 319, 1238–1240 (2008).

    CAS  Article  Google Scholar 

  4. 4.

    Fargione, J., Hill, J., Tilman, D., Polasky, S. & Hawthorne, P. Land clearing and the biofuel carbon debt. Science 319, 1235–1238 (2008).

    CAS  Article  Google Scholar 

  5. 5.

    Klopf, R. P., Baer, S. G., Bach, E. M. & Six, J. Restoration and management for plant diversity enhances the rate of belowground ecosystem recovery. Ecol. Appl. 27, 355–362 (2017).

    Article  Google Scholar 

  6. 6.

    Fargione, J. E. et al. Bioenergy and wildlife: threats and opportunities for grassland conservation. Bioscience 59, 767–777 (2009).

    Article  Google Scholar 

  7. 7.

    Gelfand, I. et al. Sustainable bioenergy production from marginal lands in the US Midwest. Nature 493, 514–517 (2013).

    CAS  Article  Google Scholar 

  8. 8.

    Sprunger, C. D. & Robertson, P. G. Early accumulation of active fraction soil carbon in newly established cellulosic biofuel systems. Geoderma 318, 42–51 (2018).

    CAS  Article  Google Scholar 

  9. 9.

    Dijkstra, F. A., West, J. B., Hobbie, S. E., Reich, P. B. & Trost, J. Plant diversity, CO2, and N influence inorganic and organic N leaching in grasslands. Ecology 88, 490–500 (2007).

    Article  Google Scholar 

  10. 10.

    Tilman, D., Reich, P. B. & Knops, J. M. H. Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441, 629–632 (2006).

    CAS  Article  Google Scholar 

  11. 11.

    Mitchell, C. E., Tilman, D. & Groth, J. V. Effects of grassland plant species diversity, abundance, and composition on foliar fungal disease. Ecology 83, 1713–1726 (2002).

    Article  Google Scholar 

  12. 12.

    Kennedy, T. A. et al. Biodiversity as a barrier to ecological invasion. Nature 417, 636–638 (2002).

    CAS  Article  Google Scholar 

  13. 13.

    Campbell, J. E., Lobell, D. B., Genova, R. C. & Field, C. B. The global potential of bioenergy on abandoned agriculture lands. Environ. Sci. Technol. 42, 5791–5794 (2008).

    CAS  Article  Google Scholar 

  14. 14.

    Jungers, J. M. et al. Long-term biomass yield and species composition in native perennial bioenergy cropping systems. Agron. J. 107, 1627–1640 (2015).

    CAS  Article  Google Scholar 

  15. 15.

    Carlsson, G., Mårtensson, L.-M., Prade, T., Svensson, S.-E. & Jensen, E. S. Perennial species mixtures for multifunctional production of biomass on marginal land. GCB Bioenergy 9, 191–201 (2017).

    CAS  Article  Google Scholar 

  16. 16.

    Vermeulen, S. J., Campbell, B. M. & Ingram, J. S. Climate change and food systems. Annu. Rev. Environ. Resour. 37, 195–222 (2012).

    Article  Google Scholar 

  17. 17.

    Oates, L. G. et al. Nitrous oxide emissions during establishment of eight alternative cellulosic bioenergy cropping systems in the North Central United States. GCB Bioenergy 8, 539–549 (2016).

    CAS  Article  Google Scholar 

  18. 18.

    Wang, M. The Greenhouse Gases, Regulated Emissions, and Energy Use in Transportation (GREET) Model: Version 1.5 Technical Report (Center for Transportation Research, Argonne National Laboratory, 2008).

  19. 19.

    Tilman, D., Cassman, K. G., Matson, P. A., Naylor, R. & Polasky, S. Agricultural sustainability and intensive production practices. Nature 418, 671–677 (2002).

    CAS  Article  Google Scholar 

  20. 20.

    Garnett, T. et al. Sustainable intensification in agriculture: premises and policies. Science 341, 33–34 (2013).

    CAS  Article  Google Scholar 

  21. 21.

    Di, H. J. & Cameron, K. C. Nitrate leaching in temperate agroecosystems: sources, factors and mitigating strategies. Nutr. Cycl. Agroecosyst. 64, 237–256 (2002).

    CAS  Article  Google Scholar 

  22. 22.

    Spalding, R. F. & Exner, M. E. Occurrence of nitrate in groundwater—a review. J. Environ. Qual. 22, 392–402 (1993).

    CAS  Article  Google Scholar 

  23. 23.

    Bingham, M. A. & Biondini, M. Nitrate leaching as a function of plant community richness and composition, and the scaling of soil nutrients, in a restored temperate grassland. Plant Ecol. 212, 413–422 (2011).

    Article  Google Scholar 

  24. 24.

    Loiseau, P., Carrere, P., Lafarge, M., Delpy, R. & Dublanchet, J. Effect of soil-N and urine-N on nitrate leaching under pure grass, pure clover and mixed grass/clover swards. Eur. J. Agron. 14, 113–121 (2001).

    CAS  Article  Google Scholar 

  25. 25.

    Leimer, S. et al. Mechanisms behind plant diversity effects on inorganic and organic N leaching from temperate grassland. Biogeochemistry 131, 339–353 (2016).

    CAS  Article  Google Scholar 

  26. 26.

    Simkin, S. M. et al. Conditional vulnerability of plant diversity to atmospheric nitrogen deposition across the United States. Proc. Natl Acad. Sci. USA 113, 4086–4091 (2016).

    CAS  Article  Google Scholar 

  27. 27.

    Clark, C. M. & Tilman, D. Loss of plant species after chronic low-level nitrogen deposition to prairie grasslands. Nature 451, 712–715 (2008).

    CAS  Article  Google Scholar 

  28. 28.

    Isbell, F. et al. Nutrient enrichment, biodiversity loss, and consequent declines in ecosystem productivity. Proc. Natl Acad. Sci. USA 110, 11911–11916 (2013).

    CAS  Article  Google Scholar 

  29. 29.

    Binder, S., Isbell, F., Polasky, S., Catford, J. A. & Tilman, D. Grassland biodiversity can pay. Proc. Natl Acad. Sci. USA 115, 3876–3881 (2018).

    CAS  Article  Google Scholar 

  30. 30.

    Hautier, Y. et al. Eutrophication weakens stabilizing effects of diversity in natural grasslands. Nature 508, 521–525 (2014).

    CAS  Article  Google Scholar 

  31. 31.

    Inouye, R. S. et al. Old-field succession on a Minnesota sand plain. Ecology 68, 12–26 (1987).

    Article  Google Scholar 

  32. 32.

    Koponen, K., Soimakallio, S., Kline, K. L., Cowie, A. & Brandão, M. Quantifying the climate effects of bioenergy—choice of reference system. Renew. Sustain. Energy Rev. 81, 2271–2280 (2018).

    Article  Google Scholar 

  33. 33.

    Schlesinger, W. H. Are wood pellets a green fuel? Science 359, 1328–1329 (2018).

    CAS  Article  Google Scholar 

  34. 34.

    Knops, J. M. H. & Bradley, K. L. Soil carbon and nitrogen accumulation and vertical distribution across a 74-year chronosequence. Soil Sci. Soc. Am. J. 73, 2096–2104 (2009).

    CAS  Article  Google Scholar 

  35. 35.

    Gibbs, H. K. & Salmon, J. M. Mapping the world's degraded lands. Appl. Geogr. 57, 12–21 (2015).

    Article  Google Scholar 

  36. 36.

    Jarchow, M. E. et al. Trade-offs among agronomic, energetic, and environmental performance characteristics of corn and prairie bioenergy cropping systems. GCB Bioenergy 7, 57–71 (2015).

    Article  Google Scholar 

  37. 37.

    Anderson, E. K. et al. Impacts of management practices on bioenergy feedstock yield and economic feasibility on Conservation Reserve Program grasslands. GCB Bioenergy 8, 1178–1190 (2016).

    CAS  Article  Google Scholar 

  38. 38.

    Jungers, J. M., Sheaffer, C. C., Fargione, J. & Lehman, C. Short-term harvesting of biomass from conservation grasslands maintains plant diversity. GCB Bioenergy 7, 1050–1061 (2015).

    Article  Google Scholar 

  39. 39.

    Azar, C. et al. The feasibility of low CO2 concentration targets and the role of bio-energy with carbon capture and storage (BECCS). Clim. Change 100, 195–202 (2010).

    CAS  Article  Google Scholar 

  40. 40.

    Righelato, R. & Spracklen, D. V. Carbon mitigation by biofuels or by saving and restoring forests? Science 317, 902 (2007).

    CAS  Article  Google Scholar 

  41. 41.

    Reynolds, L. K., McGlathery, K. J. & Waycott, M. Genetic diversity enhances restoration success by augmenting ecosystem services. PLoS ONE 7, e38397 (2012).

    CAS  Article  Google Scholar 

  42. 42.

    Blumenthal, D. M., Jordan, N. R. & Svenson, E. L. Weed control as a rationale for restoration: the example of tallgrass prairie. Conserv. Ecol. 7, 6 (2003).

    Article  Google Scholar 

  43. 43.

    Yang, Y. Two sides of the same coin: consequential life cycle assessment based on the attributional framework. J. Clean. Prod. 127, 274–281 (2016).

    Article  Google Scholar 

  44. 44.

    Rajagopal, D., Hochman, G. & Zilberman, D. Indirect fuel use change (IFUC) and the lifecycle environmental impact of biofuel policies. Energy Policy 39, 228–233 (2011).

    Article  Google Scholar 

  45. 45.

    Trost, J. J., Kiesling, R. L., Erickson, M. L., Rose, P. J. & Elliott, S. M. Land-Cover Effects on the Fate and Transport of Surface-Applied Antibiotics and 17-Beta-Estradiol on a Sandy Outwash Plain, Anoka County, Minnesota, 2008–09 (US Geological Survey, 2013).

  46. 46.

    Ruan, L., Bhardwaj, A. K., Hamilton, S. K. & Robertson, G. P. Nitrogen fertilization challenges the climate benefit of cellulosic biofuels. Environ. Res. Lett. 11, 064007 (2016).

    Article  Google Scholar 

  47. 47.

    Vora, N., Shah, A., Bilec, M. M. & Khanna, V. Food–energy–water nexus: quantifying embodied energy and GHG emissions from irrigation through virtual water transfers in food trade. ACS Sustain. Chem. Eng. 5, 2119–2128 (2017).

    CAS  Article  Google Scholar 

  48. 48.

    Murphy, C. W. & Kendall, A. Life cycle analysis of biochemical cellulosic ethanol under multiple scenarios. GCB Bioenergy 7, 1019–1033 (2015).

    CAS  Article  Google Scholar 

Download references


We thank the Global Climate and Energy Project and NSF Long-Term Ecological Research programme (DEB-0620652 and DEB-1234162) for funding this research, T. Mielke for coordinating data collection, and D. Bahauddin for data management.

Author information




Y.Y. led the data analysis and writing efforts. D.T. established the experiment, contributed to data analysis and writing, and obtained NSF funding. C.L. obtained Global Climate and Energy Project funding and contributed to the writing. J.J.T. planned and performed nitrate leaching analyses and contributed to the writing.

Corresponding author

Correspondence to David Tilman.

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.

Supplementary information

Supplementary Information

Supplementary Tables 1–14, Supplementary References 1–14

Supplementary Dataset

Data for the 4 figures presented in the main text, Detailed data for the life cycle greenhouse gas (GHG) analysis, Estimates of state-level irrigation GHG emissions

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yang, Y., Tilman, D., Lehman, C. et al. Sustainable intensification of high-diversity biomass production for optimal biofuel benefits. Nat Sustain 1, 686–692 (2018).

Download citation

Further reading


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

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