Plant and Soil

, Volume 345, Issue 1–2, pp 195–210 | Cite as

Influence of biochar on drought tolerance of Chenopodium quinoa Willd and on soil–plant relations

  • Claudia Irene KammannEmail author
  • Sebastian Linsel
  • Johannes W. Gößling
  • Hans-Werner Koyro
Regular Article


The application of pyrogenic carbon, biochar, to agricultural soils is currently discussed as a win-win strategy to sequester carbon in soil, thus improving soil fertility and mitigate global warming. Our aim was to investigate if biochar may improve plant eco-physiological responses under sufficient water supply as well as moderate drought stress. A fully randomized greenhouse study was conducted with the pseudo-cereal Chenopodium quinoa Willd, using three levels of biochar addition (0, 100 and 200 t ha−1) to a sandy soil and two water treatments (60% and 20% of the water holding capacity of the control), investigating growth, water use efficiency, eco-physiological parameters and greenhouse gas (GHG) fluxes. Biochar application increased growth, drought tolerance and leaf-N- and water-use efficiency of quinoa despite larger plant–leaf areas. The plants growing in biochar-amended soil accumulated exactly the same amount of nitrogen in their larger leaf biomass than the control plants, causing significantly decreased leaf N-, proline- and chlorophyll-concentrations. In this regard, plant responses to biochar closely resembled those to elevated CO2. However, neither soil- nor plant–soil-respiration was higher in the larger plants, indicating less respiratory C losses per unit of biomass produced. Soil-N2O emissions were significantly reduced with biochar. The large application rate of 200 t ha−1 biochar did not improve plant growth compared to 100 t ha−1; hence an upper beneficial level exists. For quinoa grown in a sandy soil, biochar application might hence provide a win-win strategy for increased crop production, GHG emission mitigation and soil C sequestration.


CO2 gas exchange Halophyte crop Biochar Water use efficiency Nitrogen use efficiency N2O emission Quinoa 





Water use efficiency


Nitrogen use efficiency


Water holding capacity


Soil organic carbon



The authors want to thank Christoph Forreiter for critical reading of the manuscript and Judy Libra for proof reading. The authors acknowledge the technical assistance of Nicol Strasilla and Gerlinde Lehr with proline and RuBisCO extractions and greenhouse gas analyses and Gerhard Mayer for his assistance at the ion-chromatograph. Thanks to Johanna Kreiling for technical assistance, and to the Department of Applied Microbiology, in particular to Stefan Ratering, for help with the GC analyses.


  1. Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ 30:258–270. doi: 10.1111/j.1365-3040.2007.01641.x PubMedCrossRefGoogle Scholar
  2. Amonette JE, Joseph S (2009) Characteristics of biochar: microchemical properties. In: Lehmann J, Joseph S (eds) Biochar for environmental management—science and technology. Earthscan, London, pp 33–52Google Scholar
  3. Barker DJ, Sullivan CY, Moser LE (1993) Water deficit effects on osmotic potential, cell wall elasticity, and proline in five forage grasses. Agron J 85:270–275CrossRefGoogle Scholar
  4. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207CrossRefGoogle Scholar
  5. Blackwell P, Riethmuller G, Collins M (2009) Biochar application to soil. In: Lehmann J, Joseph S (eds) Biochar for environmental management: science and technology. Earthscan, London, pp 207–226Google Scholar
  6. Chan KY, Van Zwieten L, Meszaros I, Downie A, Joseph S (2007) Agronomic values of greenwaste biochar as a soil amendment. Aust J Soil Res 45:629–634. doi: 10.1071/SR07109 CrossRefGoogle Scholar
  7. Chan KY, Van Zwieten L, Meszaros I, Downie A, Joseph S (2008) Using poultry litter biochars as soil amendments. Aust J Soil Res 46:437–444. doi: 10.1071/SR08036 CrossRefGoogle Scholar
  8. Chan KY, Xu Z (2009) Biochar: nutrient properties and their enhancement. In: Lehmann J, Joseph S (eds) Biochar for environmental management: science and technology. Earthscan, London, pp 67–84Google Scholar
  9. Cheng C-H, Lehmann J, Thies JE, Burton AJ, Engelhard M (2006) Oxidation of black carbon by biotic and abiotic processes. Org Geochem 37:1477–1488CrossRefGoogle Scholar
  10. Cheng C-H, Lehmann J, Thies JE, Burton SD (2008) Stability of black carbon in soils across a climatic gradient. J Geophys Res 113: doi: 10.1029/2007JG000642
  11. Clough TJ, Condron LM (2010) Biochar and the nitrogen cycle: Introduction. J Environ Qual 39:1218–1223.Google Scholar
  12. Cotrufo MF, Ineson P, Scott A (1998) Elevated CO2 reduces the nitrogen concentration of plant tissues. Global Change Biol 4:43–54CrossRefGoogle Scholar
  13. Downie A, Crosky A, Munroe P (2009) Physical properties of biochar. In: Lehmann J, Joseph S (eds) Biochar for environmental management—science and technology. Earthscan, London, pp 13–32Google Scholar
  14. Elad Y, David DR, Harel YM, Borenshtein M, Kalifa HB, Silber A, Graber ER (2010) Induction of systemic resistance in plants by biochar, a soil-applied carbon sequestering agent. Phytopathology 100:913–921PubMedCrossRefGoogle Scholar
  15. Galwey NW (1989) Quinoa. Biologist 36:5Google Scholar
  16. Gaskin JW, Speir RA, Harris K, Das KC, Lee RD, Morris LA, Fisher DS (2010) Effect of peanut hull and pine chip biochar on soil nutrients, corn nutrient status, and yield. Agron J 102:623–633CrossRefGoogle Scholar
  17. Gaunt JL, Lehmann J (2008) Energy balance and emissions associated with biochar sequestration and pyrolysis bioenergy production. Environ Sci Technol 42:4152–4158PubMedCrossRefGoogle Scholar
  18. Glaser B (2007) Prehistorically modified soils of central Amazonia: a model for sustainable agriculture in the twenty-first century. Phil Trans R Soc London B 362:187–196CrossRefGoogle Scholar
  19. Glaser B, Haumaier L, Guggenberger G, Zech W (2001) The ‘Terra Preta’ phenomenon: a model for sustainable agriculture in the humid tropics. Naturwissenschaften 88:37–41PubMedCrossRefGoogle Scholar
  20. Glaser B, Lehmann J, Zech W (2002) Ameliorating physical and chemical properties of highly weathered soils in the tropics with charcoal—a review. Biol Fertil Soils 35:219–230CrossRefGoogle Scholar
  21. Golluscio RA (2007) On the link between nitrogen productivity and residence time: two opposite nitrogen use strategies? J Arid Environ 68:165–169CrossRefGoogle Scholar
  22. Gonzalez JA, Gallardo M, Hila LM, Rosa M, Prado FE (2009) Physiological responses of quinoa (Chenopodium quinoa Willd.) to drought and waterlogging stresses: dry matter partitioning. Bot Stud 50:35–42Google Scholar
  23. Graber ER, Harel YM, Kolton M, Cytryn E, Silber A, David DR, Tsechansky L, Borenshtein M, Elad Y (2010) Biochar impact on development and productivity of pepper and tomato grown in fertigated soilless media. Plant and Soil 337:481–496CrossRefGoogle Scholar
  24. Granier F (1988) Extraction of plant proteins for two-dimensional electrophoresis. Electrophoresis 9:112–718CrossRefGoogle Scholar
  25. Granli T, Bøckmann OC (1994) Nitrous oxide from agriculture. Norweg J Agr Sci Supp 12:1–128Google Scholar
  26. Groffman PM, Tiedje JM (1991) Relationships between denitrification, CO2 production and air-filled porosity in soils of different texture and drainage. Soil Biol Biochem 23(3):299–302CrossRefGoogle Scholar
  27. Hansen J, Sato M, Kharecha P, Beerling D, Berner R, Masson-Delmotte V, Pagani M, Raymo M, Royer DL, Zachos JC (2008) Target atmospheric CO2: where should humanity aim? Open Atm Sci J 2:217–231CrossRefGoogle Scholar
  28. Hutchinson GL, Mosier AR (1981) Improved soil cover method for field measurement of nitrous oxide fluxes. Soil Sci Soc Am J 45:311–316CrossRefGoogle Scholar
  29. Ibarra-Caballero J, Villanueva-Verduz C, Molina-Galan J, Sanchez-de-Jimenez E (1988) Proline accumulation as a symptom of drought stress in maize: a tissue differentiation requirement. J Exp Bot 39:889–897CrossRefGoogle Scholar
  30. IPCC (2007a) Climate change 2007: Climate change impacts, adaptation and vulnerability. Working Group II Contribution to the Intergovernmental Panel on Climate Change Fourth Assessment Report—Summary for Policymakers. IPCC, BernGoogle Scholar
  31. IPCC (2007b) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
  32. Ishida H, Nishimori Y, Sugisawa M, Makino A, Mae T (1997) The large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase is fragmented. Plant Cell Physiol 38:471–479PubMedGoogle Scholar
  33. Jacobsen S-E, Stølen O (1993) Quinoa—morphology and phenology and prospects for its production as a new crop in Europe. Eur J Agron 2:19–29Google Scholar
  34. Jensen CR, Jacobsen S-E, Andersen MN, Núñez N, Andersen SD, Rasmussen L, Mogensen VO (2000) Leaf gas exchange and water relation characteristics of field quinoa (Chenopodium quinoa Willd.) during soil drying. Eur J Agron 13:11–25CrossRefGoogle Scholar
  35. Kim J-S, Sparovek G, Longo RM, De Melo WJ, Crowley D (2007) Bacterial diversity of terra preta and pristine forest soil from the Western Amazon. Soil Biol Biochem 39:684–690CrossRefGoogle Scholar
  36. Kimetu JM, Lehmann J, Kinyangi JM, Cheng CH, Thies J, Mugendi DN, Pell A (2009) Soil organic C stabilization and thresholds in C saturation. Soil Biol Biochem 41:2100–2104CrossRefGoogle Scholar
  37. Kolb SE, Fermanich KJ, Dornbush ME (2009) Effect of charcoal quantity on microbial biomass and activity in temperate soils. Soil Sci Soc Am J 73:1173–1181. doi: 10.2136/sssaj2008.0232 CrossRefGoogle Scholar
  38. Kuzyakov Y, Subbotina I, Chen H, Bogomolova I, Xu X (2009) Black carbon decomposition and incorporation into soil microbial biomass estimated by 14C labeling. Soil Biol Biochem 41:210–219. doi: 10.1016/j.soilbio.2008.10.016 CrossRefGoogle Scholar
  39. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 27:680–685CrossRefGoogle Scholar
  40. Laird DA, Brown RC, Amonette JE, Lehmann J (2009) Review of the pyrolysis platform for coproducing bio-oil and biochar. Biofuels Bioprod Biorefin 3:547–562CrossRefGoogle Scholar
  41. Lal R (2004) Soil carbon sequestration impacts on global climate change and food security. Science 304:1623–1627. doi: 10.1126/science.1097396 PubMedCrossRefGoogle Scholar
  42. Lal R (2009) Challenges and opportunities in soil organic matter research. Eur J Soil Sci 60:158–169CrossRefGoogle Scholar
  43. Lehmann J (2006) Bio-char sequestration in terrestrial ecosystems—a review. Mitigat Adaptat Strat Glob Chan 11:403–427. doi: 10.1007/s11027-005-9006-5 Google Scholar
  44. Lehmann J (2007a) Bio-energy in the black. Front Ecol Environ 5:381–387CrossRefGoogle Scholar
  45. Lehmann J (2007b) A handful of carbon. Nature 447:143–144PubMedCrossRefGoogle Scholar
  46. Lehmann J, Czimczik C, Laird D, Sohi S (2009) Stability of biochar in soil. In: Lehmann J, Joseph S (eds) Biochar for environmental management—science and technology. Earthscan, London, pp 183–205Google Scholar
  47. Liang B, Lehmann J, Sohi SP, Thies JE, O'Neill B, Trujillo L, Gaunt J, Solomon D, Grossman J, Neves EG, Luizão FJ (2010) Black carbon affects the cycling of non-black carbon in soil. Org Geochem. doi: 10.1016/j.orggeochem.2009.09.007 Google Scholar
  48. Liang B, Lehmann J, Solomon D, Kinyangi J, Grossman J, O'Neill B, Skjemstad JO, Thies J, Luizao FJ, Petersen J, Neves EG (2006) Black carbon increases cation exchange capacity in soils. Soil Sci Soc Am J 70:1719–1730. doi: 10.2136/sssaj2005.0383 CrossRefGoogle Scholar
  49. Loftfield N, Flessa H, Augustin J, Beese F (1997) Automated gas chromatographic system for rapid analysis of the atmospheric trace gases methane, carbon dioxide, and nitrous oxide. J Environ Qual 26:560–564CrossRefGoogle Scholar
  50. Long SP, Zhu X-G, Naidu SL, Ort DR (2006) Can improvement in photosynthesis increase crop yields? Plant Cell Environ 29:315–330PubMedCrossRefGoogle Scholar
  51. Major J, Lehmann J, Rondon M, Goodale C (2010) Fate of soil-applied black carbon: downward migration, leaching and soil respiration. Global Change Biol 16:1366–1379. doi: 10.1111/j.1365-2486.2009.02044.x CrossRefGoogle Scholar
  52. Marris E (2006) Putting the carbon back: black is the new green. Nature 442:624–626PubMedCrossRefGoogle Scholar
  53. Mathews JA (2008) How carbon credits could drive the emergence of renewable energies. Energ Pol 36:3633–3639CrossRefGoogle Scholar
  54. McHenry MP (2009) Agricultural bio-char production, renewable energy generation and farm carbon sequestration in Western Australia: certainty, uncertainty and risk. Agric Ecosys Environ 129:1–7CrossRefGoogle Scholar
  55. Morgan JA, Pataki DE, Körner C, Clark H, Del Grosso SJ, Grünzweig JM, Knapp AK, Mosier AR, Newton PCD, Niklaus PA, Nippert JB, Nowak RS, Parton WJ, Polley HW, Shaw MR (2004) Water relations in grassland and desert ecosystems exposed to elevated atmospheric CO2. Oecologia 140:11–25PubMedCrossRefGoogle Scholar
  56. Mosier AR, Mack L (1980) Gas chromatographic system for precise, rapid analysis of nitrous oxide. Soil Sci Soc Am J 44:1121–1123CrossRefGoogle Scholar
  57. Nösberger J, Long SP, Norby RJ, Stitt M, Hendrey G, Blum H (2006) Managed ecosystems and CO2: case studies, processes, and perspectives, vol 187. Ecological studies. Springer, Berlin, pp 457Google Scholar
  58. Novak JM, Busscher WJ, Watts DW, Laird DA, Ahmedna MA, Niandou MAS (2010) Short-term CO2 mineralization after additions of biochar and switchgrass to a Typic Kandiudult. Geoderma 154:281–288CrossRefGoogle Scholar
  59. Nowak RS, Ellsworth DS, Smith SD (2004) Functional responses of plants to elevated atmospheric CO2—do photosynthetic and productivity data from FACE experiments support early predictions? New Phytol 162:253–280CrossRefGoogle Scholar
  60. Owensby CE, Ham JM, Knapp AK, Auen LM (1999) Biomass production and species composition change in a tallgrass prairie ecosystem after long-term exposure to elevated atmospheric CO2. Global Change Biol 5:497–506CrossRefGoogle Scholar
  61. Reich PB, Tjoelker MG, Machado J-L, Oleksyn J (2006) Universal scaling of respiratory metabolism, size and nitrogen in plants. Nature 439:457–461PubMedCrossRefGoogle Scholar
  62. Rondon M, Lehmann J, Ramírez J, Hurtado M (2007) Biological nitrogen fixation by common beans (Phaseolus vulgaris L.) increases with bio-char additions. Biol Fertil Soils 43:699–708CrossRefGoogle Scholar
  63. Schulte PJ, Brooks JR (2003) Branch junctions and the flow of water through xylem in Douglas-fir and ponderosa pine stems. J Exp Bot 54:1597–1605. doi: 10.1093/jxb/erg169 PubMedCrossRefGoogle Scholar
  64. Smith MS, Tiedje JM (1979) The effect of roots on soil denitrification. Soil Sci Soc Am J 43:951–955. doi: 10.2136/sssaj1979.03615995004300050027x CrossRefGoogle Scholar
  65. Sperry JS, Hacke UG (2002) Desert shrub water relations with respect to soil characteristics and plant functional type. Funct Ecol 16:367–378CrossRefGoogle Scholar
  66. Spokas KA, Koskinen WC, Baker JM, Reicosky DC (2009) Impacts of woodchip biochar additions on greenhouse gas production and sorption/degradation of two herbicides in a Minnesota soil. Chemosphere 77:574–581PubMedCrossRefGoogle Scholar
  67. Spokas KA, Baker JM, Reicosky DC (2010) Ethylene: potential key for biochar amendment impacts. Plant Soil 333:443–452CrossRefGoogle Scholar
  68. Steiner C, Glaser B, Teixeira WG, Lehmann J, Blum WEH, Zech W (2008) Nitrogen retention and plant uptake on a highly weathered central Amazonian Ferralsol amended with compost and charcoal. J Plant Nutr Soil Sci 171:893–899. doi: 10.1002/jpln.200625199 CrossRefGoogle Scholar
  69. Steiner C, Teixeira M, Zech W (2007) Soil respiration curves as soil fertility indicators in perennial central Amazonian plantations treated with charcoal, and mineral or organic fertilisers. Trop Sci 47:218–230. doi: 10.1002/ts.216 CrossRefGoogle Scholar
  70. Stitt M, Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: the physiological and molecular background. Plant Cell Environ 22:583–621CrossRefGoogle Scholar
  71. Taghizadeh-Toosi A, Clough TJ, Condron LM, Sherlock RR, Anderson CR, Craigie RA (2011) Biochar incorporation into pasture soil suppresses in situ nitrous oxide emissions from ruminant urine patches. J Environ Qual, in press (open access)
  72. van Zwieten L, Singh B, Joseph S, Kimber S, Cowie A, Chan KY (2009) Biochar and emissions of non-CO2 greenhouse gases from soil. In: Lehmann J, Joseph S (eds) Biochar for environmental management—science and technology. Earthscan, London, pp 227–249Google Scholar
  73. van Zwieten L, Kimber S, Morris S, Downie A, Berger E, Rust J, Scheer C (2010) Influence of biochars on flux of N2O and CO2 from Ferrosol. Aust J Soil Res 48:555–568CrossRefGoogle Scholar
  74. Wardle DA, Nilsson M-C, Zackrisson O (2008) Fire-derived charcoal causes loss of forest humus. Science 320:629. doi: 10.1126/science.1154960 PubMedCrossRefGoogle Scholar
  75. Yanai Y, Toyota K, Okazaki M (2007) Effects of charcoal addition on N2O emissions from soil resulting from rewetting air-dried soil in short-term laboratory experiments. Soil Sci Plant Nutr 53:181–188CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Claudia Irene Kammann
    • 1
    • 2
    Email author
  • Sebastian Linsel
    • 1
  • Johannes W. Gößling
    • 1
  • Hans-Werner Koyro
    • 1
  1. 1.Department of Plant EcologyJustus-Liebig-University GießenGießenGermany
  2. 2.School of Biology and Environmental SciencesUniversity College DublinDublinIreland

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