Environmental Science and Pollution Research

, Volume 26, Issue 1, pp 659–671 | Cite as

Poultry biogas slurry can partially substitute for mineral fertilizers in hydroponic lettuce production

  • Lei Wang
  • Shirong Guo
  • Ying Wang
  • Dandan Yi
  • Jian WangEmail author
Research Article


Poultry biogas slurry, a by-product of the biogas production process, is rich in nutrients. However, improper handling increases the potential for serious environmental contamination and resource waste. The preparation of nutrient solutions for hydroponic lettuce production requires large amounts of mineral fertilizers, which provides an opportunity for poultry biogas slurry to enter the crop nutrient cycle. To assess the feasibility of the application of poultry biogas slurry, we used different proportions of biogas slurry and mineral fertilizers in a hydroponics experiment with lettuce. Four treatments were established: HS (half-strength Hoagland solution), BS (2.6% biogas slurry), BS + HS (1.3% biogas slurry + quarter-strength Hoagland solution), and BS + MF (2.6% biogas slurry + mineral fertilizers). The addition of poultry biogas slurry (BS + HS) did not have an adverse effect on lettuce growth, significantly increased the soluble sugar concentration, reduced the nitrate concentration, and the concentrations of heavy metals were still within the safety standards. In addition, the application of poultry biogas slurry could effectively reduce the production costs, energy consumption, and greenhouse gas emissions of hydroponically grown lettuce. Based on our study, poultry biogas slurry could replace 50% of the mineral fertilizer used in hydroponic lettuce production. The key is to control the electrical conductivity and replenish the nutrients that are lacking in the biogas slurry, especially magnesium.


Poultry biogas slurry Substitute fertilization Quality Heavy metals Economic and ecological benefits Lettuce 



The work was financially supported by Jiangsu Province Scientific and Technological Achievements Special Fund (no. BA2014147), the National Key Research and Development Program of China (no. 2016YED0201007), China Agriculture Research System (no. CARS-23-B12), and the Fundamental Research Funds for the Central Universities (6J1009). In addition, the authors would like to thank the anonymous reviewers and the editors for their comments to improve the paper.


  1. Abubaker J, Risberg K, Pell M (2012) Biogas residues as fertilisers—effects on wheat growth and soil microbial activities. Appl Energy 99:126–134CrossRefGoogle Scholar
  2. Alburquerque JA, Fuente CDL, Bernal MP (2012a) Chemical properties of anaerobic digestates affecting C and N dynamics in amended soils. Agric Ecosyst Environ 160:15–22CrossRefGoogle Scholar
  3. Alburquerque JA, Fuente CDL, Ferrercosta A, Carrasco L, Cegarra J, Abad M, Bernal MP (2012b) Assessment of the fertiliser potential of digestates from farm and agroindustrial residues. Biomass Bioenergy 40:181–189CrossRefGoogle Scholar
  4. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15CrossRefGoogle Scholar
  5. Ashraf M, Pjc H (2004) Potential biochemical indicators of salinity tolerance in plants. Plant Sci 166:3–16CrossRefGoogle Scholar
  6. Baitilwake MA, De Bolle S, Salomez J, Mrema JP, De Neve S (2012) Effect of organic fertilizers on nitrate accumulation in vegetables and mineral nitrogen in tropical soils of Morogoro, Tanzania. Exp Agric 48:111–126CrossRefGoogle Scholar
  7. Baral KR, Labouriau R, Olesen JE, Petersen SO (2017) Nitrous oxide emissions and nitrogen use efficiency of manure and digestates applied to spring barley. Agric Ecosyst Environ 239:188–198CrossRefGoogle Scholar
  8. Battie-Laclau P et al (2013) Photosynthetic and anatomical responses of Eucalyptus grandis leaves to potassium and sodium supply in a field experiment. Plant Cell Environ 37:70–81CrossRefGoogle Scholar
  9. Bian B, Lin C, Lv L (2016) Health risk assessment of heavy metals in soil–plant system amended with biogas slurry in Taihu basin, China. Environ Sci Pollut Res 23:16955–16964CrossRefGoogle Scholar
  10. Bian B, Lv L, Yang DH, Zhou LJ (2014) Migration of heavy metals in vegetable farmlands amended with biogas slurry in the Taihu Basin, China. Ecol Eng 71:380–383CrossRefGoogle Scholar
  11. Bian B, Wu HS, Lv L, Fan YM, Lu HM (2015a) Health risk assessment of metals in food crops and related soils amended with biogas slurry in Taihu Basin: perspective from field experiment. Environ Sci Pollut Res 22:14358–14366CrossRefGoogle Scholar
  12. Bian B, Zhou LJ, Li L, Lv L, Fan YM (2015b) Risk assessment of heavy metals in air, water, vegetables, grains, and related soils irrigated with biogas slurry in Taihu Basin, China. Environ Sci Pollut Res 22:7794–7807CrossRefGoogle Scholar
  13. Bohn T, Walczyk T, Leisibach S, Hurell RF (2004) Chlorophyll-bound magnesium in commonly consumed vegetables and fruits: relevance to magnesium nutrition. J Food Sci 69:S347–S350CrossRefGoogle Scholar
  14. Case SDC, Oelofse M, Hou Y, Oenema O, Jensen LS (2017) Farmer perceptions and use of organic waste products as fertilisers—a survey study of potential benefits and barriers. Agric Syst 151:84–95CrossRefGoogle Scholar
  15. Cataldo DA, Maroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Commun Soil Sci Plant Anal 6:71–80CrossRefGoogle Scholar
  16. Chandra RK (1984) Excessive intake of zinc impairs immune responses. JAMA 252:1443–1446CrossRefGoogle Scholar
  17. Chen DJ, Jiang LN, Huang H, Toyota K, Dahlgren RA, Lu J (2013) Nitrogen dynamics of anaerobically digested slurry used to fertilize paddy fields. Biol Fertil Soils 49:647–659CrossRefGoogle Scholar
  18. Ciompi S, Gentili E, Guidi L, Soldatini GF (1996) The effect of nitrogen deficiency on leaf gas exchange and chlorophyll fluorescence parameters in sunflower. Plant Sci 118:177–184CrossRefGoogle Scholar
  19. De la Fuente C, Alburquerque JA, Clemente R, Bernal MP (2013) Soil C and N mineralisation and agricultural value of the products of an anaerobic digestion system. Biol Fertil Soils 49:313–322CrossRefGoogle Scholar
  20. Dupont MS, Mondin Z, Williamson G, Price KR (2000) Effect of variety, processing, and storage on the flavonoid glycoside content and composition of lettuce and endive. J Agric Food Chem 48:3957–3964CrossRefGoogle Scholar
  21. Frisbie SH, Mitchell EJ, Dustin H, Maynard DM, Sarkar B (2012) World Health Organization discontinues its drinking-water guideline for manganese. Environ Health Perspect 120:775–778CrossRefGoogle Scholar
  22. Gaetke LM, Chow CK (2003) Copper toxicity, oxidative stress, and antioxidant nutrients. Toxicology 189:147–163CrossRefGoogle Scholar
  23. Hajibagheri MA, Harvey DMR, Flowers TJ (1987) Quantitative ion distribution within root cells of salt-sensitive and salt-tolerant maize varieties. New Phytol 105:367–379CrossRefGoogle Scholar
  24. Horta C, Roboredo M, Carneiro JP, Duarte AC, Torrent J, Sharpley A (2017) Organic amendments as a source of phosphorus: agronomic and environmental impact of different animal manures applied to an acid soil. Arch Agron Soil Sci 64:257–271CrossRefGoogle Scholar
  25. Illera-Vives M, Labandeira SS, Brito LM, López-Fabal A, López-Mosquera ME (2015) Evaluation of compost from seaweed and fish waste as a fertilizer for horticultural use. Sci Hortic 186:101–107CrossRefGoogle Scholar
  26. Insam H, Gómez-Brandón M, Ascher J (2015) Manure-based biogas fermentation residues—friend or foe of soil fertility? Soil Biol Biochem 84:1–14CrossRefGoogle Scholar
  27. Jin H, Chang Z (2011) Distribution of heavy metal contents and chemical fractions in anaerobically digested manure slurry. Appl Biochem Biotechnol 164:268–282CrossRefGoogle Scholar
  28. Li JS, Duan N, Guo S, Shao L, Lin C, Wang JH, Hou J, Hou Y, Meng J, Han MY (2012) Renewable resource for agricultural ecosystem in China: ecological benefit for biogas by-product for planting. Ecological Informatics 12:101–110CrossRefGoogle Scholar
  29. Li JW, Yang JP, Fei PP, Song JL, Li DS, Ge CS, Chen WY (2009) Responses of rice leaf thickness, SPAD readings and chlorophyll a/b ratios to different nitrogen supply rates in paddy field. Field Crop Res 114:426–432CrossRefGoogle Scholar
  30. Li Z, Tan XF, Lu K, Liu ZM, Wu LL (2017) The effect of CaCl2 on calcium content, photosynthesis, and chlorophyll fluorescence of tung tree seedlings under drought conditions. Photosynthetica 55:553–560CrossRefGoogle Scholar
  31. Liu WK, Du LF, Yang QC (2009) Biogas slurry added amino acids decreased nitrate concentrations of lettuce in sand culture. Acta Agriculturae Scandinavica Section B - Soil and Plant Science 59:260–264. CrossRefGoogle Scholar
  32. Liu WK, Yang QC, Du LF, Cheng RF, Zhou WL (2011) Nutrient supplementation increased growth and nitrate concentration of lettuce cultivated hydroponically with biogas slurry. Acta Agriculturae Scandinavica Section B - Soil and Plant Science 61:391–394. CrossRefGoogle Scholar
  33. Liu CW, Sung Y, Chen BC, Lai HY (2014) Effects of nitrogen fertilizers on the growth and nitrate content of lettuce (Lactuca sativa L.) International Journal of Environmental Research and Public Health 11(4):4427–4440Google Scholar
  34. Lobo AK, De OMM, Lima Neto MC, Machado EC, Ribeiro RV, Silveira JA (2015) Exogenous sucrose supply changes sugar metabolism and reduces photosynthesis of sugarcane through the down-regulation of rubisco abundance and activity. J Plant Physiol 179:113–121CrossRefGoogle Scholar
  35. Long SP, Bernacchi CJ (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. J Exp Bot 54:2393–2401CrossRefGoogle Scholar
  36. Lutts S, Kinet JM, Bouharmont J (1996) Effects of salt stress on growth, mineral nutrition and proline accumulation in relation to osmotic adjustment in rice (Oryza sativa L.) cultivars differing in salinity resistance. Plant Growth Regul 19:207–218CrossRefGoogle Scholar
  37. Ministry of Agriculture of the People’s Republic of China (MAPRC) (2013) China rural energy yearbook. China Agriculture Press, Beijing (in Chinese)Google Scholar
  38. Ministry of Environmental Protection of the People’s Republic of China (MEPPRC) (2010) The first national census bulletin of pollution sources Accessed 6 February 2010 (in Chinese)
  39. Macduff JH, Wild A, Hopper MJ, Dhanoa MS (1986) Effects of temperature on parameters of root growth relevant to nutrient uptake: measurements on oilseed rape and barley grown in flowing nutrient solution. Plant Soil 94:321–332CrossRefGoogle Scholar
  40. Marion MB (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254CrossRefGoogle Scholar
  41. Möller K, Müller T, Oechsner H, Jungbluth T, Kranert M, Kusch S (2012) Effects of anaerobic digestion on digestate nutrient availability and crop growth: a review. Eng Life Sci 12:242–257CrossRefGoogle Scholar
  42. Moreno-García B, Guillén M, Quílez D (2017) Response of paddy rice to fertilisation with pig slurry in Northeast Spain: strategies to optimise nitrogen use efficiency. Field Crop Res 208:44–54CrossRefGoogle Scholar
  43. National Bureau of Statistics of the People’s Republic of China (NBSPRC) (2012) China rural statistical yearbook. China Statistics Press, Beijing (in Chinese)Google Scholar
  44. National Bureau of Statistics of the People’s Republic of China (NBSPRC) (2015) China statistical yearbook. China Statistics Press, Beijing (in Chinese)Google Scholar
  45. Nicolle C, Cardinault N, Gueux E, Jaffrelo L, Rock E, Mazur A, Amouroux P, Rémésy C (2004) Health effect of vegetable-based diet: lettuce consumption improves cholesterol metabolism and antioxidant status in the rat. Clin Nutr 23:605–614CrossRefGoogle Scholar
  46. Nkoa R (2014) Agricultural benefits and environmental risks of soil fertilization with anaerobic digestates: a review. Agron Sustain Dev 34:473–492CrossRefGoogle Scholar
  47. Nyord T, Hansen MN, Birkmose TS (2012) Ammonia volatilisation and crop yield following land application of solid–liquid separated, anaerobically digested, and soil injected animal slurry to winter wheat. Agric Ecosyst Environ 160:75–81CrossRefGoogle Scholar
  48. Oliveira F, Rocha S, Fernandes R (2014) Iron metabolism: from health to disease. J Clin Lab Anal 28:210–218CrossRefGoogle Scholar
  49. Pérez-Pérez JG, Robles JM, Tovar JC, Botía P (2009) Response to drought and salt stress of lemon ‘Fino 49’ under field conditions: water relations, osmotic adjustment and gas exchange. Sci Hortic 122:83–90CrossRefGoogle Scholar
  50. Pu C et al (2017) Impact of direct application of biogas slurry and residue in fields: in situ analysis of antibiotic resistance genes from pig manure to fields. J Hazard Mater 344:441–449CrossRefGoogle Scholar
  51. Rao BH, Nair RM, Nayyar H (2016) Salinity and high temperature tolerance in mungbean [Vigna radiata (L.) Wilczek] from a physiological perspective. Front Plant Sci 7:957. CrossRefGoogle Scholar
  52. Roe JH (1954a) Chemical determination of ascorbic, dehydroascorbic, and diketogulonic acids. Methods Biochem Anal 1:115–139Google Scholar
  53. Roe JH (1954b) The determination of dextran in blood and urine with anthrone reagent. J Biol Chem 208:889–896Google Scholar
  54. Sandstead HH (1995) Requirements and toxicity of essential trace elements, illustrated by zinc and copper. Am J Clin Nutr 61:621S–624SCrossRefGoogle Scholar
  55. Seemann JR, Critchley C (1985) Effects of salt stress on the growth, ion content, stomatal behaviour and photosynthetic capacity of a salt-sensitive species, Phaseolus vulgaris L. Planta 164:151–162CrossRefGoogle Scholar
  56. Serafini M, Bugianesi R, Salucci M, Azzini E, Raguzzini A, Maiani G (2002) Effect of acute ingestion of fresh and stored lettuce (Lactuca sativa) on plasma total antioxidant capacity and antioxidant levels in human subjects. Br J Nutr 88:615–623CrossRefGoogle Scholar
  57. Shalata A, Neumann PM (2001) Exogenous ascorbic acid (vitamin C) increases resistance to salt stress and reduces lipid peroxidation. J Exp Bot 52:2207–2211CrossRefGoogle Scholar
  58. Sigurnjak I, Michels E, Crappé S, Buysens S, Tack FMG, Meers E (2016) Utilization of derivatives from nutrient recovery processes as alternatives for fossil-based mineral fertilizers in commercial greenhouse production of Lactuca sativa L. Sci Hortic 198:267–276CrossRefGoogle Scholar
  59. Silva EN, Ferreirasilva SL, Viégas RA, Silveira JAG (2010) The role of organic and inorganic solutes in the osmotic adjustment of drought-stressed Jatropha curcas plants. Environ Exp Bot 69:279–285CrossRefGoogle Scholar
  60. Tanaka A, Tsuji H (1980) Effects of calcium on chlorophyll synthesis and stability in the early phase of greening in cucumber cotyledons. Plant Physiol 65:1211–1215CrossRefGoogle Scholar
  61. Tavakkoli E, Fatehi F, Coventry S, Rengasamy P, Mcdonald GK (2011) Additive effects of Na+ and Cl ions on barley growth under salinity stress. J Exp Bot 62:2189–2203CrossRefGoogle Scholar
  62. Vaneeckhaute C, Meers E, Michels E, Buysse J, Tack FMG (2013) Ecological and economic benefits of the application of bio-based mineral fertilizers in modern agriculture. Biomass Bioenergy 49:239–248CrossRefGoogle Scholar
  63. Wang PR, Zhang FT, Gao JX, Sun XQ, Deng XJ (2009) An overview of chlorophyll biosynthesis in higher plants. Acta bot Boreal-Occident Sin 29(3):0629–0636 (in Chinese)Google Scholar
  64. Wang T, Wang SP, Guo SR, Sun YJ (2008) Effects of exogenous spermidine on the photosynthesis of Cucumis sativus L. seedlings under rhizosphere hypoxia stress. Front Agric China 2:55–60CrossRefGoogle Scholar
  65. Wang XK, Huang JL (2015) Principles and techniques of plant physiological biochemical experiment. Higher Education Press, Beijing (in Chinese)Google Scholar
  66. Wheeler GL, Jones MA, Smirnoff N (1998) The biosynthetic pathway of vitamin C in higher plants. Nature 393:365–369CrossRefGoogle Scholar
  67. Wortman SE (2015) Crop physiological response to nutrient solution electrical conductivity and pH in an ebb-and-flow hydroponic system. Sci Hortic 194:34–42CrossRefGoogle Scholar
  68. Yang CW, Shi DC, Wang DL (2008) Comparative effects of salt and alkali stresses on growth, osmotic adjustment and ionic balance of an alkali-resistant halophyte Suaeda glauca (Bge.). Plant Growth Regul 56:179–190CrossRefGoogle Scholar
  69. Yang CW, Xu HH, Wang LL, Liu J, Shi DC, Wang DL (2009) Comparative effects of salt-stress and alkali-stress on the growth, photosynthesis, solute accumulation, and ion balance of barley plants. Photosynthetica 47:79–86CrossRefGoogle Scholar
  70. Yuan LY, Shu S, Sun J, Guo SR, Tezuka T (2012) Effects of 24-epibrassinolide on the photosynthetic characteristics, antioxidant system, and chloroplast ultrastructure in Cucumis sativus L. under Ca(NO(3))(2) stress. Photosynth Res 112:205–214CrossRefGoogle Scholar
  71. Yuan YH, Zhong M, Shu S, du N, He L, Yuan L, Sun J, Guo S (2015) Effects of exogenous putrescine on leaf anatomy and carbohydrate metabolism in cucumber (Cucumis sativus L.) under salt stress. J Plant Growth Regul 34:451–464CrossRefGoogle Scholar
  72. Zhang J, Wang MY, Cao YC, Liang P, Wu SC, Leung AOW, Christie P (2017) Replacement of mineral fertilizers with anaerobically digested pig slurry in paddy fields: assessment of plant growth and grain quality. Environ Sci Pollut Res 24:8916–8923CrossRefGoogle Scholar
  73. Zirkler D, Peters A, Kaupenjohann M (2014) Elemental composition of biogas residues: variability and alteration during anaerobic digestion. Biomass Bioenergy 67:89–98CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Lei Wang
    • 1
    • 2
  • Shirong Guo
    • 1
    • 2
  • Ying Wang
    • 1
    • 2
  • Dandan Yi
    • 1
    • 2
  • Jian Wang
    • 1
    • 2
    Email author
  1. 1.College of HorticultureNanjing Agricultural UniversityNanjingChina
  2. 2.Nanjing Agricultural University (Suqian) Academy of Protected HorticultureSuqianChina

Personalised recommendations