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Agricultural benefits and environmental risks of soil fertilization with anaerobic digestates: a review

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Abstract

Intensive soil fertilization with mineral fertilizers has led to several issues such as high cost, nitrate pollution and loss of soil carbon. Fertilization with organic matter such as compost therefore represents an alternative for sustainable agriculture. Traditional organic amendments such as manures, composts and sewage sludge have been extensively studied in the past. However, applications of biogas digestates and their impacts on the environment and human health are still unexplored. Recent articles report the agricultural potential and conflicting results of digestate performances. As a consequence, the effectiveness of digestate as organic amendment and fertilizer is still under debate. Here we review the legislative, chemical, agronomic and environmental literature on anaerobic digestates. We found that digestates can be considered as organic amendments or organic fertilizers, when properly handled and managed. Indeed we further show that anaerobic digestates have a higher potential to harm the environment and human health than undigested animal manures and slurries. The main points are the following: (1) Most solid digestates comply with the European organic matter minimal requirement for an organic amendment; (2) the fertilizer values of liquid digestates lie between those of livestock manures and inorganic fertilizers; (3) anaerobic digestates have higher NH3 emission potential than undigested animal manures and slurries and, consequently, pose a greater risk to the broad environment; (4) high Cu and Zn concentrations in digestates from co-digestion of pig and cattle slurry feedstock could jeopardize the sustainability of agricultural soils and (5) high Mn concentrations in digestates can induce Mn toxicity in agricultural soils, upon repeated applications.

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References

  • Abdullahi YA, Akunna JC, White NA, Hallet PD, Wheatley R (2008) Investigating the effects of anaerobic and aerobic post-treatment on quality and stability of organic fraction of municipal waste as soil amendment. Bioresour Technol 99:8631–8636. doi:10.1016/j.biortech.2008.04.027

    PubMed  CAS  Google Scholar 

  • Adeli A, Varco JJ, Sistani KR, Rowe DE (2005) Effects of swine lagoon effluent relative to commercial fertilizer applications on warm-season forage nutritive value. Agro J 97:408–417. doi:10.2134/agronj2005.0408

    CAS  Google Scholar 

  • AFNOR: FD CR 13456 (2001) Amendements du sol et supports de culture—Etiquetage, specifications et listes de produits. Association Française de Normalisation, La Plaine Saint-Denis Cedex

  • Ahmad R, Jabeen N (2009) Demonstration of crop improvement in sunflower (Helianthus annus L.) by the use of organic fertilizers under saline conditions. Pak J Bot 41:1373–1384

    Google Scholar 

  • Ahring BK (2003) Preface. In: Ahring BK (ed) Biomethanation II. Springer, Berlin

    Google Scholar 

  • Al Seadi T, Moller HB (2003) Separation of slurry—a potential option for the animal production sector. In: Proceedings of the European biogas workshop “The future of biogas in Europe II”. Esbjerg, 2–4 October

  • Alburquerque JA, de la Fuente C, Ferre-Costa A, Carrasco L, Cegarra J, Abad M, Bernal MP (2012) Assessment of the fertiliser potential of digestates from farm and agro-industrial residues. Biomass Bioenergy 40:181–189. doi:10.1016/j.biombioe.2012.02.018

    CAS  Google Scholar 

  • Amon B, Kryvoruchko V, Amon T, Zechmeister-Boltenstern (2006) Methane, nitrous oxide and ammonia emissions during storage and after application of dairy cattle slurry and influence of slurry treatment. Agric Ecosyst Environ 112:153–162. doi:10.1016/j.agee.2005.08.030

    CAS  Google Scholar 

  • Amon T, Amon B, Kryvoruchko V, Zollitsch W, Mayer K, Gruber L (2007) Biogas production from maize and dairy cattle manure—influence of biomass composition on the methane yield. Agric Ecosyst Environ 118:173–182. doi:10.1016/j.agee.2006.05.007

    CAS  Google Scholar 

  • Angelidaki I, Ellegaard L, Ahring BK (2003) Applications of the anaerobic digestion process. In: Ahring BK (ed) Biomethanation II. Springer, Berlin, pp 1–33

    Google Scholar 

  • Arthurson V (2009) Closing the global energy and nutrient cycles through application of biogas residue to agricultural land—potential benefits and drawbacks. Energies 2:226–242. doi:10.3390/en20200226

    CAS  Google Scholar 

  • Asman WAH (1992) Ammonia emissions in Europe: updated emissions and emission variations. Report no. 228471008. National Institute of Public Health and Environmental Protection, Bilthoven

  • Asman WAH, Van Jaarsveld HA (1990) Regional and Europe-wide emission and transport of NHx compounds. In: Hartung J et al (eds) Ammoniak in der Unwelt, vol 2. Landwirtschaftswerlad, Munster, pp 1–35

    Google Scholar 

  • Bachmann S, Wentzel S, Eichier-Löbermann B (2011) Codigested dairy slurry as a phosphorus and nitrogen source for Zea mays L. and Amaranthus cruentus L. J Plant Nutr Soil Sci 174:908–915. doi:10.1002/jpln.201000383

    CAS  Google Scholar 

  • Bagge E, Sahlstrom L, Albihn A (2005) The effect of hygienic treatment on the microbial flora of biowaste at biogas plants. Water Res 39:4879–4880. doi:10.1016/j.watres.2005.03.016

    PubMed  CAS  Google Scholar 

  • Berger KC, Gerloff GC (1947) Manganese toxicity of potatoes in relation to strong soil acidity. Soil Sci Soc Am Proc 12:310–314. doi:10.2136/sssaj1948.036159950012000C0074x

    Google Scholar 

  • Bethlenfalvay GJ, Yoder JF (1981) The glycine–glomus–rhizobium symbiosis I. Phosphorus effect on nitrogen fixation and mycorrhizal infection. Physiol Plant 52:141–145. doi:10.1111/j.1399-3054.1981.tb06047.x

    Google Scholar 

  • Bicudo JR, Goyal SM (2003) Pathogens and manure management systems: a review. Environ Technol 24:115–130. doi:10.1080/09593330309385542

    PubMed  CAS  Google Scholar 

  • Birkmose T (2009) Nitrogen recovery from organic manures: improved slurry application techniques and treatment—the Danish scenario. International Fertiliser Society, Proceedings 656

  • Bischofsberger W, Dichtl N, Rosenwinkel KH, Seyfried CF, Böhnke B (2005) Anaerobtechnik, 2nd rev. edn. Springer, Berlin

  • Bonetta S, Ferretti E, Bonetta S, Fezia G, Carraro E (2011) Microbiological contamination of digested products from anaerobic co-digestion of bovine manure and agricultural by-products. Lett Appl Microbiol 53:552–557. doi:10.1111/j.1472-765X.2011.03148.x

    PubMed  CAS  Google Scholar 

  • Börjesson P, Berglund M (2007) Environmental system analysis of biogas systems. Part II: The environmental impact of replacing various reference systems. Biomass Bioenergy 31:326–344. doi:10.1016/j.biombioe.2007.01.004

    Google Scholar 

  • Boydston RA, Collins HP, Vaughn SF (2008) Response of weeds and ornamental plants to potting soil amended with dried distillers grains. HortSci 43:191–195

    Google Scholar 

  • Brenner A, Clemens J (2005) Vergleich der stoffflüsse mit ökologischer bilanzierung von zwei kofermentationsanlagen. Technical report. University of Bonn, Germany. http://www.usl.uni-bonn.de/pdf/forschungsbericht%20128.pdf. Accessed 2 Mar 2012

  • BSI. PAS 110 (2010) Specification for whole digestate, separated liquor and separated fibre derived from the anaerobic digestion of source-segregated biodegradable materials. British Standards Institution, London. http://www.wrap.org.uk/sites/files/wrap/PAS110_vis_10.pdf Accessed 03 January, 2013

  • Buffiere P, Loisel D, Bernet N, Delgenes JP (2006) Towards new indicators for the prediction of solid waste anaerobic digestion properties. Water Sci Technol 53:233–241

    PubMed  CAS  Google Scholar 

  • Buijsman E, Maas HFM, Asman WAH (1987) Anthropogenic NH3 emissions in Europe. Atmos Environ 21:1009–1022. doi:10.1016/0004-6981(87)90230-7

    CAS  Google Scholar 

  • Burgess JE, Quarmby J, Stephenson T (1999) Role of micronutrients in activated sludge-based biotreatment of industrial effluents. Biotechnol Adv 17:49–70. doi:10.1016/S0734-9750(98)00016-0

    PubMed  CAS  Google Scholar 

  • Burns JC, Westerman PW, King LD, Overcash MR, Cummings GA (1987) Swine manure and lagoon effluent applied to a temperate forage mixture: I. Persistence, yield, quality, and elemental removal. J Environ Qual 16:99–105. doi:10.2134/jeq1987.00472425001600020002x

    CAS  Google Scholar 

  • Campitelli P, Ceppi S (2008) Effects of composting technologies on the chemical and physiochemical properties of humic acids. Geoderma 144:325–333. doi:10.1016/j.geoderma.2007.12.003

    CAS  Google Scholar 

  • Canali S, Bartolomeo ED, Tittarelli F, Montemurro F, Verrastro V, Ferri D (2011) Comparison of different laboratory incubation procedures to evaluate nitrogen mineralization in soil amended with aerobic and anaerobic stabilized organic materials. J Food Agric Environ 9:540–546

    Google Scholar 

  • Chambers BJ, Smith KA, van der Weerden TJ (1997) Ammonia emissions following the land spreading of solid manures. In: Jarvis SC, Pain BF (eds) Gaseous nitrogen emissions from grasslands. CAB International, Oxford, pp 275–280

    Google Scholar 

  • Chantigny MH, Rochette P, Angers DA, Massé D, Côté D (2004) Ammonia volatilization and selected soil characteristics following application of anaerobically digested pig slurry. Soil Sci Soc Am J 68:306–312. doi:10.2136/sssaj2004.3060

    CAS  Google Scholar 

  • Chantigny MH, Angers DA, Belanger G, Rochette P, Masse D, Cote D (2007) Gaseous N emissions and forage N uptake on soils fertilized with raw and treated swine manure. J Environ Qual 36:1864–1872. doi:10.2134/jeq2007.0083

    PubMed  CAS  Google Scholar 

  • Chantigny MH, Angers DA, Belanger G, Rochette P, Eriksen-Hamel N, Bittman S, Buckley K, Masse D, Gasser M-O (2008) Yield and nutrient export of grain corn fertilized with raw and treated liquid swine manure. Agron J 100:1303–1309. doi:10.2134/agronj2007.0361

    Google Scholar 

  • Chesworth W (1991) Geochemistry of micronutrients. In: Mortvedt JJ, Cox FR, Shuman LM, Welch RM (eds) Micronutrients in agriculture. Soil Science Society of America, Madison, pp 96–99

    Google Scholar 

  • Chynoweth DP, Isaacson R (1987) Anaerobic digestion of biomass. Elsevier, Barking

    Google Scholar 

  • Civil Engineering Research Institute of Hokkaido (2003) Research report of environment, resources, and recycling in Hokkaido, Sapporo. Civil Engineering Institute of Hokkaido, Sapporo (in Japanese)

    Google Scholar 

  • Clark RB (1982) Plant response to mineral element toxicity and deficiency. In: Christiansen MN, Lewis CF (eds) Breeding plants for less favorable environments. Wiley, New York, pp 71–142

    Google Scholar 

  • Clemens J, Morton RH (1999) Optimizing mineral nutrition for flower production in Heliconia “Golden Torch” using response surface methodology. J Amerc Soc Hortic Sci 124:713–718

    CAS  Google Scholar 

  • Colleran E (2000) Hygienic and sanitation requirements in biogas plants treating animal manures or mixtures of manures and other organic wastes. In: Orthenblad H (ed) Anaerobic digestion: making energy and solving modern waste problems. Herning Municipal Authorities, Denmark, pp 77–86

    Google Scholar 

  • Collins HP, Alva AK, Steubel JD, Fransen SF, Frear C, Chen S, Kruger C, Granatstein D (2011) Greenhouse gas emissions from an irrigated silt loam soil amended with anaerobically digested dairy manure. Soil Sci Soc Am J 75:2206–2216. doi:10.2136/sssaj2010.0360

    CAS  Google Scholar 

  • Damgaard PH, Børsting CE, Rom HB, Sommer SG (2001) Kvaelstof, fosfor og kalium I husdyrgødning- normtal 2000. (In Danish) (Nitrogen, phosphorus and potassium in animal manure-norms 2000). DJF rapport Husdyrbrug nr. 36

  • Denman KL, Brasseur G, Chidthaisong A, Ciais P, Cox PM, Dickinson RE et al (2007) Climate Change 2007: the physical science basis. Contribution of Working Group III to the Fourth Assessment Report of the Intergovernmental Panel on climate Change. Cambridge University Press, Cambridge

    Google Scholar 

  • DeVleeschauwer D, Verdonck O, Van Assche P (1981) Phytotoxicity of refuse compost. BioCycle 22:44–46

    CAS  Google Scholar 

  • Diacono M, Montemurro F (2010) Long-term effect of organic amendments on soil fertility. A review. Agron Sustain Dev 30:401–422. doi:10.1051/agro/2009040

    CAS  Google Scholar 

  • Doran JW, Parkin TP (1994) Defining and assessing soil quality. In: Doran JW, Coleman DC, Bezdicek DF, Stewart BA (eds) Defining soil quality for sustainable environment. American Society of Agronomy special publication. American Society of Agronomy, Madison, pp 3–21

    Google Scholar 

  • Dragosits U, Theobald MR, Place CJ, Lord E, Webb J, Hill J, ApSimon HM, Sutton MA (2002) Ammonia emission, deposition and impact assessment at the field scale: a case study of sub-grid spatial variability. Environ Pollut 117:147–158. doi:10.1016/S0269-7491(01)00147-6

    PubMed  CAS  Google Scholar 

  • Drennan MF, Distefano TD (2010) Characterization of the curing process from high solids anaerobic digestion. Biores Technol 101:537–544. doi:10.1016/j.biortech.2009.08.029

    CAS  Google Scholar 

  • EA (2009) Anaerobic digestates. Waste Protocols Project. Environment Agency, Rotherham. Available from: http://www.environment-agency.gov.uk/static/documents/Business/Financial_impact_assessment_for_anaerobic_digestate.pdf. Accessed on 18 Mar 2012

  • Ebbs SD, Kochian LV (1997) Toxicity of zinc and copper to Brassica species: implications for phytoremediation. J Environ Qual 26:776–781. doi:10.2134/jeq1997.00472425002600030026x

    CAS  Google Scholar 

  • Edelmann W, Baier U, Engeli H (2004) Environmental aspects of the anaerobic digestion of the organic fraction of municipal solid wastes and of agricultural wastes. Water Sci Technol 52:203–208

    Google Scholar 

  • El-Jaoual T, Cox DA (1998) Manganese toxicity in plants. J Plant Nutr 21:353–386. doi:10.1080/01904169809365409

    CAS  Google Scholar 

  • El-Shakweer MHA, El-Sayad EA, Ewees MSA (1998) Soil and plant analysis as a guide for the interpretation of the improvement efficiency or organic conditioners added to different soils in Egypt. Commun Soil Sci Plant 29:2067–2088. doi:10.1080/00103629809370094

    CAS  Google Scholar 

  • EPA (2004) What is visibility impairment? United States Environmental Protection Agency, Washington, DC. Available at: www.epa.gov/oar/visibility/what.html. Accessed 12 Jul 2012

  • Epstein E (1961) Mineral metabolism of halophytes. In: Rorison IH (ed) Ecological aspects of the mineral nutrition of plants. Blackwell, Oxford, pp 345–353

    Google Scholar 

  • Erisman JW, Monteny GJ (1998) Consequences of new scientific findings for future abatement of ammonia emissions. Environ Pollut 102:275–282. doi:10.1016/S0269-7491(98)80044-4

    CAS  Google Scholar 

  • Esteban RL, Sawyer JE (2005) Extractable soil phosphorus and inorganic nitrogen following application of raw and anaerobically digested swine manure. Agron J 97:879–885. doi:10.2134/agronj2004.0249

    Google Scholar 

  • Fangmeier A, Hadwiger-Fangmeier A, Van der Eerden L, Jäger H (1994) Effects of atmospheric ammonia on vegetation—a review. Environ Pollut 86:43–82. doi:10.1016/0269-7491(94)90008-6

    PubMed  CAS  Google Scholar 

  • Fouda S (2011) Nitrogen availability of biogas residues. Ph.D. thesis, Technische Universitat Munchen

  • Furukawa Y, Hasegawa H (2006) Response of spinach and Komatsuna to biogas effluent made from source-separated kitchen garbage. J Environ Qual 35:1939–1947. doi:10.2134/jeq2005.0482

    PubMed  CAS  Google Scholar 

  • Gantzer C, Gaspard P, Galvez L, Huyard A (2001) Monitoring of bacteriological and parasitological contamination during various treatment of sludge. Water Res 35:3763–3770. doi:10.1016/S0043-1354(01)00105-1

    PubMed  CAS  Google Scholar 

  • Garg RN, Pathak H, Das DK, Tomar RK (2005) Use of fly ash and biogas slurry for improving wheat yield and physical properties of the soil. Environ Monit Assess 107:1–9. doi:10.1007/s10661-005-2021-x

    PubMed  CAS  Google Scholar 

  • Gell K, van Groenigen J, Cayuela ML (2011) Residues of bioenergy production chains as soil amendments: immediate and temporal phytotoxicity. J Hazard Mat 186:2017–2025. doi:10.1016/j.jhazmat.2010.12.105

    CAS  Google Scholar 

  • Gericke D (2009) Measuring and modeling of ammonia emissions after field application of biogas slurries. Doctoral thesis, Kiel University, Germany

  • Goberna M, Insam H, Franke-Whittle IH (2009) Effect of biowaste sludge maturation on the diversity of thermophilic bacteria and archaea in an anaerobic reactor. Appl Environ Microbiol 75:2566–2570. doi:10.1128/AEM.02260-08

    PubMed Central  PubMed  CAS  Google Scholar 

  • Goberna M, Podmirseg SM, Waldhuber S, Knapp BA, Garcia C, Insam H (2011) Pathogenic bacteria and mineral N in soils following the land spreading of biogas digestates and fresh manure. Appl Soil Ecol 49:18–25. doi:10.1016/j.apsoil.2011.07.007

    Google Scholar 

  • Gomez X, Cuetos MJ, Garcia AI, Moran A (2005) Evaluation of digestate stability from anaerobic process by thermogravimetric analysis. Thermochim Acta 426:179–184. doi:10.1016/j.tca.2004.07.019

    CAS  Google Scholar 

  • Gomez X, Cuetos MJ, Garcia AI, Moran A (2007) An evaluation of stability by thermogravimetric analysis of digestate obtained from different biowastes. J Hazard Mater 149:97–105. doi:10.1016/j.jhazmat.2007.03.049

    PubMed  CAS  Google Scholar 

  • Gong W, Yan X, Wang J, Hu T, Gong Y (2011) Long-term application of chemical and organic fertilizers on plant-available nitrogen pools and nitrogen management index. Biol Fertil Soils 47:767–775. doi:10.1007/s00374-011-0585-x

    CAS  Google Scholar 

  • Goodroad LL, Keeney DR (1984) Nitrous oxide emissions from soil during thawing. Can J Soil Sci 64:187–194. doi:10.4141/cjss84-020

    CAS  Google Scholar 

  • Gorsuch JW, Kringle RO, Robillard KA (1990) Chemical effects on the germination and early growth of terrestrial plants. ASTM special technical publication, pp 49–58

  • Gough RE, Carlstrom R (1999) Wheat gluten meal inhibits germination and growth of broadleaf and grassy weeds. HortSci 34:269–270

    Google Scholar 

  • Goulding KWT, Bailey NJ, Bradbury NJ, Hargreaves P, Howe M, Murphy DV, Poulton PR (1998) Nitrogen deposition and its contribution to nitrogen cycling and associated soil processes. New Phytol 139:49–58. doi:10.2307/2588247

    CAS  Google Scholar 

  • Grewal SK, Rajeev S, Sreevatsan S, Michel FC (2006) Persistence of Mycobacterium avium subsp. Paratuberculosis and other zoonotic pathogens during simulated composting, manure packing, and liquid storage of dairy manure. Appl Environ Microbial 72:565–574

    CAS  Google Scholar 

  • Gutser R, Ebertseder T, Weber A, Schraml M, Schmidhalter U (2005) Short-term and residual availability of nitrogen after long-term application of organic fertilizers on arable land. J Plant Nutr Soil Sci 168:439–446. doi:10.1002/jpln.200520510

    CAS  Google Scholar 

  • Hachida S, Sellami F, Cegarra J, Hachida R, Drira N, Medhhioub K, Ammar E (2009) Biological activity during co-composting of sludge issued from OMW evaporation ponds with poultry manure. Physico-chemical characterization of the processed organic matter. J Hazard Mater 162:402–409. doi:10.1016/j.jhazmat.2008.05.053

    Google Scholar 

  • Hao X, Chang C, Janzen HH, Hill BR, Ormann T (2005) Potential nitrogen enrichment of soil and surface water by atmospheric ammonia sorption in intensive livestock production areas. Agric Ecosyst Environ 110:185–194. doi:10.1016/j.agee.2005.04.002

    CAS  Google Scholar 

  • Hao X, Chang C, Janzen HH, Clayton G, Hill BR (2006) Sorption of atmospheric ammonia by soil and perennial grass downwind from two large cattle feedlots. J Environ Qual 35:1960–1965. doi:10.2134/jeq2005.0308

    PubMed  CAS  Google Scholar 

  • Haraldsen TK, Andersen U, Krogstad T, Sørheim R (2011) Liquid digestate from anaerobic treatment of source-separated household waste as fertilizer to barley. Waste Manag Res 29:1271–1276. doi:10.1177/0734242X11411975

    PubMed  CAS  Google Scholar 

  • Hasegawa H, Furukawa Y, Kimura SD (2005) On-farm assessment of organic amendments effects on nutrient status and nutrient use efficiency of organic rice fields in Northeastern Japan. Agric Ecosyst Environ 108:350–362. doi:10.1016/j.agee.2004.12.015

    Google Scholar 

  • Hatfield JL, Stewart BA (2002) Animal wastes utilization: effective use of manure as a soil resource. CRC, Boca Raton

    Google Scholar 

  • Havlin JL, Kissel DE, Maddux LD, Claassen MM, Long JH (1990) Crop rotation and tillage effects on soil organic carbon and nitrogen. Soil Sci Soc Amer J 54:448–452. doi:10.2136/sssaj1990.03615995005400020026x

    Google Scholar 

  • Hengnirun S, Barrington S, Prasher SO, Lyew D (1999) Development and verification of a model simulating ammonia volatilization from soil and manure. J Environ Qual 28:108–144. doi:10.2134/jeq1999.00472425002800010012x

    CAS  Google Scholar 

  • Herrmann A, Sieling K, Wienforth B, Taube F, Kage H (2013) Short-term effects of biogas residue application on yield performance and N balance parameters of maize in different cropping systems. J Agric Sci 151:449–462. doi:10.1017/S0021859612000548

    CAS  Google Scholar 

  • Holm-Nielsen JB, Al Seadi T, Oleskowicz-Popiel P (2009) The future of anaerobic digestion and biogas utilization. Bioresour Technol 100:5478–5480. doi:10.1016/j.biortech.2008.12.046

    PubMed  CAS  Google Scholar 

  • Horst WJ (1988) The physiology of Mn toxicity. In: Graham RD, Hannam RJ, Uren NC (eds) Manganese in soils and plants. Kluwer Academic, Dordrecht, pp 175–188

    Google Scholar 

  • Hubbard RK, Lowrance RR (1998) Dairy cattle manure management. In: Agricultural utilization of municipal, animal and industrial wastes. USDA, Agric. Res. Service, Conservation Res. Rep. No. 44. USDA, Washington, DC, pp 91–100

  • Huisjsmans JFM, Hol JMG, Hendriks MMW (2002) Effect of application techniques, manure characteristics, weather and field conditions on ammonia volatilization from manure applied to grassland. Neth J Agric Sci 49:323–342. doi:10.1016/S1573-5214(01)80021-X

    Google Scholar 

  • Hutchison ML, Walters LD, Avery SM, Munro F, Moore A (2005) Analysis of livestock production, waste storage, and pathogen levels and prevalences in farm manures. Appl Environ Microbiol 71:1231–1236. doi:10.1128/AEM.71.3.1231-1236.2005

    PubMed Central  PubMed  CAS  Google Scholar 

  • Iakimenko O, Otabbong E, Sadovnikova L, Persson J, Nilsson I, Orlov D, Ammosova Y (1996) Dynamic transformation of sewage sludge and farmyard manure components. 1. Content of humic substances and mineralization of organic carbon and nitrogen in incubated soils. Agric Ecosyst Environ 58:121–126. doi:10.1016/0167-8809(95)01006-8

    Google Scholar 

  • IEA (2010) Utilisation of digestate from biogas plants as biofertiliser. International Energy Agency, IEA Bioenergy Task 37, Paris

    Google Scholar 

  • Inglet GE, Rose DJ, Stevenson DG, Chen D, Biswas A (2009) Total phenolic and antioxidant activity of water and ethanolic extracts from distillers dried grains with solubles with or without microwave irradiation. Cereal Chem 86:661–664. doi:10.1094/CCHEM-86-6-0661

    Google Scholar 

  • Israel DW (1987) Investigation of the role of phosphorus in symbiotic dinitrogen fixation. Plant Physiol 84:835–840. doi:10.1104/pp. 84.3.835

    PubMed Central  PubMed  CAS  Google Scholar 

  • Jacobs LW (1981) Agricultural application of sewage sludge. In: Norchardt JA (ed) Sludge and its ultimate disposal. Ann Arbor Science, Ann Arbor, pp 109–126

    Google Scholar 

  • Jacobson HGM, Swanback TR (1932) Manganese content of certain Connecticut soils and its relation to the growth of tobacco. J Am Soc Agron 24:237–245

    CAS  Google Scholar 

  • Jäkel K, Mau S (1999) Umweltwirkung von biogasgülle. Abschluβbericht zum forschungs-projekt, Dresden. https://publikationen.sachsen.de/bdb/artikel/15244/documents/18424. Accessed 3 Oct 2013

  • Jarvis SC, Pain BF (1990) Ammonia volatilization from agricultural land. Proceedings 298. The Fertilizer Society, Peterborough

    Google Scholar 

  • Jenkinson DS, Andrew SPS, Lynch JM, Goss MJ, Tinker P (1990) The turnover of organic carbon and nitrogen in soil. Phil Trans R Soc London Ser B 329:361–368

    CAS  Google Scholar 

  • Jørgensen U, Petersen BM (2006) Interactions between biomass energy technologies and nutrient and carbon balances at the farm level. In: Petersen SO (ed) Proc. 12th Ramiran Int. Conf., pp 49–56

  • Kamprath EJ, Foy CD (1971) Lime–fertilizer–plant interactions in acid soils. In: Olson RA, Army TJ, Hanway JJ, Kilmer VJ (eds) Fertilizer technology and use. Soil Science Society of America, Madison, pp 105–141

    Google Scholar 

  • Kaparaju P, Rintala J, Oikari A (2012) Agricultural potential of anaerobically digested industrial orange waste with and without aerobic post-treatment. Environ Technol 33:85–94

    PubMed  CAS  Google Scholar 

  • Khallel R, Reddy KR, Overcash MR (1981) Changes in soil physical properties due to organic waste applications: a review. J Environ Qual 10:133–141. doi:10.2134/jeq1981.00472425001000020002x

    Google Scholar 

  • Kirchmann H, Bernal MP (1997) Organic waste treatment and C stabilization efficiency. Soil Biol Biochem 29:1747–1753. doi:10.1016/S0038-0717(97)00065-5

    CAS  Google Scholar 

  • Kluge R, Wagner W, Mokry M, Dederer M et al (2008) Final report of the project “Inhaltsstoffe von Garprodukten und Moglichkeiten zu ihrer geordneten landwirtschaftlichen Verwertung”. http://www.landwirtschaftmlr.badenwuerttemberg.de/servlet/PB/show/1235603_l1/ltz_Projektbericht. Accessed Feb 2009

  • Komilis DP, Ham RK (2003) The effects of lignin and sugars to the aerobic decomposition of solid wastes. Waste Manag 23:419–423. doi:10.1016/S0956-053X(03)00062-X

    PubMed  CAS  Google Scholar 

  • Krupa SV (2003) Effects of atmospheric ammonia (NH3) on terrestrial vegetation: a review. Environ Pollut 124:179–221. doi:10.1016/S0269-7491(02)00434-7

    PubMed  CAS  Google Scholar 

  • Kruse M, ApSimon HM, Bell JNB (1989) Validity and uncertainty in the calculation of an emission inventory for ammonia arising from agriculture in Great Britain. Environ Pollut 56:237–257. doi:10.1016/0269-7491(89)90040-7

    PubMed  CAS  Google Scholar 

  • Lafleur B, Thiffault E, Pare D, Camire C, Bernier-Cardou M, Masse S (2012) Effects of hog manure application on the nutrition and growth of hybrid poplar (Populus spp.) and on soil solution chemistry in short-rotation woody crops. Agric Ecosyst Environ 155:95–104. doi:10.1016/j.agee.2012.04.002

    Google Scholar 

  • Lam VT, Watanabe T, Phan TT, Khai LTL (2002) A case study: introduction of low-cost biogas digester to small-case farming systems. Japan International Research Centre for Agricultural Sciences (JIRCAS). Working report 26, pp 65–72

  • Larsen T, Luxhoi J, Magid J, Jensen LS, Krogh PH (2007) Properties of anaerobically digested and composted municipal solid waste assessed by linking soil mesofauna dynamics and nitrogen modeling. Biol Fertil Soils 44:59–68. doi:10.1007/s00374-007-0178-x

    Google Scholar 

  • Leege PB, Thompson WH (1997) Test methods for the examination of composting and compost. The US Composting Council, Bethesda

    Google Scholar 

  • Lemke RL, Izaurralde RC, Malhi SS, Arsha MA, Nyborg M (1998) Nitrous oxide emissions from agricultural soils of the boreal and parkland regions of Alberta. Soil Sci Soc Am J 62:1096–1102. doi:10.2136/sssaj1998.03615995006200040034x

    CAS  Google Scholar 

  • Liu D, Christians N (1994) Isolation and identification of root-inhibiting compounds from corn gluten hydrolysate. J Plant Growth Regul 13:227–230. doi:10.1007/BF00226041

    CAS  Google Scholar 

  • Loria ER, Sawyer JE (2005) Extractable soil phosphorus and inorganic nitrogen following application of raw and anaerobically digested swine manure. Agron J 97:879–885. doi:10.2134/agronj2004.0249

    Google Scholar 

  • Loria ER, Sawyer JE, Barker DW, Lundvall JP, Lorimor JC (2007) Use of anaerobically digested swine manure as a nitrogen source in corn production. Agron J 99:1119–1129. doi:10.2134/agronj2006.0251

    Google Scholar 

  • Luste S, Luostarinen S (2010) Anaerobic co-digestion of meat-processing by-products and sewage sludge. Effect of hygienization and organic load rate. Bioresour Technol 101:2657–2664. doi:10.1016/j.biortech.2009.10.071

    PubMed  CAS  Google Scholar 

  • MAFF (1995) Fertiliser recommendations for agricultural and horticultural crops (RB209), 6th edn. MAFF, Her Majesty’s Stationery Office, London

    Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic, San Diego

    Google Scholar 

  • Martin JH (2004) A Comparison of Dairy Cattle Manure Management with and without Anaerobic Digestion and Biogas Utilization. Report for the AgSTAR Program, U.S. Environmental Protection Agency, 2004, pp. 58. Available at: http://www.ncgreenpower.org/documents/nydairy2003.pdf. Accessed 18 Jan 2013

  • Masse D, Gilbert Y, Topp E (2011) Pathogen removal in farm-scale psychrophilic anaerobic digesters processing swine manure. Bioresour Technol 102:641–646. doi:10.1016/j.biortech.2010.08.020

    PubMed  CAS  Google Scholar 

  • Matsunaka T, Sawamoto T, Ishimura H, Takakura K, Takekawa A (2006) Efficient use of digested cattle slurry from biogas with respect to nitrogen recycling in grassland. Int Congr Ser 1293:242–250

    CAS  Google Scholar 

  • Mattila PK, Joki-Tokola E, Tanni R (2003) Effect of treatment and application technique of cattle slurry on its utilization by ley: II. Recovery of nitrogen and composition of herbage yield. Nutr Cycl Agroecosyst 65:231–242

    CAS  Google Scholar 

  • McConnell DD, Shiralipour A, Smith WH (1993) Compost application improves soil physical properties. Biocycles 34:61–63

    CAS  Google Scholar 

  • McLachlan KL, Chong C, Voroney RP, Liu HW, Holbein BE (2004) Assessing the potential phytotoxicity of digestates during processing of municipal solid waste by anaerobic digestion; a comparison to aerobic digestion. In: Bertschinger L, Anderson JD (eds) Sustainability of horticultural systems, Acta Hort (ISHS) 638, pp 225–230

  • McMurry PH, Takano H, Anderson GR (1983) Study of the ammonia (gas)–sulphuric acid (aerosol) reaction rate. Environ Sci Technol 17:347–352. doi:10.1021/es00112a008

    CAS  Google Scholar 

  • Metz B, Davidson OR, Bosh PR, Dave R, Meyer LA (2007) Climate change 2007: mitigation. Contribution of working group III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge

    Google Scholar 

  • Michalzik B, Kalbitz K, Park JH, Solinger S, Matzner E (2001) Fluxes and concentrations of dissolved organic carbon and nitrogen—a synthesis for temperate forests. Biogeochem 52:173–205

    Google Scholar 

  • Misselbrook TH, Van Der Weerden TJ, Pain BF, Jarvis SC, Chambers BJ, Smith KA, Phillips VR, Demmers TGM (2000) Ammonia emission factors for UK agriculture. Atmos Environ 34:871–880. doi:10.1016/S1352-2310(99)00350-7

    CAS  Google Scholar 

  • Möller K, Müller T (2012) Effects of anaerobic digestion on digestate nutrient availability and crop growth: a review. Eng Life Sci 12:242–257. doi:10.1002/elsc.201100085

    Google Scholar 

  • Möller K, Stinner W (2009) Effects of different manuring systems with and without biogas digestion on soil mineral nitrogen content and on gaseous nitrogen losses (ammonia, nitrous oxides). Eur J Agron 30:1–16. doi:10.1016/j.eja.2008.06.003

    Google Scholar 

  • Möller K, Stinner W, Deuker A, Leithold G (2008) Effects of different manuring systems with and without biogas digestion on nitrogen cycle and crop yield in mixed organic farming systems. Nutr Cycl Agroecosyst 82:209–232. doi:10.1007/s10705-008-9196-9

    Google Scholar 

  • Möller K, Schulz R, Müller T (2010) Substrate inputs, nutrient flows and nitrogen loss of two centralized biogas plants in southern Germany. Nutr Cycl Agroecosyst 87:307–325. doi:10.1007/s10705-009-9340-1

    Google Scholar 

  • Morris HD, Pierre WH (1947) The effect of calcium, phosphorus, and iron on the tolerance of lespediza to manganese toxicity in culture solutions. Proc Soil Sci Soc Am 12:382–386

    Google Scholar 

  • Mosier AR, Kroeze C, Nevison C, Oenema O, Seitzinger S, van Cleemput O (1998a) Closing the global N2O budget: nitrous oxide emissions through the agricultural nitrogen cycle. Nutr Cycl Agroecosyst 52:225–248. doi:10.1023/A:1009740530221

    CAS  Google Scholar 

  • Mosier AR, Duxbury JM, Freney JR, Heinemeyer O, Minami K (1998b) Assessing and mitigating N2O emissions from agricultural soils. Climate Change 40:7–38. doi:10.1023/A:1005386614431

    CAS  Google Scholar 

  • Mshandete A, Bjornssona L, Kivaisi AK, Rubindamayugi ST, Mattiasson B (2005) Enhancement of anaerobic batch digestion of sisal pulp waste by mesophilic aerobic pre-treatment. Water Res 39:1575. doi:10.1016/j.watres.2004.11.037

    Google Scholar 

  • Mulla DJ, Birr AS, Randall G, Moncerief J, Schmitt M, Sekely A, Kerre E (2001) Impacts of animal agriculture on water quality: technical work paper. Minnesota Environmental Quality Board, Minnesota Planning (Agency), St. Paul

    Google Scholar 

  • Murto M, Bjornsson L, Mattiasson B (2004) Impact of food industrial waste on anaerobic co-digestion of sewage sludge and pig manure. J Environ Manag 70:101–107. doi:10.1016/j.jenvman.2003.11.001

    CAS  Google Scholar 

  • Newton GL, Hubbard RK, Johnson JC,. Davis JG, Vellidis G, Lowrance R, Johnson AW, Williams RG, Dove CR (1994) Utilization and environmental consequences of land application of liquid manure in the southeastern United States coastal plain. In: Proc. Great Plains Anim. Waste Conf. Confined Anim. Prod. Water Quality. Balancing Anim. Prod. and the Environ. Great Plains Agric. Council publ. no. 151, pp 66–73

  • Ni K, Pacholski A, Gericke D, Kage H (2012) Analysis of ammonia losses after application of biogas slurries by an empirical model. J Plant Nutr Soil Sci 175:253–264. doi:10.1002/jpln.201000358

    CAS  Google Scholar 

  • Nicholson FA, Chambers BJ, Smith KA (1996) Nutrient composition of poultry manures in England and Wales. Bioresour Technol 58:279–284. doi:10.1016/S0960-8524(97)86087-7

    CAS  Google Scholar 

  • Nkoa R, Coulombe J, Desjardins Y, Tremblay N (2001) Towards optimization of growth via nutrient supply phasing: nitrogen supply phasing increases broccoli (Brassica oleracea var italica) growth and yield. J Exp Bot 52:821–827

    PubMed  CAS  Google Scholar 

  • NRC (2002) Air emissions from animal feeding operations: current knowledge, future needs. Final report, National Research Council. The National Academies, Washington, DC

  • Ökologischen L, Bodenschutz (2008) Einsatz von Garresten aus der Biogasproduktion als Dungemittel. LfL-Information, Institut fur Agrarokologie

  • Odgers E (1991) Regulations bolster voluntary programs for cleanup of agricultural nonpoint “bad actors” in Wisconsin. In: National livestock, poultry and aquaculture waste management: Proc. Natl. Workshop. ASAE Publ. 03-92. ASAE, St. Joseph, pp 273–277

  • Odlare M, Pell M, Svensson K (2008) Changes in soil chemical and microbiological properties during 4 years of application of various organic residues. Waste Manag 28:1246–1253. doi:10.1016/j.wasman.2007.06.005

    PubMed  CAS  Google Scholar 

  • Oenema O, Tamminga S (2005) Nitrogen in global animal production and management options for improving nitrogen use efficiency. Sci China Ser C Life Sci 48:871–887

    CAS  Google Scholar 

  • Olsen JE, Larsen H (1987) Bacterial decimation times in anaerobic digestions of animal slurries. Biol Wastes 21:153–168. doi:10.1016/0269-7483(87)90121-2

    CAS  Google Scholar 

  • Olsen JE, Jorgensen JB, Nansen (1985) On the reduction of Mycobacterium avium subsp. Paratuberculosis in bovine slurry subjected to batch mesophilic or thermophilic anaerobic-digestion. Agric Wastes 13:273–280. doi:10.1016/0141-4607(85)90052-6

    Google Scholar 

  • Ottoson JR, Schnurer A, Vinneras B (2008) In situ ammonia production as a sanitation agent during anaerobic digestion at mesophilic temperature. Lett Appl Microbiol 46:325–330. doi:10.1111/j.1472-765X.2007.02317.x

    PubMed  CAS  Google Scholar 

  • Paavola T, Rintala J (2008) Effects of storage on characteristics and hygienic quality of digestates from four co-digestion concepts of manure and biowaste. Bioresour Technol 99:7041–7050. doi:10.1016/j.biortech.2008.01.005

    PubMed  CAS  Google Scholar 

  • Pagliai M, Guidi G, Lamarca M, Giachetti M, Luchamante G (1981) Effects of sewage sludges and composts on soil porosity and aggregation. J Environ Qual 10:556–561. doi:10.2134/jeq1981.00472425001000040028x

    Google Scholar 

  • Pahlsson AMB (1989) Toxicity of heavy metals (Cu, Zn, Cd, Pb) to vascular plants. Wat Air Pollut 47:287–319. doi:10.1007/BF00279329

    Google Scholar 

  • Pain BF, Misselbrook TH, Clarkson CR, Rees YJ (1990) Odour and ammonia emissions following the spreading of anaerobically digested pig slurry on grassland. Biol Wastes 34:259–267. doi:10.1016/0269-7483(90)90027-P

    CAS  Google Scholar 

  • Parawira W, Murto M, Zvauya R, Mattiasson B (2004) Anaerobic batch digestion of solid potato waste alone and in combination with sugar beet leaves. Renew Energy 29:1811–1823. doi:10.1016/j.renene.2004.02.005

    CAS  Google Scholar 

  • Pell AN (1997) Manure and microbes: public and animal health problem? J Dairy Sci 80:2673–2681. doi:10.3168/jds.S0022-0302(97)76227-1

    PubMed  CAS  Google Scholar 

  • Pepper IL, Brooks JP, Gerba CP (2006) Pathogens in biosolids. Adv Agron 90:1–41. doi:10.1016/S0065-2113(06)90001-7

    Google Scholar 

  • Petersen SO (1999) Nitrous oxide emissions from manure and inorganic fertilizers applied to spring barley. J Environ Qual 28:1610–1618. doi:10.2134/jeq1999.00472425002800050027x

    CAS  Google Scholar 

  • Pitcairn CER, Leith ID, Sheppard LJ, Sutton MA, Fowler D, Munro RC, Tang S, Wilson D (1998) The relationship between nitrogen deposition, species composition and foliar nitrogen concentrations in woodland flora in the vicinity of livestock farms. Environ Pollut 102:41–48. doi:10.1016/S0269-7491(98)80013-4

    CAS  Google Scholar 

  • Plymforshell L (1995) Survival of salmonellas and Ascaris suum eggs in a thermophilic biogas plant. Acta Vet Scand 36:79–85

    CAS  Google Scholar 

  • Pötsch EM (2004) Abschlussbericht zum Forschungsprojekt BAL 2941. Nährstoffgehalt von Gärrückständen aus landwirtschaftlichen Biogasanlagen und deren Einsatz im Dauergrünland - Nutrient content of fermentation residues from agricultural biogas systems and their utilization on permanent grassland. http://www.raumberg-gumpenstein.at/c/index.php?option=com_docman&task=doc_view&gid=1442&itemid=100014. Accessed 3 Oct 2013

  • Poetsch EM, Pfundtner E, Much P (2004) Nutrient content and hygienic properties of fermentation residues from agricultural biogas plants. In: Lúscher A, Kessler W, Huguenin O, Lobsiger M, Millar N, Suter D (eds) Land use systems in grassland dominated regions. Proceedings of the 20th General Meeting of the European Grassland Federation, Luzern, Switzerland, 21–24 June 2004, pp. 1055–1057

  • Poggi-Varaldo J, Trejo-Espino G, Fernandez-Villagomez G, Esparza-Garcia F, Caffarel-Mendez S, Rinderknecht-Seijas N (1999) Quality of anaerobic compost from paper mill and municipal solid wastes for soil amendment. Water Sci Technol 40:179–186. doi:10.1016/S0273-1223(99)00716-7

    CAS  Google Scholar 

  • Poole HA, Sheehnan TJ (1980) Mineral nutrition of orchids. In: Arditti J (ed) Orchid biology: reviews and perspectives II. Cornell University Press, Ithaca, pp 197–211

  • PRE/630/2011 (2011) Orden de 23 de marzo, por la que se modifican los anexos I, II, III, IV, V, y VI del Real Decreto 824/2005, de 8 de junio, sobre productos fertilizantes. BOE 2011 72:31871–31910

  • Provenzano MR, Iannuzi G, Fabbri C, Senesi N (2011) Qualitative characterization and differentiation of digestates from different biowastes using FTIR and fluorescence spectroscopies. J Environ Prot 2:83–89. doi:10.4236/jep.2011.21009

    CAS  Google Scholar 

  • Qi X, Zhang S, Wang Y, Wang R (2005) Advantages of the integrated pig–biogas–vegetable greenhouse system in North China. Ecol Eng 24:177–185. doi:10.1016/j.ecoleng.2004.11.001

    Google Scholar 

  • Ravishankara AR, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125. doi:10.1126/science.1176985

    PubMed  CAS  Google Scholar 

  • Reddacliff LA, Vidali A, Whittington RJ (2003) The effect of decontamination protocols on the number of sheeps strain Mycobacterium avium subsp. Paratubercolosis isolated from tissues and faeces. Vet Microbiol 95:271–282. doi:10.1016/S0378-1135(03)00181-0

    PubMed  CAS  Google Scholar 

  • Risk N, Snider D, Wagner-Riddle C (2013) Mechanisms leading to enhanced soil nitrous oxide fluxes induced by freeze–thaw cycles. Can J Soil Sci 93:401–414. doi:10.4141/cjss2012-071

    CAS  Google Scholar 

  • Rivard CJ, Rodriguez JB, Nagle NJ, Self JR, kay BD, Soltanpour PN, Nieves RA (1995) Anaerobic digestion of municipal solid waste. Appl Biochem Biotechnol 51(52):125–135. doi:10.1007/BF02933417

    Google Scholar 

  • Robson AD, O’Hara GW, Abbott LK (1981) Involvement of phosphorus in nitrogen fixation by subterranean clover (Tritifolium subterraneum L.). Aust J Plant Physiol 8:427–436. doi:10.1071/PP9810427

    CAS  Google Scholar 

  • Rochette P, van Bochov E, Prevost D, Angers DA, Cote D, Bertrand N (2000) Soil carbon and nitrogen dynamics following application of pig slurry for the 19th consecutive years: II. Nitrous oxide fluxes and mineral nitrogen. Soil Sci Soc Am J 64:1396–1403. doi:10.2136/sssaj2000.6441396x

    CAS  Google Scholar 

  • Rubaek GH, Henriksen K, Petersen J, Rasmussen B, Sommer SG (1996) Effects of application technique and anaerobic digestion on gaseous loss from animal slurry applied to ryegrass (Lolium perenne). J Agric Sci 126:481–492. doi:10.1017/S0021859600075572

    Google Scholar 

  • Ryden JC, Whitehead DC, Lockyer DR, Thompson RB, Skinner JH, Garwood EA (1987) Ammonia emission from grassland and livestock production systems in the UK. Environ Pollut 48:173–184. doi:10.1016/0269-7491(87)90032-7

    PubMed  CAS  Google Scholar 

  • Sahlstrom L (2003) A review of survival of pathogenic bacteria in organic waste used in biogas plants. Bioresour Technol 87:161–166. doi:10.1016/S0960-8524(02)00168-2

    PubMed  CAS  Google Scholar 

  • Sahlstrom L, Aspan A, Bagge E, Danielsson-Tham ML, Albihn A (2004) Bacterial pathogen incidences in sludge from Swedish sewage treatment plants. Water Res 38:1989–1990. doi:10.1016/j.watres.2004.01.031

    PubMed  CAS  Google Scholar 

  • Sahm H (1981) Biologie der Methan-Bildung (Biology of methane formation). Chemie Ingenieur Technik 53:854–863. doi:10.1002/cite.330531105

    CAS  Google Scholar 

  • Sanchez M, Gomez X, Barriocanal G, Cuetos MJ, Moran A (2008) Assessment of the stability of livestock farm wastes treated by anaerobic digestion. Int Biodeterior Biodegrad 62:421–426. doi:10.1016/j.ibiod.2008.04.002

    CAS  Google Scholar 

  • Sandars DL, Audsley E, Caňete C, Cumby TR, Scotford IM, Williams AG (2003) Environmental benefits of livestock manure management practices and technology by life cycle assessment. Biosyst Eng 84:267–270. doi:10.1016/S1537-5110(02)00278-7

    Google Scholar 

  • Sanderson MG, Collins WJ, Johnson CE, Derwent RG (2006) Present and future acid deposition to ecosystems: the effect of climate change. Atmos Environ 40:1275–1283. doi:10.1016/j.atmosenv.2005.10.031

    CAS  Google Scholar 

  • Schattauer A, Abdoun E, Weiland P, Plöchl M, Heiermann M (2011) Abundance of trace elements in demonstration biogas plants. Biosyst Eng 108:57–65. doi:10.1016/j.biosystemseng.2010.10.010

    Google Scholar 

  • Schievano A, Adani F, Tambone F, D’Imporzano G, Scaglia B, Genevini PL (2009) What is digestate? In: Adani F, Schievano A, Boccasile G (eds) Anaerobic digestion: opportunities for agriculture and environment. Lombardia, Milan, pp 7–18

    Google Scholar 

  • Schnurer A, Schnurer J (2006) Fungal survival during anaerobic digestion of organic household waste. Waste Manag 26:1205–1211. doi:10.1016/j.wasman.2005.09.007

    PubMed  Google Scholar 

  • Sidhu J, Gibbs RA, Ho GE, Unkovitch I (2001) The role of indigenous microorganisms in suppression of Salmonella regrowth in composted biosolids. Water Res 35:913–920. doi:10.1016/S0043-1354(00)00352-3

    PubMed  CAS  Google Scholar 

  • Siebert S (2008) Quality requirements and quality assurance of digestion residuals in Germany. In: ECN/ORBIT workshop The Future of Anaerobic Digestion of Organic Waste in Europe. Nuremberg, Germany

  • Siebert S, Thelen-Jüngling M, Kehres B (2008) Development of quality assurance and quality characteristics of composts and digestates in Germany. In: Rodic-Wiersma L, Barth J, Bidlingmaier W, de Bertoldi M, Diaz LF (eds) 6th International conference ORBIT 2008—Moving Organic Waste Recycling Towards Resource Management and Biobased Economy. Wageningen, the Netherlands, October 13–15, 2008, pp 1–12

  • Slana I, Pribylova R, Kralova A, Pavlik I (2011) Persistence of Mycobacterium avium subsp. Paratubercolosis at a farm-scale biogas plant supplied with manure from paratuberculosis-affected dairy cattle. Appl Environ Microbiol 77:3115–3119. doi:10.1128/AEM.02407-10

    PubMed Central  PubMed  CAS  Google Scholar 

  • Smet E, Van Langenhore H, De Bo IZ (1998) The emission of volatile compounds during the aerobic and the combine anaerobic/aerobic composting of biowastes. Atmos Environ 33:1295–1303. doi:10.1016/S1352-2310(98)00260-X

    Google Scholar 

  • Snell-Castro R, Gordon JJ, Delgenes JP, Dabert P (2005) Characterisation of the microbial diversity in a pig manure storage pit using small subunit rDNA sequence analysis. FEMS Microbiol Ecol 52:229–230. doi:10.1016/j.femsec.2004.11.016

    PubMed  CAS  Google Scholar 

  • Somasundaram E, Amanullahaiyapuri MM, Thirukkumaran K, Sathyamoorthi K (2007) Influence of organic sources of nutrients on the yield and economics of crops under maize based cropping system. J Appl Sci Res 3:1774–1777

    Google Scholar 

  • Sommer SG, Hutchings NJ (2001) Ammonia emission from applied manure and its reduction—invited paper. Eur J Agron 15:1–15. doi:10.1016/S1161-0301(01)00112-5

    CAS  Google Scholar 

  • Spencer JL, Guan J (2004) Public health implications related to spread of pathogens in manure from livestock and poultry operations. In: Spencer JFT, Ragout de Spencer AL (eds) Public health microbiology: methods and protocols. Humana, Totowa, pp 503–515

    Google Scholar 

  • Stabnikova O, Goh WK, Ding HB, Tay JH, Wang JY (2005) The use of sewage sludge and horticultural waste to develop artificial soil for plant cultivation in Singapore. Bioresour Technol 96:1073–1080. doi:10.1016/j.biortech.2004.09.024

    PubMed  CAS  Google Scholar 

  • Sutka RL, Ostrom NE, Ostrom PH, Gandhi H, Breznak JA (2003) Nitrogen isotopomer site preference of N2O produced by Nitrosomonas europea and Methylococcus capsulatus Bath. Rapid Commun Mass Spectrom 17:738–745. doi:10.1002/rcm.968

    PubMed  CAS  Google Scholar 

  • Svensson K, Odlare M, Pell M (2004) The fertilizing effect of compost and biogas residues from source separated household waste. J Agric Sci 142:461–467. doi:10.1017/S0021859604004514

    CAS  Google Scholar 

  • Svoboda N, Taube F, Wienforth B, Kluβ C, Kage H, Herrmann A (2013a) Nitrogen leaching losses after biogas residue application to maize. Soil Tillage Res 130:69–80. doi:10.1016/j.still.2013.02.006

    Google Scholar 

  • Svoboda N, Taube F, Wienforth B, Kluβ C, Wienforth B, Kage H, Ohl S, Hartung E, Herrmann A (2013b) Crop production for biomass and water protection. A trade-off? Agric Ecosyst Environ 177:36–47. doi:10.1016/j.agee.2013.05.024

    CAS  Google Scholar 

  • Tambone F, Genevini P, D’Imporzano G, Adani F (2009) Assessing amendment properties of digestate by studying the organic matter composition and the degree of biological stability during the anaerobic digestion of the organic fraction of MSW. Bioresour Technol 100:3140–3142. doi:10.1016/j.biortech.2009.02.012

    PubMed  CAS  Google Scholar 

  • Tambone F, Scaglia B, D’Imporzano G, Schievano A, Salati V, Adani F (2010) Assessing amendment and fertilizing properties of digestates from anaerobic digestion through a comparative study with digested sludge and compost. Chemosphere 81:577–583. doi:10.1016/j. chemosphere .2010.08.034

    PubMed  CAS  Google Scholar 

  • Tang IN (1980) On the equilibrium partial pressure of nitric acid and ammonia in the atmosphere. Atmos Environ 14:819–828. doi:10.1016/0004-6981(80)90138-9

    CAS  Google Scholar 

  • Tang IN, Munkelwitz HR (1977) Aerosol growth studies III. Ammonium bisulfate aerosols in a moist atmosphere. J Aerosol Sci 8:321–330. doi:10.1016/0021-8502(77)90019-2

    CAS  Google Scholar 

  • Tani M, Sakamoto N, Kishomoto T, Umetsu K (2006) Utilization of anaerobically digested slurry combined with other waste following application to agricultural land. Int Congr Ser 1293:331. doi:10.1016/j.ics.2006.03.013

    Google Scholar 

  • Teglia C, Tremier A, Martel JL (2011a) Characterization of solid digestates: part 1, review of existing indicators to assess solid digestates agricultural use. Waste Biomass Valor 2:43–58. doi:10.1007/s12649-010-9051-5

    Google Scholar 

  • Teglia C, Tremier A, Martel JL (2011b) Characterization of solid digestates: part 2, assessment of the quality and suitability for composting of six digested products. Waste Biomass Valor 2:113–126. doi:10.1007/s12649-010-9059-x

    CAS  Google Scholar 

  • Terhoeven-Urselmans T, Scheller E, Raubuch M, Ludwig B, Joergensen RG (2009) CO2 evolution and N mineralization after biogas slurry application in the field and its yield effect on spring barley. Appl Soil Ecol 42:297–300. doi:10.1016/j.apsoil.2009.05.012

    Google Scholar 

  • Thornton SF, McManus J (2002) Application of organic carbon and nitrogen stable isotope and C/N ratios as source indicators of organic matter provenance in estuarine systems: evidence from the Tay Estuary, Scotland. Estuar Coast Shelf Sci 38:219–233. doi:10.1006/ecss.1994.1015

    Google Scholar 

  • Tietjen C (1975) From biodung to biogas—historical review of European experience. In: Jewell WJ (ed) Energy, agriculture, and waste management. Ann Arbor Science, Cornell, p 274

    Google Scholar 

  • Tipping PJ (1996) Centralised anaerobic digestion: review of environmental effects. MAFF contract CSA 2730. MAFF, London

    Google Scholar 

  • Tiquia SM, Tam NFY, Hodgkiss IJ (1996) Effects of composting on phytotoxicity of spent pig manure sawdust litter. Environ Pollut 93:249–256. doi:10.1016/S0269-7491(96)00052-8

    PubMed  CAS  Google Scholar 

  • Tiwari TN, Tiwari KN, Upadhyay RM (2000) Effect of crop residues and biogas slurry incorporation in wheat on yield and soil fertility. J Ind Soc Soil Sci 48:515–520

    Google Scholar 

  • Vallejo A, Skiba UM, Garcia-Torres L, Arce A, Lopez-Fernandez S, Sanchez-Martin L (2006) Nitrous oxides emission from soil bearing a potato crop as influenced by fertilization with treated pig slurries and composts. Soil Biol Biochem 38:2782–2793. doi:10.1016/j.soilbio.2006.04.040

    CAS  Google Scholar 

  • Van der Eerben LJM, de Visser PHB, van Dijk CJ (1998) Risk of damage to crops in the direct neighborhood of ammonia sources. Environ Pollut 102:49–53. doi:10.1016/S0269-7491(98)80014-6

    Google Scholar 

  • Voća N, Kricka T, Cosic T, Rupic V, Jukic Z, Kalambura S (2005) Digested residues as a fertilizer after the mesophilic process of anaerobic digestion. Plant Soil Environ 51:262–266

    Google Scholar 

  • Wachendorf M, Büchter M, Volkers K, Bobe J, Rave G, Loges R, Taube F (2006) Performance and environmental effects of forage production on sandy soils. V. Impact of grass understorey, slurry application and mineral N fertilizer on nitrate leaching under maize for silage. Grass Forage Sci 61:243–252. doi:10.1111/j.1365-2494.2006.00528.x

    CAS  Google Scholar 

  • Wagner-Riddle C, Thurtell GW, Kidd GE, Beauchamp EG, Sweetman R (1997) Estimates of nitrous oxide emissions from agricultural fields over 28 months. Can J Soil Sci 77:135–144. doi:10.4141/S96-103

    CAS  Google Scholar 

  • Warneck P (2000) Chemistry of the natural atmosphere, 2nd edn. Academic, New York

    Google Scholar 

  • Watcharasukarn M, Kaparaju P, Steyer JP, Krogfelt KA, Angelidaki I (2009) Screening Escherichia coli, Enteroccocus faecalis, and Clostridium perfringens as indicator organisms in evaluating pathogen-reducing capacity in biogas plants. Microb Ecol 58:221–230. doi:10.1007/s00248-009-9497-9

    PubMed  Google Scholar 

  • Weiland P (2010) Biogas production: current state and perspectives. Appl Microbiol Biotechnol 85:849–860. doi:10.1007/s00253-009-2246-7

    PubMed  CAS  Google Scholar 

  • Wienhold BJ, Andrews SS, Karlen DL (2004) Soil quality: a review of the science and experiences in the USA. Environ Geochem Health 26:89–95. doi:10.1023/B:EGAH.0000039571.59640.3c

    PubMed  CAS  Google Scholar 

  • Williams JH, Guidi G, L’Hermite (1985) Long-term effects of sewage sludge and farm slurries applications. Elsevier, Barking

    Google Scholar 

  • Wong MH, Cheung YH, Cheung CL (1983) The effect of ammonia and ethylene oxide in animal manure and sewage sludge on the seed germination and root elongation of Brassica parachinensis. Environ Poll Ser A 30:109–123. doi:10.1016/0143-1471(83)90008-9

    Google Scholar 

  • Wong JWC, Li GX, Wong MH (1996) The growth of Brassica chinensis in heavy metal-contaminated sewage sludge compost from Hong Kong. Bioresour Technol 58:309–313. doi:10.1016/S0960-8524(96)00121-6

    CAS  Google Scholar 

  • Wrage N, Velthof GL, van Beusichem ML, Oenema O (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem 33:1723–1732. doi:10.1016/S0038-0717(01)00096-7

    CAS  Google Scholar 

  • Wulf S, Maeting M, Clemens J (2002a) Application technique and slurry-co-fermentation effects on ammonia, nitrous oxide, and methane emissions after spreading: I. Ammonia volatilization. J Environ Qual 31:1789–1794. doi:10.2134/jeq2002.1789

    PubMed  CAS  Google Scholar 

  • Wulf S, Maeting M, Clemens J (2002b) Application technique and slurry-co-fermentation effects on Ammonia, nitrous oxide, and methane emissions after spreading: II. Greenhouse gas emissions. J Environ Qual 31:1795–1801. doi:10.2134/jeq2002.1795

    PubMed  CAS  Google Scholar 

  • Zaoui R (1988) Valorga digestion process. In: Alston, YR, Richards GE (eds) Proceeding of international conference on landfill gas and anaerobic digestion of solid waste. Chester, England. Harwell Laboratory, UKAEA, Oxon. 0X11 ORA, pp 481–500

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Correspondence to Roger Nkoa.

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Nkoa, R. Agricultural benefits and environmental risks of soil fertilization with anaerobic digestates: a review. Agron. Sustain. Dev. 34, 473–492 (2014). https://doi.org/10.1007/s13593-013-0196-z

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