Nitrogen balance in a stockless organic cropping system with different strategies for internal N cycling via residual biomass

Nitrogen balance in a stockless organic cropping system with different strategies for internal N... Nutr Cycl Agroecosyst (2018) 112:165–178 https://doi.org/10.1007/s10705-018-9935-5(0123456789().,-volV)(0123456789().,-volV) ORIGINAL ARTICLE Nitrogen balance in a stockless organic cropping system with different strategies for internal N cycling via residual biomass . . Tora Ra˚berg Georg Carlsson Erik Steen Jensen Received: 6 July 2017 / Accepted: 4 July 2018 / Published online: 31 July 2018 The Author(s) 2018 Abstract A major future challenge in agriculture is second study year. The N balance ranged between -1 to reduce the use of new reactive nitrogen (N) while - 9.9 and 24 kg N ha , with more positive budgets maintaining or increasing productivity without caus- in AD and BR than in IS. The storage of biomass for ing a negative N balance in cropping systems. We reallocation in spring led to an increasing accumula- investigated if strategic management of internal tion of N in the BR and AD systems from one year to biomass N resources (green manure ley, crop residues another. These strategies also provide an opportunity and cover crops) within an organic crop rotation of six to supply the crop with the N when most needed, main crops, could maintain the N balance. Two years thereby potentially decreasing the risk of N losses of measurements in the field experiment in southern during winter. Sweden were used to compare three biomass man- agement strategies: anaerobic digestion of ensiled Keywords Anaerobic digestion  Arable and biomass and application of the digestate to the non- horticultural crops  N balance  N fixation  Soil and legume crops (AD), biomass redistribution as silage to residue N  Strategic biomass N management non-legume crops (BR), and leaving the biomass in situ (IS). Neither aboveground crop N content from Abbreviations soil, nor the proportion of N derived from N fixation AD Anaerobic digestion in legumes were influenced by biomass management BNF Biological nitrogen fixation treatment. On the other hand, the allocation of N-rich BR Biomass redistribution silage and digestate to non-legume crops resulted in IS In situ -1 higher N fixation in AD and BR (57 and 58 kg ha %Ndfa Proportion (%) of accumulated nitrogen -1 -1 -1 year ), compared to IS (33 kg ha year ) in the derived from nitrogen fixation Electronic supplementary material The online version of Introduction this article (https://doi.org/10.1007/s10705-018-9935-5) con- tains supplementary material, which is available to authorized users. The planetary boundary research highlight the impor- tance of reducing global inputs of new reactive T. Ra˚berg (&)  G. Carlsson  E. S. Jensen nitrogen (N) to ecosystems (Steffen et al. 2015). The Department of Biosystems and Technology, Swedish University of Agricultural Sciences, P.O. Box 103, amounts of N applied as fertiliser in agriculture have 230 53 Alnarp, Sweden not been sufficiently constrained to prevent e-mail: tora.raberg@slu.se 123 166 Nutr Cycl Agroecosyst (2018) 112:165–178 widespread leakage to freshwaters and the atmo- manure ley and cover crop cuttings) in situ is a sphere, with effects on human health, biodiversity and common practice in agriculture, but it may result in climate (Fowler et al. 2013). Organic agriculture, substantial losses of N, if mineralisation and acquisi- compared with conventional, offers benefits such as tion of the following crop is not well synchronised increased cycling of nutrients and lower energy usage (Pang and Letey 1998;Moller et al. 2008a; Mohanty for processing fertilisers of organic origin than for et al. 2013). It may be possible to improve the synthetic fertilisers (Worrell et al. 2000; Vance 2001; synchrony between application of residual biomass N, Rockstro¨m et al. 2009). Consumers today are often N fixation and plant acquisition of N by pre-treating concerned about the environment and/or the chemicals and storing the biomass as silage or as digestate from used in food production, and both supply and demand anaerobic digestion (Gutser et al. 2005; Gunnarsson for certified organic production continue to grow et al. 2011; Frøseth et al. 2014). Ensiling initiates (Mueller and Thorup-Kristensen 2001; Willer and mineralisation, but also conserves the biomass by Schaack 2015). For example, the EU-28 increased its lowering the pH and creating an anaerobic environ- total area cultivated as organic from 5.0 to 11 million ment (Herrmann et al. 2011). Anaerobic digestion of hectares between 2002 and 2015 (Eurostat 2015). This plant material and subsequent use of the residual large-scale conversion of production needs to be met digestate as a fertiliser is of particular interest to with intensified research to ensure that the methods are supply N for non-legume crops in the absence of optimised for high yields and that pollution is animal manure in stockless organic systems (Gu- minimised. naseelan 1997). In general, there is a larger proportion Modern agriculture has increasingly led to special- of plant available N in the digestate compared with in ization in either crop or animal production in entire fresh or ensiled biomass (Weiland 2010). A high level regions, causing limited availability of animal manure of mineral N in the soil will generally decrease both for stockless farms (Schmidt et al. 1999; Mueller and nodulation and N fixation (Streeter and Wong 1988; Thorup-Kristensen 2001; Stinner et al. 2008). Thus, Waterer and Vessey 1993) and thereby make the many arable and horticultural organic farms choose to legume more dependent on soil mineral N. Increased import a considerable amount of concentrated fer- yield and N fixation might be possible by redistribut- tiliser made from by-products of the food industry ing the N rich silage or digestate to non-legume sole (Watson et al. 2002; Wivstad 2009; Colomb et al. crops. It is challenging to balance N inputs in organic 2013). To reduce the need for external fertiliser inputs, farming to ensure long-term soil fertility with high and researchers suggest strategies that could improve soil stable yields, avoiding depletion of the soil N pool and fertility and internal nutrient cycling at the farm level, at the same time avoid a surplus that has negative such as improved residue management, intercropping impacts on the surrounding ecosystem (de Ponti et al. and growing cover crops (Tilman et al. 2002; Bom- 2012; Colomb et al. 2013; Seufert and Ramankutty marco et al. 2013). Cycling of N is central to reduce 2017). the need for production of more reactive N (Bodirsky Calculation of N balance is a tool for expanding the et al. 2014). However, N is often the most limiting understanding of the N cycle and evaluate the effect of nutrient for crop performance in terms of yield and different management practices on the soil-crop N quality, and is needed in larger quantities than any of cycle and the sustainability of N management methods the other essential nutrients (Mengel and Kirkby 1978; (Watson et al. 2002). A N balance can summarise the Sinclair and Horie 1989). To obtain high yield and complex agricultural N cycle by documenting the quality, mineralisation of N from organic fertilisers major flow paths as N enters and emerges from various and SOM needs to be in synchrony with crop pools and leaves the system for various fates (Mei- acquisition. singer et al. 2008). Calculating the N balance at crop, Incorporation of residues from legume cover crops cropping system or farm level is also a valuable tool and forage legumes, containing symbiotically fixed N, for identifying risks of N depletion or build-up of a N improves N supply substantially and is very important surplus, thereby highlighting the potential need for in organic farming systems without livestock, where improved N management. A N balance made for 76 other options for N input are limited. Incorporating organic arable farms in Sweden showed an average N residual biomass (here defined as crop residue, green surplus of 39 kg/ha (Wivstad 2009). The surplus was 123 Nutr Cycl Agroecosyst (2018) 112:165–178 167 Materials and methods mainly due to imported nutrients from digestate, yeast liquid and dried slaughter house waste. Horticultural Study site and soil cropping systems tend to import even more N than arable farms, which results in a N balance with higher The experiment was established in 2012 at the N surpluses (Watson et al. 2002), and is thus prone to a higher risk of N losses. Swedish University of Agricultural Sciences in 0 00 0 00 Alnarp, southern Sweden (5539 21 N, 1303 30 E), The objective of this study was to assess how different strategies for internal N cycling via residual on a sandy loam soil of Arenosol type (Deckers et al. biomass influenced the N balance of a stockless 1998). The field experiment was conducted on organ- organic cropping system, where the input of N was ically certified agricultural land within the SITES limited to biological N fixation, N contained in Lo¨nnstorp field research station, with grass-clover ley seeds/plantlets for crop establishment and atmospheric as the pre-crop. The annual mean atmospheric depo- -1 N deposition. The specific aims were (1) to determine sition of N contributed with a total of 9.4 kg ha -1 year during 2013–2014, in the region where the field whether anaerobic digestion (AD) of the residual biomass from the cropping system, and use of its experiment was situated (SMHI 2016). digestate for N recirculation, would improve the N acquisition in the following crop, compared to the Climatic data corresponding biomass redistribution (BR) of silage or just leaving the biomass in situ (IS) and (2) to test if The region has a typical northern-European maritime strategic management of residual biomass (AD and climate with mild winter and summer temperatures BR) could improve the N balance of the cropping (annual average of 9.3 C and 664 mm precipitation) system. Six main crops, including both arable and (Ra˚berg et al. 2017). horticultural crops, were combined in a field experi- ment with the purpose to study how the soil N Crop rotation acquisition and symbiotic N fixation of the different crops respond to the biomass management strategies. Six different crops in a rotation including different legume species, over-wintering cash and cover crops We used the N balance method as a tool to determine how a biomass management strategy influenced the (Table 1) were studied during 2 years (2013 and risk of depleting or creating surplus of soil N at both 2014). The rotation consisted of the following food individual crop and at the cropping system level, but crops: pea/barley (Pisum sativum L./Hordeum vulgare without considering N emissions to the environment in L.), lentil/oat (Lens culinaris Medik/Avena sativa L.), the calculation. The hypotheses were: I) the amount white cabbage (Brassica oleracea L.), beetroot (Beta and proportion of N fixed in legume crops (legumes vulgaris L.) and winter rye (Secale cereale L.). The sixth main crop was a green manure ley composed of in the green manure ley, lentil (Lens culinaris Medik), pea (Pisum sativum L.), clover (Trifolium pratense L. the following six species in equal proportions: orchard grass (Dactylis glomerata L.), meadow fescue (Fes- and T. repens L.) in cover crop) is greater with AD and BR than in the IS management, II) N acquisition from tuca pratensis L.), timothy grass (Phleum pratense L.), lucerne (Medicago sativa L.), yellow sweet clover soil and residual biomass in non-legume crops is greater in AD than BR and IS, III) the N balance at the (Melilotus officinalis L.) and red clover (Trifolium pratense L.) (Ra˚berg et al. 2017). The green manure cropping system level ranks IS \ BR \ AD, and IV) the total N acquisition originating from soil and added ley was under-sown in pea/barley, cut three times biomass in all crops is on average larger in AD and BR during the year after establishment, and cut again in than in IS. early spring the subsequent year, before establishing white cabbage as the next crop. The herbage was removed in BR and AD and left in situ in IS. Cover crops were included in the rotation after white cabbage (buckwheat, Fagopyrum esculentum Moench/oilseed radish, Raphanum sativus L.) and rye (buckwheat/lacy phacelia, Phacelia tanacetifolia Benth.), and was 123 168 Nutr Cycl Agroecosyst (2018) 112:165–178 Table 1 The main crops Main crop Cover and winter crops and cover crops in the rotation White cabbage Buckwheat/oilseed radish Lentil/oat ? english ryegrass/red and white clover English ryegrass/red and white clover Beet root Winter rye Winter rye Buckwheat/phacelia Pea/barley ? green manure ley Green manure ley Green manure ley Green manure ley under-sown in lentil/oat (ryegrass, Lolium perenne L./ randomly distributed within each block (18 plots). The red clover, Trifolium pratense L./white clover T. reference treatment was a system where all the residual biomass (crop residues, green manure ley repens L.). All six main crops in the rotation were grown during each year of the experiment. Winter rye and cover crops cuttings) was incorporated fresh was replaced by spring barley during the establish- in situ (IS) in the experimental plot (Fig. 1). The IS ment year (2012), since the experiment started in treatment was used as a reference, as it is common spring without any autumn-sown crop from the practice to leave most of the crop residue in the field in previous year. The choice of crops in the rotation organic arable farming (Ogren 1992; Ascard and was based on maximising the cash crop yield and Bunnvik 2008). Two additional biomass management improve the functional diversity to strengthen ecosys- treatments were: (1) ensiling and redistributing all tem services (Ra˚berg et al. 2017). residual biomass (BR) to experimental plots with cabbage, winter rye and beetroot; and (2) all of the Field management residual biomass was ensiled and later anaerobically digested (AD) in a biogas reactor, and the digestate The ley pre-crop was incorporated by inversion tillage was applied to cabbage, winter rye and beetroot, as (tillage depth 25 cm) before the experiment started. described in Ra˚berg et al. (2017). The N supplied to During the field experiment, a non-inversion rotary the crops in each treatment are presented in the cultivator was used mixing the crop residue with soil supplementary material. This design allowed for to a maximum depth of 15 cm. The experimental area -1 received an initial supply of 115 kg N ha of plant- based digestate applied with trailing hoses in spring 2012. No other external fertiliser was added during the field experiment. Crop protection followed the national organic regulations. The weeding was made by hand in the row crops (cabbage and beetroot) in the same way and around the same dates in all treatments. Seed bed preparations was made by harrowing approximately a week before sowing to allow for weeds to germinate, and then weeds were removed by a second harrowing. The cabbage was grown under an insect mesh and hand-sprayed with Bacillus thuringiensis every second week after spotting Lepi- doptera larvae. Fig. 1 Residue management within the crop rotation: (1) Experimental design IS = In situ incorporation, (2) BR = biomass redistributed to the non-leguminous crops grown in pure stand and (3) AD = digested biomass distributed to the non-leguminous crops The field experiment comprised in total 72 experi- grown in pure stand. The residual biomass in IS was applied mental plots measuring 3 9 6 m, distributed in four fresh, in BR it was ensiled prior to field application and in AD it blocks. All six crops and the three treatments were was ensiled and anaerobically digested as a pre-treatment 123 Nutr Cycl Agroecosyst (2018) 112:165–178 169 Calculations and statistics sampling and harvesting of each crop with the three different management strategies in every year. N fixation and N acquisition from soil and added Sampling and harvest biomass The residual biomass was collected and ensiled The N inputs from N fixation was assessed according to the N natural abundance method (Unkovich et al. separately in BR and AD, with harvest from spring until October each year, to allow time for digestion in 1997, 2008), using the lowest observed legume d N- AD. The same strategy was used for the collection of value as b-value in Eq. (1), as recommended by e.g. biomass in BR to make it comparable to AD. The Hansen and Vinther (2001) and Huss-Danell et al. method resulted in a 1-year delay for the use of the (2007). The b-value is defined as a measure of the N May harvest of green manure ley and ryegrass/clover content of the target legume (d N ) when fully in the BR and AD treatments. Measurements of yield dependent on N fixation for its N acquisition (Unkovich et al. 2008). In the present study, the and N content started in 2012 and the last samples were collected in 2015 for two over-wintering crops, samples used as b-value were also included in the calculations of the average N fixation per treatment. green manure ley and ryegrass/clover cover crop. Samples from overwintering crops harvested in May, The N signature of the grasses and weeds grown together with the legumes in the green manure ley, were allocated to the biomass production of the previous year. Since no effects of the biomass intercrops and cover crops were used as reference management treatments could be expected during plants (d N ). ref the establishment year, the study is based on samples 15 15 ðd N  d N Þ ref L and measurements from 2013 to 2014. Average yields %N ¼  100; ð1Þ dfa d N  b ref and N content in harvests during 2012 are listed in supplementary material, Table S2. %N = the proportion of the total N uptake origi- dfa 15 15 All residual biomass (crop residues, green manure nating from N fixation; d N = the N signature of 2 ref ley and cover crops) was weighed before returning it to the grasses and weeds grown together with the 15 15 the field plot (IS) or ensiled for later redistribution (BR legumes; d N = the N signature of the legume; 15 15 and AD), as described in Ra˚berg et al. (2017). b = the N signature of the target legume (d N ) Subsamples from a 0.25 m surface per plot were when fully dependent on N fixation for its N taken for analyses of botanical composition (grouped acquisition. -1 into legumes and non-legumes), N concentration and The amount of N fixed (kg N ha ) in each legume natural abundance of the stable isotope N. After crop was calculated by multiplying %Ndfa with total drying and milling the edible and residual biomass crop N content (N concentration  crop biomass). Soil fractions of each subsample (see Raberg et al. 2017 for N acquisition in legumes, representing N from the soil 15 14 details), the N concentration and N/ N ratio in each N pool as well as from added residual biomass, was fraction was measured with an elemental analyser calculated by subtracting the amount of N fixed from coupled to an isotope ratio mass spectrometer (PDZ the total crop N content in the aboveground plant parts. Europe 20-20, at UC Davies in USA) in legume- For non-legume crops, the amount of N acquired from containing crop mixtures. A Flash 2000 Thermo soil and added biomass was the same as the total Scientific elemental analyser (at SLU, Alnarp, Swe- aboveground crop N content. den) was used for determination of N concentration in each fraction of sole crops. The analyses of these Nitrogen balance subsamples were then used for calculating N fixation, N export in edible fractions and N circulation via The balance of N for the cropping sequences was residual biomass (see below). calculated per crop and as an annual sum of each treatment for the years 2013 and 2014. The N balance was calculated from data on N input and output from the cropping system (Eq. 2, Fig. 2). 123 170 Nutr Cycl Agroecosyst (2018) 112:165–178 Fig. 2 Input and output components of the N balance. The N coming in and leaving from the crop- soil system was quantified, except for the losses of nitrogen (ammonia volatilization, denitrification and N leaching) (dashed arrow) fractions, amounts of N in residual biomass), both on N balance ¼ bnf þ dep þ seed þ biomass added ð2Þ individual crop and on cropping system level (except edible fractionbiomass removed for %Ndfa which was only tested at crop level). These bnf = biological N fixation in current year, calculated ANOVAs were performed using the general linear as described above; dep = atmospheric N deposition; model (GLM) in the Minitab software, assuming block seed = seed N and plantlet N; biomass = N from and treatment as fixed factors. Whenever a significant added added residual biomass from previous year; edible interaction between year and treatment was found, fraction = exported N in the edible fraction of cash treatment effects were again tested for significance crops; biomass = total N from residual biomass separately for each year. removed removed to be circulated succeeding year. The regional measurements of atmospheric N deposition during the time of the field experiments Results -1 -1 added 9.4 kg total N ha year (SMHI 2016), which was divided and allocated on two crops when there Nitrogen acquisition was more than one crop in the same field and in the same year (i.e. main crop and cover crop). The N Total N content in the aboveground parts of the crops -1 -1 contribution from seeds was obtained from measured ranged between 140 and 180 kg ha year (Fig. 3), seed N content for the cereals and grain legumes with no significant difference between the biomass (Table 3), and was calculated from literature for the strategies. non-food seeds and plantlets (Schroeder et al. 1974). The amounts of N added via residual biomass Nitrogen fixation corresponded to the redistribution of ensiled (BR) and digested (AD) biomass from the previous year The total N fixation in leguminous crops constituted (supplementary material, Table S1). The N outputs in 14–26% of total N content in the aboveground plant the balance consisted of the amounts of N exported in parts of all crops, which corresponded to an average of -1 -1 the harvested edible fraction of the cash crops and N 23–40 kg ha year (Fig. 3). The %Ndfa was found exported in residual biomass in AD and BR to be to be in the range 68–98% across all legume species in redistributed in the next growing season. the cropping system, and was not significantly differ- Analyses of variance (ANOVA) were conducted to ent between biomass management treatments test the significance in differences between years (Table 2). The amount of N fixed was higher with (2013 and 2014) and effects of block and treatment BR and AD treatments, compared to IS (p = 0.002) as (IS, BR and AD) on the response variables (%Ndfa, the years were analysed together. The effect was only amounts of N derived from N fixation and from soil significant in 2014 (p = 0.021) (Fig. 3), when the acquisition, amounts of N in export of edible crop years were analysed separately. A large part of the 123 Nutr Cycl Agroecosyst (2018) 112:165–178 171 N acquisition from soil The total N acquisition from soil varied between 110 -1 and 140 kg N ha calculated as an average for the entire crop rotation, and the total N content was significantly higher (p = 0.002) in 2014, compared to 2013 (Fig. 3). Differences between the three biomass residue management methods were small and in most cases non-significant (Fig. 4a and b). The BR treat- ment led to significantly (p \ 0.001) higher soil N acquisition in the cover crop buckwheat/lacy phacelia in both years as compared to IS and AD treatments (Fig. 4). Nitrogen exported in the edible crop fraction Fig. 3 The total mean N content of the crop biomass from the -1 The average N content in the exported edible fractions entire cropping systems in 2013 and 2014 in kg ha . Total N is of the five food crops varied between 49 and presented as a sum of N acquired from the soil and through N -1 fixation. The letters show significant differences between 60 kg ha , with the highest amount exported in rye treatments in N fixation. The error bars represent standard grain and the lowest in pea/barley. The N content in error for each fraction (N = 4 except for ley with N = 3 in 2013) the edible fraction was not affected by the three treatments (Table 3), even if the N supply differed increased N fixation was derived from the legumes of substantially (table in supplementary material). the green manure ley, with a significantly higher (p \ 0.001) N fixation in BR and AD compared to IS Nitrogen in residual biomass in 2014 (Fig. 4b). The amount of N fixation in lentil and pea varied inconsistently between treatments in The total amount of N in residual biomass varied the 2 years. No significant difference between treat- -1 between 97 and 129 kg N ha (Table 4). There was a ments was found for the amount of N fixed in clover significant interaction between treatment and year grown together with ryegrass in the cover crop, which -1 -1 when the total N content of all the crops from the three ranged between 12 and 78 kg N ha year and was systems were compared (p = 0.001), but when each higher in 2013 than in 2014. year was analysed individually there was no signifi- cant difference between the three treatments. In 2013, the green manure ley cuttings constituted 36–40% of the total amount of residual biomass N, and in 2014 the Table 2 The proportion of nitrogen acquired through N BR = biomass redistributed to the non-leguminous crops fixation (%Ndfa) in legumes at different biomass treatments grown in pure stand and (3) AD = digested biomass distributed within the crop rotation: (1) IS = In situ incorporation, (2) to the non-leguminous crops grown in pure stand Crops Ndfa (%) 2013 2014 IS BR AD IS BR AD Lentil 83 ± 3.8 87 ± 7.7 98 ± 1.7 73 ± 3.8 68 ± 11 80 ± 11 Clover 96 ± 0.5 95 ± 2.9 95 ± 1.3 93 ± 3.0 92 ± 1.6 94 ± 0.9 Pea 94 ± 2.1 86 ± 2.1 88 ± 3.7 89 ± 3.5 87 ± 1.6 89 ± 4.5 Green manure ley 74 ± 8.3 85 ± 3.3 83 ± 3.6 76 ± 2.1 81 ± 2.2 81 ± 1.2 Presented as mean ± standard error (N = 4, except for green manure ley 2013 with N = 3) 123 172 Nutr Cycl Agroecosyst (2018) 112:165–178 Fig. 4 Nitrogen content of the aboveground biomass of individual crops (kg N -1 ha ) in 2013 (a) and 2014 (b), presented as mean ± standard error (N = 4 except for ley with N = 3 in 2013). The grey bars represent N acquisition from soil and residual crop biomass, and the white bars represent N fixation of the legumes. IS = In situ incorporation. BR = biomass redistributed to the non-leguminous crops grown in pure stand. AD = digested biomass distributed to the non- leguminous crops grown in pure stand. The error bars represent standard error for each fraction. * = Significance according to ANOVA at p \ 0.05. ** = Significance according to ANOVA at p \ 0.01 part increased to between 49 and 54%. When summed The three crops that were fertilised with biomass in for all biomass resources in the cropping system, the BR and AD resulted in N surplus for the N balance of total N content of the residual biomass increased over both years, with the highest surplus in cabbage with -1 time, regardless of treatment, with an average differ- the BR treatment in 2014 (178 kg ha ). The excep- -1 ence of 19 kg N ha between 2013 and 2014 tion from the surplus results was the winter rye crop (Table 4). with BR treatment in 2014, which resulted in -1 - 8kgha (Fig. 5b). Cabbage, red beet and rye all Nitrogen balance had a negative N balance in IS, ranging from - 36 to -1 - 68 kg ha . The lentil/oat intercrop resulted in a The N balances at the cropping system level was more negative result for all treatments, and most negative -1 positive in 2014 than in 2013 in the BR and AD for AD and BR, from - 37 to - 79 kg ha . The pea/ treatments, when not considering the residual biomass barley intercrop resulted in a surplus of -1 N as a temporary export in the harvest year and input 21–47 kg ha for IS (2014 and 2013 respectively), in the subsequent year (Table 5; Stored biomass not while the balance for BR and AD resulted in 5 to -1 considered as export). - 47 kg ha . The non-legume cover crops had a -1 negative result for BR and AD, - 15 to - 57 kg ha , 123 Nutr Cycl Agroecosyst (2018) 112:165–178 173 Table 3 Nitrogen exported in edible fractions of crops (kg N to the non-leguminous crops grown in pure stand and (3) -1 ha ) at different biomass treatments within the crop rotation: AD = digested biomass distributed to the non-leguminous (1) IS = In situ incorporation, (2) BR = biomass redistributed crops grown in pure stand Crop Nitrogen export in edible fraction 2013 2014 IS BR AD IS BR AD Cabbage 44 ± 5.1 44 ± 8.9 45 ± 4.6 52 ± 2.9 56 ± 5.8 58 ± 6.6 Lentil/oat 67 ± 8.1 81 ± 8.3 70 ± 9.2 53 ± 14 62 ± 9.7 52 ± 7.6 Beetroot 41 ± 15 31 ± 13 51 ± 12 42 ± 4.4 40 ± 6.5 39 ± 4.7 Rye 75 ± 12 84 ± 15 90 ± 12 63 ± 4.0 75 ± 12 60 ± 7.5 Pea/barley 28 ± 11 17 ± 3.8 26 ± 7.9 44 ± 13 67 ± 6.4 35 ± 12 Mean 43 ± 3.2 43 ± 3.5 47 ± 3.0 42 ± 1.5 50 ± 3.8 41 ± 4.0 Presented as mean ± standard error (n = 4). The mean value for the entire cropping system (bottom line) was calculated from 6 ha, even if ley is excluded in the sum, but nevertheless crucial for the production of edible produce in the cropping system -1 Table 4 Nitrogen in residual biomass (kg N ha ) at different leguminous crops grown in pure stand and (3) AD = digested biomass treatments within the crop rotation: (1) IS = In situ biomass distributed to the non-leguminous crops grown in pure incorporation, (2) BR = biomass redistributed to the non- stand -1 Crop N in residual biomass (kg ha ) 2013 2014 IS BR AD IS BR AD Cabbage 36.3 ± 3.29 33.7 ± 4.36 46.3 ± 4.50 30.2 ± 2.14 35.3 ± 5.33 35.2 ± 3.02 Buckwheat/oilseed radish 62.9 ± 5,20 63.3 ± 4.82 60.8 ± 8.17 58.8 ± 4.54 61.2 ± 3.69 56.1 ± 8.01 Lentil/oat 34.2 ± 2.70 38.2 ± 4.06 33.3 ± 6.51 66.7 ± 9.49 44.4 ± 6.59 35.2 ± 10.7 Ryegrass/clover 108 ± 4.34 121 ± 9.82 139 ± 10.4 52.4 ± 5.99 64.3 ± 6.46 54.7 ± 3.65 Beetroot 22.0 ± 9.24 21.7 ± 7.10 24.7 ± 3.67 31.0 ± 2.39 31.6 ± 4.87 30.4 ± 4.81 Rye 29.8 ± 5.77 31.0 ± 3.59 33.6 ± 1.84 42.0 ± 3.40 45.1 ± 5.69 35.9 ± 5.69 b a b b a b Buckwheat/phacelia 16.9 – 2.03 50.7 – 10.6 21.3 – 2.71 23.9 – 1.30 35.9 – 1.68 24.9 – 4.75 Pea/barley 47.9 ± 8.34 37.8 ± 5.53 29.0 ± 8.57 56.6 ± 9.57 49.8 ± 6.37 51.9 ± 8.49 Ley 222 ± 64.0 262 ± 9.52 221 ± 15.2 342 ± 19.2 404 ± 42.8 384 ± 23.2 Mean 97 ± 7.0 110 ± 5.5 102 ± 1.8 117 ± 3.5 129 ± 8.1 118 ± 5.7 Superscript letters and numbers in bold mark significant differences. Presented as mean ± standard error (n = 4, ley n = 3 in 2013). The mean value for the entire cropping system (bottom line) was calculated from 6 ha -1 while IS resulted in a positive result (7 kg ha ) due to Discussion the absence of exported biomass. Both the cover crop ryegrass/clover and the green manure ley (summer and The sustainability of the N management in stockless organic farming systems depends on the balance spring yield) resulted in negative results in BR and AD -1 (- 17 to - 284 kg ha ), as biomass was removed between nutrient export via cash crops, nutrient inputs and stored for manuring the next year’s crop. There through N fixation, the internal redistribution and was surplus N in IS for both crops, from 7 to 57 kg N reduction of losses (Legg and Meisinger 1982). -1 ha in the ryegrass/clover cover crop and Stockless organic systems often depend on growing -1 39–74 kg N ha in the green manure ley (Fig. 5). green manure leys, which occupy land for one or more growing seasons. We designed a cropping system with 1/6 of the land allocated for green manure ley and the 123 174 Nutr Cycl Agroecosyst (2018) 112:165–178 Table 5 Nitrogen balance calculated by taking into account considering the temporary stored N in residual biomass or the storage and redistribution of residual biomass as silage/ the N addition from biomass (Stored biomass not considered as -1 digestate in the subsequent year in BR and AD (Stored biomass export) (kg N ha ) considering export and addition next year), and without Treatment Year Stored biomass considering export and addition next year Stored biomass not considered as export IS 2013 - 9.9 - 9.9 2014 1.1 1.1 BR 2013 - 12 - 3.3 2014 - 43 7.8 AD 2013 - 22 - 7.9 2014 - 60 24 remaining land used for food crops, and studied how crops or cover crops. On the contrary, one of the cover different strategies for managing residual biomass crops (buckwheat/phacelia, grown after winter rye) affected internal N cycling and the N balance. The showed significantly higher N acquisition in BR than composition of the rotation was based on a large in AD and IS. A likely reason why AD did not result in variation of species from different plant families, to an increased non-legume N acquisition is that the avoid the risk of multiplying soil-borne diseases and NH concentration in the digestate was lower than the choice of varieties had partial resistance to the expected. The digestate obtained in this study con- -1 most common diseases. tained 0.18–0.27 kg NH –N Mg fresh weight The proportion of N fixation (%Ndfa) in the (Ra˚berg et al. 2017), which is relatively low compared legumes of this study was high and not significantly to similar studies using plant-based digestates (Moller influenced by biomass management method. This was et al. 2008a; Gunnarsson et al. 2011). The total amount probably because the legumes were grown in inter- of N in the digestate was considerably lower than in crops/mixtures with cereal/grasses. The competitive the biomass resources in IS and BR (supplementary ability of cereals and grasses for uptake of mineral N material, Table S1), indicating that there were signif- results in a non-proportional acquisition of soil icant N losses during the handling of the silage before mineral N between the species, leading to a low digestion and/or during the handling of the digestate. availability of mineral N for the legumes and a high As discussed in Raberg et al. (2017), the lack of pre- %Ndfa (Carlsson and Huss-Danell 2003; Hauggaard- treatment before the anaerobic digestion might also Nielsen et al. 2008; Bedoussac et al. 2015). The first have contributed to the low NH concentration in our hypothesis of higher amount of N fixation in AD and study. There are several options for improved man- BR, compared to IS was confirmed for the green agement of the biogas feedstock to optimize both the manure ley in 2014, and a similar tendency could also methane yield and the NH concentration of the be seen in 2013. The higher amount of N fixation is digestate, i.e. mixing, shredding, alkali pre-treatment most likely a consequence of the removal of N-rich and minimising the contact with oxygen at storage cuttings, reducing the N availability and thereby the prior to digestion (Hjorth et al. 2011; Carrere et al. competitiveness of the grasses, thus promoting the 2016). Furthermore, there may also have been N losses growth and N fixation of the legumes (Unkovich et al. at the handling and during field application of the ¨ ¨ 1998;Moller et al. 2008b; Dahlin and Stenberg 2010). digestate (Wulf et al. 2002; Banks et al. 2011;Moller According to the second hypothesis, the N acqui- and Mu¨ller 2012). Using shallow direct injection of the sition from soil and redistributed biomass N resources digestate into the soil would have reduced the risk of N in non-legumes would be higher in AD than the other losses at application (Mo¨ller and Mu¨ller 2012), but this treatments, as the mineral N concentration was technology was not possible to apply in our experi- expected to be higher in the digestate than in the mental plots. biomass/silage in IS and BR. However, this hypothesis Our third hypothesis suggested a lower ranking of was not confirmed for any of the non-legume main IS N balance compared to BR and AD. The N balance 123 Nutr Cycl Agroecosyst (2018) 112:165–178 175 Fig. 5 The N balance per crop x treatment, a 2013, b 2014. The negative side of the bars illustrates export of N in edible plant parts and biomass N exported for redistribution the following year. The positive side illustrates N fixed, biomass addition, deposition and -1 seed contribution (kg ha ). The black line across each bar shows the balance point between import and export of N per crop and for each treatment 123 176 Nutr Cycl Agroecosyst (2018) 112:165–178 that did not consider the temporary removal and Thomsen 2005; De Ruijter et al. 2010). On the other delayed addition of residual biomass in BR and AD hand, an increasing N surplus over time in the BR and -1 resulted in a surplus in 2014 of 7.8 and 24 kg N ha AD treatments could also lead to larger risks for N respectively, with the highest N surplus in the AD losses in these systems in the long term. An interesting treatment (IS \ BR \ AD). The N stored in BR and option in this case would be to sell parts of the AD and applied to the non-legume crops in the spring digestate or silage. This possibility further highlights was potentially protected from being lost after min- the advantage of strategic biomass management in eralisation during autumn and winter (Mo¨ller and stockless organic cropping systems. Mu¨ller 2012; Frøseth et al. 2014). This method that temporary stores residual biomass and thus decreases the risk of N losses from large N surplus could provide Conclusion an improvement to stockless organic farms, where the -1 N surplus can be as high as 194 kg ha (Watson et al. Our objective was to assess how different strategies 2002). It is highly relevant to maintain a low level of N for internal N cycling via residual biomass influence in soils like Arenosol, which have high infiltration and the N balance of a stockless organic cropping systems. drainage rate (De Paz and Ramos 2004). The increased The result of the assessment was that the AD and BR N content in the biomass from 2013 to 2014 of the scenarios showed more positive N balances than IS. current study originated partly from a higher N Strategically choosing where and when to add biomass fixation in BR and AD, but mainly from the soil N pool N resources in the crop rotation thus has large potential and applied residual biomass in all three treatments. to sustain crop yields and soil fertility, i.e. avoiding the Consequently, the fourth hypothesis of higher total N risk of soil N depletion at the cropping system level. acquisition from soil and added biomass in AD and BR The positive effects are dominated by the increased N compared to IS was not confirmed (Fig. 3). fixation in the legumes, compared to leaving the The fact that the amount of residual biomass N residues, cover crop biomass and green manure ley increased over time explains the negative N balances cuttings in situ. Additionally, the risk for N losses was in BR and AD when the storage and redistribution of potentially decreased due to the over winter storage of biomass N was taken into account (Table 4), since the the biomass returned to non-legumes in the subsequent temporarily exported biomass N was larger than the growth season. Nevertheless, care needs to be taken biomass N redistributed from the previous year. The when applying residual biomass to selected crops in difference between the key inputs and outputs at the the cropping system, since high application rates cropping system level, i.e. N fixation minus N export might also lead to N losses depending on timing and in edible crop fractions, was more negative in IS than incorporation technique of the silage/digestate into the in BR and AD. soil. The conclusion is that organic stockless farms If the field experiment would have continued for a could improve circulation of N by collecting the full 6-year cycle or more, it is possible that the N residual biomass after harvest and thereby reduce the balances in BR and AD would become increasingly potential risk for N leakage and N emissions. These larger than in IS, due to an accumulated effect of aspects require further research about how strategic higher quantities of N fixation and targeted applica- biomass N management influences N losses at differ- tion of silage/digestate to N-demanding non-legume ent processes and at the entire cropping system level. crops. The strategic management of residual biomass A comparison between the management systems in in BR and AD would thus sustain crop yields with low terms of the energy use and greenhouse gas emissions risk of long-term depletion of soil N fertility, which related to transportation and storage of the biomass might be the case in IS where the N balance is less resources would also be relevant for a full assessment positive. In addition, BR and AD can also be expected of the environmental benefits. to reduce the risks for NO leakage and gaseous N Acknowledgements We acknowledge the Swedish Research emissions compared to the in situ application of Council Formas and the Swedish University of Agricultural residual biomass in IS, where more N would be Sciences for funding of the research. 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Nitrogen balance in a stockless organic cropping system with different strategies for internal N cycling via residual biomass

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Abstract

Nutr Cycl Agroecosyst (2018) 112:165–178 https://doi.org/10.1007/s10705-018-9935-5(0123456789().,-volV)(0123456789().,-volV) ORIGINAL ARTICLE Nitrogen balance in a stockless organic cropping system with different strategies for internal N cycling via residual biomass . . Tora Ra˚berg Georg Carlsson Erik Steen Jensen Received: 6 July 2017 / Accepted: 4 July 2018 / Published online: 31 July 2018 The Author(s) 2018 Abstract A major future challenge in agriculture is second study year. The N balance ranged between -1 to reduce the use of new reactive nitrogen (N) while - 9.9 and 24 kg N ha , with more positive budgets maintaining or increasing productivity without caus- in AD and BR than in IS. The storage of biomass for ing a negative N balance in cropping systems. We reallocation in spring led to an increasing accumula- investigated if strategic management of internal tion of N in the BR and AD systems from one year to biomass N resources (green manure ley, crop residues another. These strategies also provide an opportunity and cover crops) within an organic crop rotation of six to supply the crop with the N when most needed, main crops, could maintain the N balance. Two years thereby potentially decreasing the risk of N losses of measurements in the field experiment in southern during winter. Sweden were used to compare three biomass man- agement strategies: anaerobic digestion of ensiled Keywords Anaerobic digestion  Arable and biomass and application of the digestate to the non- horticultural crops  N balance  N fixation  Soil and legume crops (AD), biomass redistribution as silage to residue N  Strategic biomass N management non-legume crops (BR), and leaving the biomass in situ (IS). Neither aboveground crop N content from Abbreviations soil, nor the proportion of N derived from N fixation AD Anaerobic digestion in legumes were influenced by biomass management BNF Biological nitrogen fixation treatment. On the other hand, the allocation of N-rich BR Biomass redistribution silage and digestate to non-legume crops resulted in IS In situ -1 higher N fixation in AD and BR (57 and 58 kg ha %Ndfa Proportion (%) of accumulated nitrogen -1 -1 -1 year ), compared to IS (33 kg ha year ) in the derived from nitrogen fixation Electronic supplementary material The online version of Introduction this article (https://doi.org/10.1007/s10705-018-9935-5) con- tains supplementary material, which is available to authorized users. The planetary boundary research highlight the impor- tance of reducing global inputs of new reactive T. Ra˚berg (&)  G. Carlsson  E. S. Jensen nitrogen (N) to ecosystems (Steffen et al. 2015). The Department of Biosystems and Technology, Swedish University of Agricultural Sciences, P.O. Box 103, amounts of N applied as fertiliser in agriculture have 230 53 Alnarp, Sweden not been sufficiently constrained to prevent e-mail: tora.raberg@slu.se 123 166 Nutr Cycl Agroecosyst (2018) 112:165–178 widespread leakage to freshwaters and the atmo- manure ley and cover crop cuttings) in situ is a sphere, with effects on human health, biodiversity and common practice in agriculture, but it may result in climate (Fowler et al. 2013). Organic agriculture, substantial losses of N, if mineralisation and acquisi- compared with conventional, offers benefits such as tion of the following crop is not well synchronised increased cycling of nutrients and lower energy usage (Pang and Letey 1998;Moller et al. 2008a; Mohanty for processing fertilisers of organic origin than for et al. 2013). It may be possible to improve the synthetic fertilisers (Worrell et al. 2000; Vance 2001; synchrony between application of residual biomass N, Rockstro¨m et al. 2009). Consumers today are often N fixation and plant acquisition of N by pre-treating concerned about the environment and/or the chemicals and storing the biomass as silage or as digestate from used in food production, and both supply and demand anaerobic digestion (Gutser et al. 2005; Gunnarsson for certified organic production continue to grow et al. 2011; Frøseth et al. 2014). Ensiling initiates (Mueller and Thorup-Kristensen 2001; Willer and mineralisation, but also conserves the biomass by Schaack 2015). For example, the EU-28 increased its lowering the pH and creating an anaerobic environ- total area cultivated as organic from 5.0 to 11 million ment (Herrmann et al. 2011). Anaerobic digestion of hectares between 2002 and 2015 (Eurostat 2015). This plant material and subsequent use of the residual large-scale conversion of production needs to be met digestate as a fertiliser is of particular interest to with intensified research to ensure that the methods are supply N for non-legume crops in the absence of optimised for high yields and that pollution is animal manure in stockless organic systems (Gu- minimised. naseelan 1997). In general, there is a larger proportion Modern agriculture has increasingly led to special- of plant available N in the digestate compared with in ization in either crop or animal production in entire fresh or ensiled biomass (Weiland 2010). A high level regions, causing limited availability of animal manure of mineral N in the soil will generally decrease both for stockless farms (Schmidt et al. 1999; Mueller and nodulation and N fixation (Streeter and Wong 1988; Thorup-Kristensen 2001; Stinner et al. 2008). Thus, Waterer and Vessey 1993) and thereby make the many arable and horticultural organic farms choose to legume more dependent on soil mineral N. Increased import a considerable amount of concentrated fer- yield and N fixation might be possible by redistribut- tiliser made from by-products of the food industry ing the N rich silage or digestate to non-legume sole (Watson et al. 2002; Wivstad 2009; Colomb et al. crops. It is challenging to balance N inputs in organic 2013). To reduce the need for external fertiliser inputs, farming to ensure long-term soil fertility with high and researchers suggest strategies that could improve soil stable yields, avoiding depletion of the soil N pool and fertility and internal nutrient cycling at the farm level, at the same time avoid a surplus that has negative such as improved residue management, intercropping impacts on the surrounding ecosystem (de Ponti et al. and growing cover crops (Tilman et al. 2002; Bom- 2012; Colomb et al. 2013; Seufert and Ramankutty marco et al. 2013). Cycling of N is central to reduce 2017). the need for production of more reactive N (Bodirsky Calculation of N balance is a tool for expanding the et al. 2014). However, N is often the most limiting understanding of the N cycle and evaluate the effect of nutrient for crop performance in terms of yield and different management practices on the soil-crop N quality, and is needed in larger quantities than any of cycle and the sustainability of N management methods the other essential nutrients (Mengel and Kirkby 1978; (Watson et al. 2002). A N balance can summarise the Sinclair and Horie 1989). To obtain high yield and complex agricultural N cycle by documenting the quality, mineralisation of N from organic fertilisers major flow paths as N enters and emerges from various and SOM needs to be in synchrony with crop pools and leaves the system for various fates (Mei- acquisition. singer et al. 2008). Calculating the N balance at crop, Incorporation of residues from legume cover crops cropping system or farm level is also a valuable tool and forage legumes, containing symbiotically fixed N, for identifying risks of N depletion or build-up of a N improves N supply substantially and is very important surplus, thereby highlighting the potential need for in organic farming systems without livestock, where improved N management. A N balance made for 76 other options for N input are limited. Incorporating organic arable farms in Sweden showed an average N residual biomass (here defined as crop residue, green surplus of 39 kg/ha (Wivstad 2009). The surplus was 123 Nutr Cycl Agroecosyst (2018) 112:165–178 167 Materials and methods mainly due to imported nutrients from digestate, yeast liquid and dried slaughter house waste. Horticultural Study site and soil cropping systems tend to import even more N than arable farms, which results in a N balance with higher The experiment was established in 2012 at the N surpluses (Watson et al. 2002), and is thus prone to a higher risk of N losses. Swedish University of Agricultural Sciences in 0 00 0 00 Alnarp, southern Sweden (5539 21 N, 1303 30 E), The objective of this study was to assess how different strategies for internal N cycling via residual on a sandy loam soil of Arenosol type (Deckers et al. biomass influenced the N balance of a stockless 1998). The field experiment was conducted on organ- organic cropping system, where the input of N was ically certified agricultural land within the SITES limited to biological N fixation, N contained in Lo¨nnstorp field research station, with grass-clover ley seeds/plantlets for crop establishment and atmospheric as the pre-crop. The annual mean atmospheric depo- -1 N deposition. The specific aims were (1) to determine sition of N contributed with a total of 9.4 kg ha -1 year during 2013–2014, in the region where the field whether anaerobic digestion (AD) of the residual biomass from the cropping system, and use of its experiment was situated (SMHI 2016). digestate for N recirculation, would improve the N acquisition in the following crop, compared to the Climatic data corresponding biomass redistribution (BR) of silage or just leaving the biomass in situ (IS) and (2) to test if The region has a typical northern-European maritime strategic management of residual biomass (AD and climate with mild winter and summer temperatures BR) could improve the N balance of the cropping (annual average of 9.3 C and 664 mm precipitation) system. Six main crops, including both arable and (Ra˚berg et al. 2017). horticultural crops, were combined in a field experi- ment with the purpose to study how the soil N Crop rotation acquisition and symbiotic N fixation of the different crops respond to the biomass management strategies. Six different crops in a rotation including different legume species, over-wintering cash and cover crops We used the N balance method as a tool to determine how a biomass management strategy influenced the (Table 1) were studied during 2 years (2013 and risk of depleting or creating surplus of soil N at both 2014). The rotation consisted of the following food individual crop and at the cropping system level, but crops: pea/barley (Pisum sativum L./Hordeum vulgare without considering N emissions to the environment in L.), lentil/oat (Lens culinaris Medik/Avena sativa L.), the calculation. The hypotheses were: I) the amount white cabbage (Brassica oleracea L.), beetroot (Beta and proportion of N fixed in legume crops (legumes vulgaris L.) and winter rye (Secale cereale L.). The sixth main crop was a green manure ley composed of in the green manure ley, lentil (Lens culinaris Medik), pea (Pisum sativum L.), clover (Trifolium pratense L. the following six species in equal proportions: orchard grass (Dactylis glomerata L.), meadow fescue (Fes- and T. repens L.) in cover crop) is greater with AD and BR than in the IS management, II) N acquisition from tuca pratensis L.), timothy grass (Phleum pratense L.), lucerne (Medicago sativa L.), yellow sweet clover soil and residual biomass in non-legume crops is greater in AD than BR and IS, III) the N balance at the (Melilotus officinalis L.) and red clover (Trifolium pratense L.) (Ra˚berg et al. 2017). The green manure cropping system level ranks IS \ BR \ AD, and IV) the total N acquisition originating from soil and added ley was under-sown in pea/barley, cut three times biomass in all crops is on average larger in AD and BR during the year after establishment, and cut again in than in IS. early spring the subsequent year, before establishing white cabbage as the next crop. The herbage was removed in BR and AD and left in situ in IS. Cover crops were included in the rotation after white cabbage (buckwheat, Fagopyrum esculentum Moench/oilseed radish, Raphanum sativus L.) and rye (buckwheat/lacy phacelia, Phacelia tanacetifolia Benth.), and was 123 168 Nutr Cycl Agroecosyst (2018) 112:165–178 Table 1 The main crops Main crop Cover and winter crops and cover crops in the rotation White cabbage Buckwheat/oilseed radish Lentil/oat ? english ryegrass/red and white clover English ryegrass/red and white clover Beet root Winter rye Winter rye Buckwheat/phacelia Pea/barley ? green manure ley Green manure ley Green manure ley Green manure ley under-sown in lentil/oat (ryegrass, Lolium perenne L./ randomly distributed within each block (18 plots). The red clover, Trifolium pratense L./white clover T. reference treatment was a system where all the residual biomass (crop residues, green manure ley repens L.). All six main crops in the rotation were grown during each year of the experiment. Winter rye and cover crops cuttings) was incorporated fresh was replaced by spring barley during the establish- in situ (IS) in the experimental plot (Fig. 1). The IS ment year (2012), since the experiment started in treatment was used as a reference, as it is common spring without any autumn-sown crop from the practice to leave most of the crop residue in the field in previous year. The choice of crops in the rotation organic arable farming (Ogren 1992; Ascard and was based on maximising the cash crop yield and Bunnvik 2008). Two additional biomass management improve the functional diversity to strengthen ecosys- treatments were: (1) ensiling and redistributing all tem services (Ra˚berg et al. 2017). residual biomass (BR) to experimental plots with cabbage, winter rye and beetroot; and (2) all of the Field management residual biomass was ensiled and later anaerobically digested (AD) in a biogas reactor, and the digestate The ley pre-crop was incorporated by inversion tillage was applied to cabbage, winter rye and beetroot, as (tillage depth 25 cm) before the experiment started. described in Ra˚berg et al. (2017). The N supplied to During the field experiment, a non-inversion rotary the crops in each treatment are presented in the cultivator was used mixing the crop residue with soil supplementary material. This design allowed for to a maximum depth of 15 cm. The experimental area -1 received an initial supply of 115 kg N ha of plant- based digestate applied with trailing hoses in spring 2012. No other external fertiliser was added during the field experiment. Crop protection followed the national organic regulations. The weeding was made by hand in the row crops (cabbage and beetroot) in the same way and around the same dates in all treatments. Seed bed preparations was made by harrowing approximately a week before sowing to allow for weeds to germinate, and then weeds were removed by a second harrowing. The cabbage was grown under an insect mesh and hand-sprayed with Bacillus thuringiensis every second week after spotting Lepi- doptera larvae. Fig. 1 Residue management within the crop rotation: (1) Experimental design IS = In situ incorporation, (2) BR = biomass redistributed to the non-leguminous crops grown in pure stand and (3) AD = digested biomass distributed to the non-leguminous crops The field experiment comprised in total 72 experi- grown in pure stand. The residual biomass in IS was applied mental plots measuring 3 9 6 m, distributed in four fresh, in BR it was ensiled prior to field application and in AD it blocks. All six crops and the three treatments were was ensiled and anaerobically digested as a pre-treatment 123 Nutr Cycl Agroecosyst (2018) 112:165–178 169 Calculations and statistics sampling and harvesting of each crop with the three different management strategies in every year. N fixation and N acquisition from soil and added Sampling and harvest biomass The residual biomass was collected and ensiled The N inputs from N fixation was assessed according to the N natural abundance method (Unkovich et al. separately in BR and AD, with harvest from spring until October each year, to allow time for digestion in 1997, 2008), using the lowest observed legume d N- AD. The same strategy was used for the collection of value as b-value in Eq. (1), as recommended by e.g. biomass in BR to make it comparable to AD. The Hansen and Vinther (2001) and Huss-Danell et al. method resulted in a 1-year delay for the use of the (2007). The b-value is defined as a measure of the N May harvest of green manure ley and ryegrass/clover content of the target legume (d N ) when fully in the BR and AD treatments. Measurements of yield dependent on N fixation for its N acquisition (Unkovich et al. 2008). In the present study, the and N content started in 2012 and the last samples were collected in 2015 for two over-wintering crops, samples used as b-value were also included in the calculations of the average N fixation per treatment. green manure ley and ryegrass/clover cover crop. Samples from overwintering crops harvested in May, The N signature of the grasses and weeds grown together with the legumes in the green manure ley, were allocated to the biomass production of the previous year. Since no effects of the biomass intercrops and cover crops were used as reference management treatments could be expected during plants (d N ). ref the establishment year, the study is based on samples 15 15 ðd N  d N Þ ref L and measurements from 2013 to 2014. Average yields %N ¼  100; ð1Þ dfa d N  b ref and N content in harvests during 2012 are listed in supplementary material, Table S2. %N = the proportion of the total N uptake origi- dfa 15 15 All residual biomass (crop residues, green manure nating from N fixation; d N = the N signature of 2 ref ley and cover crops) was weighed before returning it to the grasses and weeds grown together with the 15 15 the field plot (IS) or ensiled for later redistribution (BR legumes; d N = the N signature of the legume; 15 15 and AD), as described in Ra˚berg et al. (2017). b = the N signature of the target legume (d N ) Subsamples from a 0.25 m surface per plot were when fully dependent on N fixation for its N taken for analyses of botanical composition (grouped acquisition. -1 into legumes and non-legumes), N concentration and The amount of N fixed (kg N ha ) in each legume natural abundance of the stable isotope N. After crop was calculated by multiplying %Ndfa with total drying and milling the edible and residual biomass crop N content (N concentration  crop biomass). Soil fractions of each subsample (see Raberg et al. 2017 for N acquisition in legumes, representing N from the soil 15 14 details), the N concentration and N/ N ratio in each N pool as well as from added residual biomass, was fraction was measured with an elemental analyser calculated by subtracting the amount of N fixed from coupled to an isotope ratio mass spectrometer (PDZ the total crop N content in the aboveground plant parts. Europe 20-20, at UC Davies in USA) in legume- For non-legume crops, the amount of N acquired from containing crop mixtures. A Flash 2000 Thermo soil and added biomass was the same as the total Scientific elemental analyser (at SLU, Alnarp, Swe- aboveground crop N content. den) was used for determination of N concentration in each fraction of sole crops. The analyses of these Nitrogen balance subsamples were then used for calculating N fixation, N export in edible fractions and N circulation via The balance of N for the cropping sequences was residual biomass (see below). calculated per crop and as an annual sum of each treatment for the years 2013 and 2014. The N balance was calculated from data on N input and output from the cropping system (Eq. 2, Fig. 2). 123 170 Nutr Cycl Agroecosyst (2018) 112:165–178 Fig. 2 Input and output components of the N balance. The N coming in and leaving from the crop- soil system was quantified, except for the losses of nitrogen (ammonia volatilization, denitrification and N leaching) (dashed arrow) fractions, amounts of N in residual biomass), both on N balance ¼ bnf þ dep þ seed þ biomass added ð2Þ individual crop and on cropping system level (except edible fractionbiomass removed for %Ndfa which was only tested at crop level). These bnf = biological N fixation in current year, calculated ANOVAs were performed using the general linear as described above; dep = atmospheric N deposition; model (GLM) in the Minitab software, assuming block seed = seed N and plantlet N; biomass = N from and treatment as fixed factors. Whenever a significant added added residual biomass from previous year; edible interaction between year and treatment was found, fraction = exported N in the edible fraction of cash treatment effects were again tested for significance crops; biomass = total N from residual biomass separately for each year. removed removed to be circulated succeeding year. The regional measurements of atmospheric N deposition during the time of the field experiments Results -1 -1 added 9.4 kg total N ha year (SMHI 2016), which was divided and allocated on two crops when there Nitrogen acquisition was more than one crop in the same field and in the same year (i.e. main crop and cover crop). The N Total N content in the aboveground parts of the crops -1 -1 contribution from seeds was obtained from measured ranged between 140 and 180 kg ha year (Fig. 3), seed N content for the cereals and grain legumes with no significant difference between the biomass (Table 3), and was calculated from literature for the strategies. non-food seeds and plantlets (Schroeder et al. 1974). The amounts of N added via residual biomass Nitrogen fixation corresponded to the redistribution of ensiled (BR) and digested (AD) biomass from the previous year The total N fixation in leguminous crops constituted (supplementary material, Table S1). The N outputs in 14–26% of total N content in the aboveground plant the balance consisted of the amounts of N exported in parts of all crops, which corresponded to an average of -1 -1 the harvested edible fraction of the cash crops and N 23–40 kg ha year (Fig. 3). The %Ndfa was found exported in residual biomass in AD and BR to be to be in the range 68–98% across all legume species in redistributed in the next growing season. the cropping system, and was not significantly differ- Analyses of variance (ANOVA) were conducted to ent between biomass management treatments test the significance in differences between years (Table 2). The amount of N fixed was higher with (2013 and 2014) and effects of block and treatment BR and AD treatments, compared to IS (p = 0.002) as (IS, BR and AD) on the response variables (%Ndfa, the years were analysed together. The effect was only amounts of N derived from N fixation and from soil significant in 2014 (p = 0.021) (Fig. 3), when the acquisition, amounts of N in export of edible crop years were analysed separately. A large part of the 123 Nutr Cycl Agroecosyst (2018) 112:165–178 171 N acquisition from soil The total N acquisition from soil varied between 110 -1 and 140 kg N ha calculated as an average for the entire crop rotation, and the total N content was significantly higher (p = 0.002) in 2014, compared to 2013 (Fig. 3). Differences between the three biomass residue management methods were small and in most cases non-significant (Fig. 4a and b). The BR treat- ment led to significantly (p \ 0.001) higher soil N acquisition in the cover crop buckwheat/lacy phacelia in both years as compared to IS and AD treatments (Fig. 4). Nitrogen exported in the edible crop fraction Fig. 3 The total mean N content of the crop biomass from the -1 The average N content in the exported edible fractions entire cropping systems in 2013 and 2014 in kg ha . Total N is of the five food crops varied between 49 and presented as a sum of N acquired from the soil and through N -1 fixation. The letters show significant differences between 60 kg ha , with the highest amount exported in rye treatments in N fixation. The error bars represent standard grain and the lowest in pea/barley. The N content in error for each fraction (N = 4 except for ley with N = 3 in 2013) the edible fraction was not affected by the three treatments (Table 3), even if the N supply differed increased N fixation was derived from the legumes of substantially (table in supplementary material). the green manure ley, with a significantly higher (p \ 0.001) N fixation in BR and AD compared to IS Nitrogen in residual biomass in 2014 (Fig. 4b). The amount of N fixation in lentil and pea varied inconsistently between treatments in The total amount of N in residual biomass varied the 2 years. No significant difference between treat- -1 between 97 and 129 kg N ha (Table 4). There was a ments was found for the amount of N fixed in clover significant interaction between treatment and year grown together with ryegrass in the cover crop, which -1 -1 when the total N content of all the crops from the three ranged between 12 and 78 kg N ha year and was systems were compared (p = 0.001), but when each higher in 2013 than in 2014. year was analysed individually there was no signifi- cant difference between the three treatments. In 2013, the green manure ley cuttings constituted 36–40% of the total amount of residual biomass N, and in 2014 the Table 2 The proportion of nitrogen acquired through N BR = biomass redistributed to the non-leguminous crops fixation (%Ndfa) in legumes at different biomass treatments grown in pure stand and (3) AD = digested biomass distributed within the crop rotation: (1) IS = In situ incorporation, (2) to the non-leguminous crops grown in pure stand Crops Ndfa (%) 2013 2014 IS BR AD IS BR AD Lentil 83 ± 3.8 87 ± 7.7 98 ± 1.7 73 ± 3.8 68 ± 11 80 ± 11 Clover 96 ± 0.5 95 ± 2.9 95 ± 1.3 93 ± 3.0 92 ± 1.6 94 ± 0.9 Pea 94 ± 2.1 86 ± 2.1 88 ± 3.7 89 ± 3.5 87 ± 1.6 89 ± 4.5 Green manure ley 74 ± 8.3 85 ± 3.3 83 ± 3.6 76 ± 2.1 81 ± 2.2 81 ± 1.2 Presented as mean ± standard error (N = 4, except for green manure ley 2013 with N = 3) 123 172 Nutr Cycl Agroecosyst (2018) 112:165–178 Fig. 4 Nitrogen content of the aboveground biomass of individual crops (kg N -1 ha ) in 2013 (a) and 2014 (b), presented as mean ± standard error (N = 4 except for ley with N = 3 in 2013). The grey bars represent N acquisition from soil and residual crop biomass, and the white bars represent N fixation of the legumes. IS = In situ incorporation. BR = biomass redistributed to the non-leguminous crops grown in pure stand. AD = digested biomass distributed to the non- leguminous crops grown in pure stand. The error bars represent standard error for each fraction. * = Significance according to ANOVA at p \ 0.05. ** = Significance according to ANOVA at p \ 0.01 part increased to between 49 and 54%. When summed The three crops that were fertilised with biomass in for all biomass resources in the cropping system, the BR and AD resulted in N surplus for the N balance of total N content of the residual biomass increased over both years, with the highest surplus in cabbage with -1 time, regardless of treatment, with an average differ- the BR treatment in 2014 (178 kg ha ). The excep- -1 ence of 19 kg N ha between 2013 and 2014 tion from the surplus results was the winter rye crop (Table 4). with BR treatment in 2014, which resulted in -1 - 8kgha (Fig. 5b). Cabbage, red beet and rye all Nitrogen balance had a negative N balance in IS, ranging from - 36 to -1 - 68 kg ha . The lentil/oat intercrop resulted in a The N balances at the cropping system level was more negative result for all treatments, and most negative -1 positive in 2014 than in 2013 in the BR and AD for AD and BR, from - 37 to - 79 kg ha . The pea/ treatments, when not considering the residual biomass barley intercrop resulted in a surplus of -1 N as a temporary export in the harvest year and input 21–47 kg ha for IS (2014 and 2013 respectively), in the subsequent year (Table 5; Stored biomass not while the balance for BR and AD resulted in 5 to -1 considered as export). - 47 kg ha . The non-legume cover crops had a -1 negative result for BR and AD, - 15 to - 57 kg ha , 123 Nutr Cycl Agroecosyst (2018) 112:165–178 173 Table 3 Nitrogen exported in edible fractions of crops (kg N to the non-leguminous crops grown in pure stand and (3) -1 ha ) at different biomass treatments within the crop rotation: AD = digested biomass distributed to the non-leguminous (1) IS = In situ incorporation, (2) BR = biomass redistributed crops grown in pure stand Crop Nitrogen export in edible fraction 2013 2014 IS BR AD IS BR AD Cabbage 44 ± 5.1 44 ± 8.9 45 ± 4.6 52 ± 2.9 56 ± 5.8 58 ± 6.6 Lentil/oat 67 ± 8.1 81 ± 8.3 70 ± 9.2 53 ± 14 62 ± 9.7 52 ± 7.6 Beetroot 41 ± 15 31 ± 13 51 ± 12 42 ± 4.4 40 ± 6.5 39 ± 4.7 Rye 75 ± 12 84 ± 15 90 ± 12 63 ± 4.0 75 ± 12 60 ± 7.5 Pea/barley 28 ± 11 17 ± 3.8 26 ± 7.9 44 ± 13 67 ± 6.4 35 ± 12 Mean 43 ± 3.2 43 ± 3.5 47 ± 3.0 42 ± 1.5 50 ± 3.8 41 ± 4.0 Presented as mean ± standard error (n = 4). The mean value for the entire cropping system (bottom line) was calculated from 6 ha, even if ley is excluded in the sum, but nevertheless crucial for the production of edible produce in the cropping system -1 Table 4 Nitrogen in residual biomass (kg N ha ) at different leguminous crops grown in pure stand and (3) AD = digested biomass treatments within the crop rotation: (1) IS = In situ biomass distributed to the non-leguminous crops grown in pure incorporation, (2) BR = biomass redistributed to the non- stand -1 Crop N in residual biomass (kg ha ) 2013 2014 IS BR AD IS BR AD Cabbage 36.3 ± 3.29 33.7 ± 4.36 46.3 ± 4.50 30.2 ± 2.14 35.3 ± 5.33 35.2 ± 3.02 Buckwheat/oilseed radish 62.9 ± 5,20 63.3 ± 4.82 60.8 ± 8.17 58.8 ± 4.54 61.2 ± 3.69 56.1 ± 8.01 Lentil/oat 34.2 ± 2.70 38.2 ± 4.06 33.3 ± 6.51 66.7 ± 9.49 44.4 ± 6.59 35.2 ± 10.7 Ryegrass/clover 108 ± 4.34 121 ± 9.82 139 ± 10.4 52.4 ± 5.99 64.3 ± 6.46 54.7 ± 3.65 Beetroot 22.0 ± 9.24 21.7 ± 7.10 24.7 ± 3.67 31.0 ± 2.39 31.6 ± 4.87 30.4 ± 4.81 Rye 29.8 ± 5.77 31.0 ± 3.59 33.6 ± 1.84 42.0 ± 3.40 45.1 ± 5.69 35.9 ± 5.69 b a b b a b Buckwheat/phacelia 16.9 – 2.03 50.7 – 10.6 21.3 – 2.71 23.9 – 1.30 35.9 – 1.68 24.9 – 4.75 Pea/barley 47.9 ± 8.34 37.8 ± 5.53 29.0 ± 8.57 56.6 ± 9.57 49.8 ± 6.37 51.9 ± 8.49 Ley 222 ± 64.0 262 ± 9.52 221 ± 15.2 342 ± 19.2 404 ± 42.8 384 ± 23.2 Mean 97 ± 7.0 110 ± 5.5 102 ± 1.8 117 ± 3.5 129 ± 8.1 118 ± 5.7 Superscript letters and numbers in bold mark significant differences. Presented as mean ± standard error (n = 4, ley n = 3 in 2013). The mean value for the entire cropping system (bottom line) was calculated from 6 ha -1 while IS resulted in a positive result (7 kg ha ) due to Discussion the absence of exported biomass. Both the cover crop ryegrass/clover and the green manure ley (summer and The sustainability of the N management in stockless organic farming systems depends on the balance spring yield) resulted in negative results in BR and AD -1 (- 17 to - 284 kg ha ), as biomass was removed between nutrient export via cash crops, nutrient inputs and stored for manuring the next year’s crop. There through N fixation, the internal redistribution and was surplus N in IS for both crops, from 7 to 57 kg N reduction of losses (Legg and Meisinger 1982). -1 ha in the ryegrass/clover cover crop and Stockless organic systems often depend on growing -1 39–74 kg N ha in the green manure ley (Fig. 5). green manure leys, which occupy land for one or more growing seasons. We designed a cropping system with 1/6 of the land allocated for green manure ley and the 123 174 Nutr Cycl Agroecosyst (2018) 112:165–178 Table 5 Nitrogen balance calculated by taking into account considering the temporary stored N in residual biomass or the storage and redistribution of residual biomass as silage/ the N addition from biomass (Stored biomass not considered as -1 digestate in the subsequent year in BR and AD (Stored biomass export) (kg N ha ) considering export and addition next year), and without Treatment Year Stored biomass considering export and addition next year Stored biomass not considered as export IS 2013 - 9.9 - 9.9 2014 1.1 1.1 BR 2013 - 12 - 3.3 2014 - 43 7.8 AD 2013 - 22 - 7.9 2014 - 60 24 remaining land used for food crops, and studied how crops or cover crops. On the contrary, one of the cover different strategies for managing residual biomass crops (buckwheat/phacelia, grown after winter rye) affected internal N cycling and the N balance. The showed significantly higher N acquisition in BR than composition of the rotation was based on a large in AD and IS. A likely reason why AD did not result in variation of species from different plant families, to an increased non-legume N acquisition is that the avoid the risk of multiplying soil-borne diseases and NH concentration in the digestate was lower than the choice of varieties had partial resistance to the expected. The digestate obtained in this study con- -1 most common diseases. tained 0.18–0.27 kg NH –N Mg fresh weight The proportion of N fixation (%Ndfa) in the (Ra˚berg et al. 2017), which is relatively low compared legumes of this study was high and not significantly to similar studies using plant-based digestates (Moller influenced by biomass management method. This was et al. 2008a; Gunnarsson et al. 2011). The total amount probably because the legumes were grown in inter- of N in the digestate was considerably lower than in crops/mixtures with cereal/grasses. The competitive the biomass resources in IS and BR (supplementary ability of cereals and grasses for uptake of mineral N material, Table S1), indicating that there were signif- results in a non-proportional acquisition of soil icant N losses during the handling of the silage before mineral N between the species, leading to a low digestion and/or during the handling of the digestate. availability of mineral N for the legumes and a high As discussed in Raberg et al. (2017), the lack of pre- %Ndfa (Carlsson and Huss-Danell 2003; Hauggaard- treatment before the anaerobic digestion might also Nielsen et al. 2008; Bedoussac et al. 2015). The first have contributed to the low NH concentration in our hypothesis of higher amount of N fixation in AD and study. There are several options for improved man- BR, compared to IS was confirmed for the green agement of the biogas feedstock to optimize both the manure ley in 2014, and a similar tendency could also methane yield and the NH concentration of the be seen in 2013. The higher amount of N fixation is digestate, i.e. mixing, shredding, alkali pre-treatment most likely a consequence of the removal of N-rich and minimising the contact with oxygen at storage cuttings, reducing the N availability and thereby the prior to digestion (Hjorth et al. 2011; Carrere et al. competitiveness of the grasses, thus promoting the 2016). Furthermore, there may also have been N losses growth and N fixation of the legumes (Unkovich et al. at the handling and during field application of the ¨ ¨ 1998;Moller et al. 2008b; Dahlin and Stenberg 2010). digestate (Wulf et al. 2002; Banks et al. 2011;Moller According to the second hypothesis, the N acqui- and Mu¨ller 2012). Using shallow direct injection of the sition from soil and redistributed biomass N resources digestate into the soil would have reduced the risk of N in non-legumes would be higher in AD than the other losses at application (Mo¨ller and Mu¨ller 2012), but this treatments, as the mineral N concentration was technology was not possible to apply in our experi- expected to be higher in the digestate than in the mental plots. biomass/silage in IS and BR. However, this hypothesis Our third hypothesis suggested a lower ranking of was not confirmed for any of the non-legume main IS N balance compared to BR and AD. The N balance 123 Nutr Cycl Agroecosyst (2018) 112:165–178 175 Fig. 5 The N balance per crop x treatment, a 2013, b 2014. The negative side of the bars illustrates export of N in edible plant parts and biomass N exported for redistribution the following year. The positive side illustrates N fixed, biomass addition, deposition and -1 seed contribution (kg ha ). The black line across each bar shows the balance point between import and export of N per crop and for each treatment 123 176 Nutr Cycl Agroecosyst (2018) 112:165–178 that did not consider the temporary removal and Thomsen 2005; De Ruijter et al. 2010). On the other delayed addition of residual biomass in BR and AD hand, an increasing N surplus over time in the BR and -1 resulted in a surplus in 2014 of 7.8 and 24 kg N ha AD treatments could also lead to larger risks for N respectively, with the highest N surplus in the AD losses in these systems in the long term. An interesting treatment (IS \ BR \ AD). The N stored in BR and option in this case would be to sell parts of the AD and applied to the non-legume crops in the spring digestate or silage. This possibility further highlights was potentially protected from being lost after min- the advantage of strategic biomass management in eralisation during autumn and winter (Mo¨ller and stockless organic cropping systems. Mu¨ller 2012; Frøseth et al. 2014). This method that temporary stores residual biomass and thus decreases the risk of N losses from large N surplus could provide Conclusion an improvement to stockless organic farms, where the -1 N surplus can be as high as 194 kg ha (Watson et al. Our objective was to assess how different strategies 2002). It is highly relevant to maintain a low level of N for internal N cycling via residual biomass influence in soils like Arenosol, which have high infiltration and the N balance of a stockless organic cropping systems. drainage rate (De Paz and Ramos 2004). The increased The result of the assessment was that the AD and BR N content in the biomass from 2013 to 2014 of the scenarios showed more positive N balances than IS. current study originated partly from a higher N Strategically choosing where and when to add biomass fixation in BR and AD, but mainly from the soil N pool N resources in the crop rotation thus has large potential and applied residual biomass in all three treatments. to sustain crop yields and soil fertility, i.e. avoiding the Consequently, the fourth hypothesis of higher total N risk of soil N depletion at the cropping system level. acquisition from soil and added biomass in AD and BR The positive effects are dominated by the increased N compared to IS was not confirmed (Fig. 3). fixation in the legumes, compared to leaving the The fact that the amount of residual biomass N residues, cover crop biomass and green manure ley increased over time explains the negative N balances cuttings in situ. Additionally, the risk for N losses was in BR and AD when the storage and redistribution of potentially decreased due to the over winter storage of biomass N was taken into account (Table 4), since the the biomass returned to non-legumes in the subsequent temporarily exported biomass N was larger than the growth season. Nevertheless, care needs to be taken biomass N redistributed from the previous year. The when applying residual biomass to selected crops in difference between the key inputs and outputs at the the cropping system, since high application rates cropping system level, i.e. N fixation minus N export might also lead to N losses depending on timing and in edible crop fractions, was more negative in IS than incorporation technique of the silage/digestate into the in BR and AD. soil. The conclusion is that organic stockless farms If the field experiment would have continued for a could improve circulation of N by collecting the full 6-year cycle or more, it is possible that the N residual biomass after harvest and thereby reduce the balances in BR and AD would become increasingly potential risk for N leakage and N emissions. These larger than in IS, due to an accumulated effect of aspects require further research about how strategic higher quantities of N fixation and targeted applica- biomass N management influences N losses at differ- tion of silage/digestate to N-demanding non-legume ent processes and at the entire cropping system level. crops. The strategic management of residual biomass A comparison between the management systems in in BR and AD would thus sustain crop yields with low terms of the energy use and greenhouse gas emissions risk of long-term depletion of soil N fertility, which related to transportation and storage of the biomass might be the case in IS where the N balance is less resources would also be relevant for a full assessment positive. In addition, BR and AD can also be expected of the environmental benefits. to reduce the risks for NO leakage and gaseous N Acknowledgements We acknowledge the Swedish Research emissions compared to the in situ application of Council Formas and the Swedish University of Agricultural residual biomass in IS, where more N would be Sciences for funding of the research. This field study was carried mineralised in autumn and exposed to losses during out within the Swedish Infrastructure for Ecosystem Science times of low crop N acquisition (Hansen et al. 2004; (SITES) Lonnstorp Research Station in Alnarp. We thank Ph.D. 123 Nutr Cycl Agroecosyst (2018) 112:165–178 177 Emma Kreuger, Lund University, the research station technical De Ponti T, Rijk B, Van Ittersum MK (2012) The crop yield gap manager Erik Rasmusson, field assistant Lina Hirsch and between organic and conventional agriculture. Agric Syst university lecturer Sven-Erik Svensson for technical support. 108:1–9 De Ruijter FJ, Huijsmans JFM, Rutgers B (2010) Ammonia Open Access This article is distributed under the terms of the volatilization from crop residues and frozen green manure Creative Commons Attribution 4.0 International License (http:// crops. Atmos Environ 44(28):3362–3368 creativecommons.org/licenses/by/4.0/), which permits unre- Deckers JA, Nachtergaele F, Spaargaren OC (1998) World stricted use, distribution, and reproduction in any medium, reference base for soil resources. Food and Agriculture provided you give appropriate credit to the original Organization of the United Nations, Rome author(s) and the source, provide a link to the Creative Com- Eurostat (2015) Agriculture—organic farming—organic crop mons license, and indicate if changes were made. area. http://ec.europa.eu/eurostat/web/agriculture/data/ database. Accessed 08 Aug 2017 Fowler D, Coyle M, Skiba U, Sutton MA, Cape JN, et al (2013) The global nitrogen cycle in the twenty-first century. Philos Funding Funding was provided by Swedish Research Council Trans R Soc B 368(1621):20130165 FORMAS (Grant No. 2010-7733-18410-52). 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Nutrient Cycling in AgroecosystemsSpringer Journals

Published: Jul 31, 2018

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