Legumes for mitigation of climate change and the provision of feedstock for biofuels and biorefineries. A review
- 2.9k Downloads
Humans are currently confronted by many global challenges. These include achieving food security for a rapidly expanding population, lowering the risk of climate change by reducing the net release of greenhouse gases into the atmosphere due to human activity, and meeting the increasing demand for energy in the face of dwindling reserves of fossil energy and uncertainties about future reliability of supply. Legumes deliver several important services to societies. They provide important sources of oil, fiber, and protein-rich food and feed while supplying nitrogen (N) to agro-ecosystems via their unique ability to fix atmospheric N2 in symbiosis with the soil bacteria rhizobia, increasing soil carbon content, and stimulating the productivity of the crops that follow. However, the role of legumes has rarely been considered in the context of their potential to contribute to the mitigation of climate change by reducing fossil fuel use or by providing feedstock for the emerging biobased economies where fossil sources of energy and industrial raw materials are replaced in part by sustainable and renewable biomass resources. The aim of this review was to collate the current knowledge regarding the capacity of legumes to (1) lower the emissions of the key greenhouse gases carbon dioxide (CO2) and nitrous oxide (N2O) compared to N-fertilized systems, (2) reduce the fossil energy used in the production of food and forage, (3) contribute to the sequestration of carbon (C) in soils, and (4) provide a viable source of biomass for the generation of biofuels and other materials in future biorefinery concepts. We estimated that globally between 350 and 500 Tg CO2 could be emitted as a result of the 33 to 46 Tg N that is biologically fixed by agricultural legumes each year. This compares to around 300 Tg CO2 released annually from the manufacture of 100 Tg fertilizer N. The main difference is that the CO2 respired from the nodulated roots of N2-fixing legumes originated from photosynthesis and will not represent a net contribution to atmospheric concentrations of CO2, whereas the CO2 generated during the synthesis of N fertilizer was derived from fossil fuels. Experimental measures of total N2O fluxes from legumes and N-fertilized systems were found to vary enormously (0.03–7.09 and 0.09–18.16 kg N2O–N ha−1, respectively). This reflected the data being collated from a diverse range of studies using different rates of N inputs, as well as the large number of climatic, soil, and management variables known to influence denitrification and the portion of the total N lost as N2O. Averages across 71 site-years of data, soils under legumes emitted a total of 1.29 kg N2O–N ha−1 during a growing season. This compared to a mean of 3.22 kg N2O–N ha−1 from 67 site-years of N-fertilized crops and pastures, and 1.20 kg N2O–N ha−1 from 33 site-years of data collected from unplanted soils or unfertilized non-legumes. It was concluded that there was little evidence that biological N2 fixation substantially contributed to total N2O emissions, and that losses of N2O from legume soil were generally lower than N-fertilized systems, especially when commercial rates of N fertilizer were applied. Elevated rates of N2O losses can occur following the termination of legume-based pastures, or where legumes had been green- or brown-manured and there was a rapid build-up of high concentrations of nitrate in soil. Legume crops and legume-based pastures use 35% to 60% less fossil energy than N-fertilized cereals or grasslands, and the inclusion of legumes in cropping sequences reduced the average annual energy usage over a rotation by 12% to 34%. The reduced energy use was primarily due to the removal of the need to apply N fertilizer and the subsequently lower N fertilizer requirements for crops grown following legumes. Life cycle energy balances of legume-based rotations were also assisted by a lower use of agrichemicals for crop protection as diversification of cropping sequences reduce the incidence of cereal pathogens and pests and assisted weed control, although it was noted that differences in fossil energy use between legumes and N-fertilized systems were greatly diminished if energy use was expressed per unit of biomass or grain produced. For a change in land use to result in a net increase C sequestration in soil, the inputs of C remaining in plant residues need to exceed the CO2 respired by soil microbes during the decomposition of plant residues or soil organic C, and the C lost through wind or water erosion. The net N-balance of the system was a key driver of changes in soil C stocks in many environments, and data collected from pasture, cropping, and agroforestry systems all indicated that legumes played a pivotal role in providing the additional organic N required to encourage the accumulation of soil C at rates greater than can be achieved by cereals or grasses even when they were supplied with N fertilizer. Legumes contain a range of compounds, which could be refined to produce raw industrial materials currently manufactured from petroleum-based sources, pharmaceuticals, surfactants, or food additives as valuable by-products if legume biomass was to be used to generate biodiesel, bioethanol, biojet A1 fuel, or biogas. The attraction of using leguminous material feedstock is that they do not need the inputs of N fertilizer that would otherwise be necessary to support the production of high grain yields or large amounts of plant biomass since it is the high fossil energy use in the synthesis, transport, and application of N fertilizers that often negates much of the net C benefits of many other bioenergy sources. The use of legume biomass for biorefineries needs careful thought as there will be significant trade-offs with the current role of legumes in contributing to the organic fertility of soils. Agricultural systems will require novel management and plant breeding solutions to provide the range of options that will be required to mitigate climate change. Given their array of ecosystem services and their ability to reduce greenhouse gas emissions, lower the use of fossil energy, accelerate rates of C sequestration in soil, and provide a valuable source of feedstock for biorefineries, legumes should be considered as important components in the development of future agroecosystems.
KeywordsLegumes Biological N2 fixation Carbon sequestration Greenhouse gases Biorefinery Biofuels
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .1
2.1 Mitigation of green-house gas emissions . . . . . . . 4
2.1.1 CO2 emissions arising from N-fertilizer production and symbiotic N2 fixation. . . . . . . . . . . 4
2.1.2 N2O emissions. . . . . . . . . . . . . . . . . . . . . 5
220.127.116.11 N2O emissions from legume and N-fertilized systems. . . . . . . . . . . . . . .6
18.104.22.168 N2O emissions derived from legume residues. . . . . . . . . . . . . . . . . . . . . 10
2.2 Comparisons of energy use by legume-based and N-fertilized systems. . . . . . . . . . . . . . . . . . . . . . 12
2.3.1 Legume effects on soil carbon sequestration. . . . . . . . . . . . . . . . . . . . . . . 14
2.3.2 Pastures. . . . . . . . . . . . . . . . . . . . . . 15
2.3.3 Cropping sequences. . . . . . . . . . . . . . 16
2.3.4 Woody perennial legumes. . . . . . . . . . 18
3. A role for legumes to replace fossil resources?. . . . . .19
3.1 Legume biomass yields potentials and constituents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20
3.2 Legumes as biorefinery feedstocks for biofuels, materials, and chemicals. . . . . . . . . . . . . . . . . . 22
3.2.1 Biofuels. . . . . . . . . . . . . . . . . . . . . . . . . . 24
22.214.171.124 Bioethanol. . . . . . . . . . . . . . . . . . . 24
126.96.36.199 Biodiesel. . . . . . . . . . . . . . . . . . . .25
3.2.2 Biogas and digestate for fertilizer. . . . . . . . . 27
3.2.3 Thermochemical conversion for production of heat, electricity, and biochar. . . . . . . . . . . . 28
3.2.4 Materials and chemicals. . . . . . . . . . . . . . . . 29
4. Concluding remarks. . . . . . . . . . . . . . . . . . . . . . .29
5. Acknowledgments. . . . . . . . . . . . . . . . . . . . . . . . 30
Biomass from agriculture, forestry, and marine environments is expected to play an important role in replacing scarce energy sources in the transition from a fossil economy to a biobased economy (IEA 2009; Bessou et al. 2010; Fairley 2011). A biobased economy is defined as the replacement of fossil fuels in the production of industrial chemicals, transportation fuels, electricity, heat, and other products by biomass in so-called biorefinery concepts. The political and scientific arguments for this transition are multiple: diversification of energy sources due to declining fossil reserves (energy security), less dependence on fossil raw material exporters (energy security), new uses of biomass to stimulate rural development, and the reduction of greenhouse gases (GHG) to mitigate global climate change (Bessou et al. 2010; Langeveld and Sanders 2010).
The Global Warming Potential (GWP) of some major greenhouse gases and historic trends in changes in their atmospheric concentrations
GWPa (100 year)
Year and surface air concentration (ppm on a volume basis)
Rising concentrations of CO2 are the main concern since CO2 emissions from the combustion of fossil fuels account for >50% of the estimated increased greenhouse effect (IPCC 2007). The agricultural contribution to the global GHG emission has been estimated to be 13.5% of the total GHG CO2-equivalents (IPCC 2007) and is derived from (1) the use of fossil energy for the manufacture and transport of fertilizer nitrogen (N), other fertilizers and agrichemicals, and the consumption of petroleum-based fuels for on-farm machinery operation; (2) changes in land-use that release GHG due to the net decomposition of soil organic matter, or when the carbon (C) in the wood is converted to CO2 by burning when land is deforested for cropping or livestock; (3) the release of N2O from soil as a result of inefficiencies in crop recovery of fertilizer and other sources of N; and (4) CH4 released from the enteric digestion of forage within the rumen of livestock, on-farm manure management, and rice (Oryza sativa) cultivation on wetlands (Jenkinson 2001; Crews and Peoples 2005; Bessou et al. 2010). To mitigate climate change from agriculture, it is important to adopt strategies that reduce these sources of GHG emissions.
Leguminous crops (e.g., field pea, Pisum sativum; faba bean, Vicia faba; chickpea, Cicer arietinum; soybean, Glycine max), forages [e.g., clovers, Trifolium spp.; alfalfa (lucerne), Medicago sativa], trees, and shrubs (e.g., species of Leucaena, Callinadra, Gliricidia, Acacia, and Sesbania) provide a range of agroecosystems services for humans. These include (1) N (protein)-rich foods, feeds, and green-manures; (2) a lowering of the need for fertilizer N to support crop and pasture production as the result of contributions of symbiotically fixed dinitrogen (N2) to the growth of the legume host, and the subsequent improvement of soil fertility through inputs of legume organic residues (Rochester et al. 2001; Jensen and Hauggaard-Nielsen 2003; Crews and Peoples 2004); (3) improvements in soil structural characteristics (Rochester et al. 2001; McCallum et al. 2004); (4) direct impacts on soil biology by reducing the incidence of cereal root pathogens, and/or encouraging beneficial microorganisms (Kirkegaard et al. 2008; Osborne et al. 2010); (5) diversification of species grown in rotations reducing the requirement for pesticides and other agrichemicals, encouraging systems resilience and biodiversity (Jensen and Hauggaard-Nielsen 2003; Köpke and Nemecek 2010); (6) deep-rooted perennial legumes reducing the risk of groundwater contamination by nitrate (NO3−), or the development of dryland salinity, due to their ability to grow and extract water all year round (Angus et al. 2001; Entz et al. 2001; Lefroy et al. 2001); and (7) the revegetation and reclamation of degraded or cleared lands (Thrall et al. 2005; Chaer et al. 2011; De Faria et al. 2011). Even though legumes obtain N through biological nitrogen fixation (BNF), rather than through fossil energy-derived fertilizer N, they are generally not considered as a mitigation option (Smith et al. 2007). With the exception of soybean, legumes are also usually not regarded as particularly relevant as biomass crops or as crop components as feedstock in biorefinery for biofuel and/or biomaterials production (Venendaal et al. 1997; Brehmer et al. 2008; Bessou et al. 2010).
This paper reviews the potential new roles for the use of legumes in future agriculture to (1) reduce the emissions of the key GHG CO2 and N2O; (2) lower fossil energy consumption during the production of food, forage, and fiber; (3) increase the sequestering of organic C in soils; and (4) provide an energy-efficient biomass source for biorefineries to produce biofuels, chemicals, and materials to replace fossil-resource-derived products.
2 The potential for legumes to mitigate climate change
2.1 Mitigation of greenhouse gas emissions
As GHG concentrations rise, it has become increasingly important to account for losses of CO2 and N2O arising from agriculture (Table 1). Emissions of these gases may occur either directly as the result of farming activities (e.g., cultivation and harvesting) or indirectly during the production and transport of required inputs (e.g., fertilizers, herbicides, and pesticides). The potential role of N2-fixing legumes in reducing GHG emissions through direct effects on CO2 and N2O fluxes in the production of high-protein grain and forage will be compared to the applications of fertilizer N in the following sections.
2.1.1 CO2 emissions arising from N fertilizer production and symbiotic N2 fixation
A century after its invention, the Haber–Bosch process of ammonia (NH3) production essentially remains unchanged. Ammonia is synthesized from a 3:1 volume mixture of H2 and N2 at elevated temperature and pressure in the presence of an iron catalyst (Smil 2001). All the N2 used is obtained from the air and the H2 can be obtained by either (a) partial oxidation of heavy fuel oil or coal, or (b) steam reforming of natural gas or other light hydrocarbons (natural gas liquids, liquefied petroleum gas, or naphtha; Smil 2001; Crews and Peoples 2004). It has been estimated that the fossil energy requirements associated with providing the high temperature and pressures and the generation of H2 feedstock required for the synthesis of N fertilizer represents 1–2% of the total world energy consumption (Smil 2001; Jenkinson 2001). It has also been calculated that the varying efficiencies of different processing plants result in the release of between 0.7 and 1.0 kg of CO2–C (equivalent to 2.6–3.7 kg CO2 gas) per kilogram of NH3–N produced (Jenkinson 2001; Jensen and Hauggaard-Nielsen 2003). About half of the CO2 generated during NH3 production will be reused if the NH3 is converted to urea, which is the most widely used form of N fertilizer applied to agroecosystems (67% of total fertilizer N consumed in 2007; IFA 2010). However, once the urea is applied to the soil, it is rapidly hydrolyzed by the enzyme urease to NH3 and the CO2 originally captured during urea production will also be released (Jenkinson 2001). Consequently, the annual global fertilizer production of around 100 Tg N (1 Tg = 1012 g; IFA 2010) manufactured with an efficiency of 2.6–3.7 kg CO2 generated per kilogram of N synthesized represents around 300 Tg of CO2 being released into the atmosphere each year.
There are nearly 18,000 legume species, many of major agricultural importance. Legumes range from herbaceous annuals plants to gigantic trees (e.g., Moreton Bay chestnut, Castanospermum australe). Many legumes possess the ability to form nitrogen-fixing symbioses with soil bacteria broadly called “rhizobia” (see Ferguson et al. 2010 for an up-to-date review). The symbiosis is initiated through an exchange of chemical signals; specifically legume roots secrete not only sugars but also flavones and isoflavones. These exist as “chemical cocktails” of “rhizobial” gene activators and repressors, representing part of host specificity. For example, a bacterium that normally induces nodules in white clover will not nodulate or fix nitrogen with soybean, and vice versa. The flavone signal also works as a chemoattractant to “rhizobia” which then attach to root hairs in the susceptible zone right behind the growing root tip region [there are some exceptions to root hair nodulation process—for example groundnut (Arachis hypogae) where rhizobia rely upon entry through root cracks]. Here, they activate bacterial genes (nod and nol genes) that cooperate to synthesize and secrete a nodulation (Nod) factor. Nod factor perception leads to two interrelated processes, namely root hair/root cortex infection, and cortical and pericycle cell divisions. The combined meristems form the nascent root nodule, well-plumbed with a bifurcated vascular system, designed to provide photosynthate (usually as sucrose-derived malate; Udvardi et al. 1988) and to transport the products of symbiotic N2 fixation back to the plant. The young cells inside the emerging nodule become invaded by the “rhizobia”, which now differentiate into N2-fixing bacteroids. Bacterial N2 fixation genes express the components of the nitrogenase enzyme complex (NifH, NifD, and NifK), that together with critical genes for regulation, iron and molybdenum supply, electron transport facilitate the conversion of atmospheric N2 into NH3 (ammonia) which in turn is assimilated within the nodule cell cytoplasm to glutamine. Glutamine in turn serves as the N donor for the subsequent synthesis of a complex set of amino acid and or N transport compounds (such as ureides in soybean, or glutamine and asparagine in temperate legumes; Peoples and Herridge 1990). Nodule development is regulated internally by an “autoregulation of nodulation” (AON) circuit (cf., Gresshoff et al. 2009; Reid et al. 2011) and externally by stress as well as nitrate (Carroll et al. 1985; Ferguson et al. 2010).
Current global estimates of annual amounts of N2 fixed by agricultural legumes range between 33 and 46 Tg N (Herridge et al. 2008). Assuming that the N2 fixation process respires on average 10 g more CO2 from a legume’s nodulated root system for every gram of N assimilated than plants utilizing fertilizer or soil N for growth, then between 350 and 500 Tg of additional CO2 might be respired from the nodulated roots of legumes each year as a direct result of BNF.
Globally, the amount of CO2 respired from the root systems of N2-fixing legumes could be comparable to, or higher than, the CO2 generated during N-fertilizer production. However, the CO2 respired from the nodulated roots of legumes originated from the atmosphere via photosynthesis, so any of the CO2 that was not subsequently recaptured by the plant and eventually escaped from the legume canopy to the atmosphere would essentially be C neutral. By contrast, all the CO2 released during the synthesis of fertilizer N would be derived from fossil energy and represents a net contribution to atmospheric concentrations of CO2.
2.1.2 N2O emissions
About 5% of the total atmospheric greenhouse effect is attributed to N2O of which 60% to 70% of the annual global anthropogenic emissions have been calculated to come from animal and crop production (Mosier 2001; IPCC 2007). While N2O can be generated in the process of nitrification where nitrite is converted to NO3−, N2O losses as the result of denitrification are generally considered to be the more important source in most cropping and pasture systems (Rochester 2003; Peoples et al. 2004b; Soussana et al. 2010). Denitrification occurs when the soil is very moist and O2 supply is restricted, a suitable mineralizable organic C is present to be used as an energy source by denitifying microbes, and there are high concentrations of NO3− (Peoples et al. 2004b; Stehfest and Bouwman 2006). Many species of soil bacteria are able to survive in anoxic conditions by using the denitrification process. Essentially, NO3− is substituted for O2 as a respiratory electron acceptor; the NO3− is reduced to nitrite and in sequence to N2O and N2. The bulk of the gaseous losses will be as N2, but the small proportion of the total emissions in the form of N2O (i.e., the ratio of N2O/N2) can be affected by many different variables such as N application rate, soil organic C content, soil pH, and texture (Rochester 2003; Stehfest and Bouwman 2006; Peoples et al. 2009b). This illustrates the potential difficulty in reliably measuring or predicting specific losses of N2O from what is essentially a very complex, transient, and variable process.
The IPCC (2006) suggested that for every 100 kg of fertilizer N added to the soil, on average 1.0 kg of N can be expected to be emitted as N2O. As a GHG, N2O absorbs approximately 300 times as much infra-red radiation per kilogram as CO2 (Table 1), and since an emission of 1.0 kg N2O–N equates to 1.57 kg N2O gas, the impact of every kilogram of N2O–N released would be equivalent to around 470 kg CO2. In addition to this amount, the IPCC includes further sources of N2O as 1.0% of the N deposited on the soil surface as residues (IPCC 2006). For many years, the IPCC reference manual (IPCC 1996) and the good practice guide for inventories (IPCC 2000) (erroneously) considered 1.25 kg of N2O–N to be emitted for every 100 kg of biologically fixed N2. In other words, if BNF by legumes was responsible for emissions from the soil (rhizosphere) or from the nodules of this magnitude during growth, with subsequent additional losses when organic N in above-ground and below-ground legumes residues were mineralized, then legumes would be no more favorable than N fertilizer in terms of GHG emissions. Although the recent IPCC publications no longer includes BNF as a source of N2O (IPCC 2006), some countries around the world continue to utilize the former recommendations. The following sections review N2O emissions both during a legume’s growth cycle, and subsequently from legume residues, and compare the magnitude of these N2O losses with fertilized systems.
2.1.3 N2O emissions from legume and N-fertilized systems
Examples of total N2O emissions from field-grown legumes, N fertilized grass pastures and crops, or un-fertilized soils in North and South America, Europe, South Asia, East Asia, Australia, and New Zealand
Category and species
Number of site-years
Total N2O emission per growing season or year (kg N2O–N ha−1)
Pure legume standsa
Mixed pasture swarda
Mean of all legumes
Mean of fertilized systems
No N fertilizer or legume
Crop(s) in 2003
N fertilizer applied (kg N ha−1)
N2O emissions (kg N2O–N ha−1)
Crop(s) in 2004
N fertilizer applied (kg N ha−1)
N2O emissions (kg N2O–N ha−1)
Nitrous oxide fluxes normalized by the optical density (o.d.) of growth medium of several Bradyrhizobium spp. strains recommended for various grain and forage legumes (Alves et al., unpublished data)
Legume host species
N2O flux (μmol N2O h−1 o.d.−1)
BR 2003/2811 (mixture)
BR 85 (CPAC 7)
BR 86 (CPAC 15)
Soybean shoot dry matter (DM) and N accumulation, and cumulative N2O emissions from soil over 64 days
Shoot DM (g plant−1)
Shoot N (g N plant−1)
N2O emission (mg N pot−1)
Soybean cv Conquista
Non-nod soybean cv T-201
Further evidence that N2O emissions are unlikely to be directly linked to BNF comes from investigations by Jantalia et al. (2008) in Brazil where N2O fluxes were monitored in different double-cropping systems (i.e., one summer crop and one winter crop grown in each year) over two consecutive years (Table 3). In that study, the soybean in the soybean–wheat sequence fixed between 100 and 200 kg N ha−1 in above-ground biomass, while in neighboring plots, the soybean–vetch sequence, the total amounts of N fixed by both legume crops represented 165 to 280 kg N ha−1 (Jantalia et al. 2008). Yet despite the large inputs of fixed N by the legumes, their measured emissions of N2O were not significantly different from the N2O fluxes coming from maize–wheat or sorghum (Sorghum bicolor)–wheat sequences receiving between 45 and 60 kg fertilizer N ha−1 (Table 3).
Shifts in the species composition of soil microbial populations and a high microbial diversity commonly detected in the legume rhizosphere (Lupwayi and Kennedy 2007; Osborne et al. 2010) could also be contributing factors to the high N2O flux since the release of readily metabolizable substrates into the legume rhizosphere stimulates microbial growth and activity and promotes oxygen consumption. This could conceivably create temporary anaerobic microsites in soil that would favor denitrification (Bertelsen and Jensen 1992; Lemke et al. 2007). There is also some evidence to suggest that the increased populations of microbes associated with the root systems of N2-fixing legumes include denitrifying bacteria (Zhong et al. 2009).
Emissions of N2O tend to be lower under legumes than N-fertilized crops and pastures, particularly when commercially relevant rates of N fertilizer are applied. This undoubtedly reflects differences in both the relative size of the N inputs and the concentrations of soil NO3− available to be denitrified. There is little evidence to support a direct association between BNF and N2O emissions from legume fields. While the source(s) of N responsible for the N2O emitted during a legume’s growing season have not been identified, it is likely that the N2O is derived from the denitrification of NO3− that often accumulates in soil either as the result of inefficient recovery of NO3− by legume roots or the mineralization of labile sources of legume N released from the nodulated roots and fallen leaf material (Bertelsen and Jensen 1992; Rochette and Janzen 2005).
2.1.4 N2O emissions derived from legume residues
The decomposition and mineralization of organic N in legume residues into inorganic forms following a legume phase is a microbial-mediated process associated with the breakdown of organic compounds being used to provide the soil microbes with a C source for respiration and growth (Fillery 2001). Much of the simple organic N released from legume residues is rapidly assimilated (immobilized) by the soil microbial population (Bremer and van Kessel 1992; Murphy et al. 1998; Peoples et al. 2009b). Inorganic N (mineral N—ammonium, NH4+, and NO3−) only accumulates in soil if the amounts of N released from residues exceed the C-limited microbial requirement for N for growth. Since legume tissues tend to have higher N contents and lower C/N ratios than non-leguminous material, legume residues are more likely to result in net mineralization and a build-up of inorganic N in soil (Peoples and Herridge 1990; Kumar and Goh 2000). Concentrations of inorganic N in field soils are generally observed to be higher when sowing a subsequent crop in a rotation if it follows a legume crop or pasture than a cereal (Chalk 1998; Fillery 2001; Jensen and Hauggaard-Nielsen 2003). This can often be related to the amounts of legume N accumulated during a pasture phase or the amounts of crop legume N remaining in residues following grain harvest (Evans et al. 2003; Peoples et al. 2001, 2004a).
Since legume residues provide a source of easily decomposable C substrate for denitrifying microorganisms, emissions of N2O could occur either during the process of nitrification of N derived from legume residues or as a result of the denitrification of the NO3− pool that subsequently builds up in the soil. In general terms, the susceptibility of N derived from legume residues to loss processes is determined by how well the release (supply) of mineralized N is synchronized with the demand for N by following crops (Crews and Peoples 2005).
The fate of legume or fertilizer N is often measured using 15N-labeled materials. These studies indicate that while a much lower proportion of the N originally present in legume residues is usually taken up by a subsequent wheat, rice, or maize crop (on average 15–20%; Peoples et al. 1995a; Fillery 2001; Peoples et al. 2009b) than from fertilizer (on average 30–40%; Peoples et al. 1995a; Krupnik et al. 2004; Crews and Peoples 2005), considerably more legume N is retained in the soil system than fertilizer N (60% vs. 30%, respectively; Crews and Peoples 2005; Peoples et al. 2009b). While the extent of losses will be influenced by whether the system is rainfed or irrigated, average losses from cereals appear to be in the order of 10–20% for legume N and 30–40% for fertilizer (Peoples et al. 2004b, 2009b). Meta-analysis of 15N field experiments has shown that the extent of losses is driven by the size of the N inputs regardless of the source and has indicated that total losses of legume N tend to be less than from fertilizer when both are applied at rates of <125 kg N ha−1 (Gardner and Drinkwater 2009). While quite a lot may be known about total losses of legume or fertilizer N, it is more difficult to generalize about denitrification as the pathway of N loss, or more specifically about how much of the losses from above- and below-ground legume residues might be in the form of N2O.
Another key period of risk for N losses from legume systems in the cool–temperate climates of the northern hemisphere occurs during winter and early spring thaw since high rates of nitrification can occur in cool wet soils (Magid et al. 2001), while any plant roots present will be unlikely to be actively assimilating the NO3− mineralized from legume residues (Jensen and Hauggaard-Nielsen 2003). Emissions of N2O collected from either lentil or field pea residues immediately following spring snow melt were not significantly different from neighboring wheat stubble plots in Saskatchewan (0.1 kg N2O–N ha−1) and Alberta, Canada (0.4 to 0.6 kg N2O–N ha−1), suggesting that N2O emissions by crop legume residues remaining from the previous year can be negligible (Lemke et al. 2007). However, the situation was found to be very different elsewhere in Canada following the autumn termination and plough-down of N-rich alfalfa biomass where significantly higher fluxes of N2O were measured during winter and early spring (5.38 kg N2O–N ha−1) than detected coming from a bare soil during the same period (2.84 kg N2O–N ha−1; Wagner-Riddle et al. 1997). There was also evidence that these elevated emissions may persist for up to 2 years after removal of the alfalfa stand (Wagner-Riddle and Thurtell 1998). By way of comparison, the initial losses of N2O following alfalfa plough-down over the winter–early spring period was more than 3-fold greater that the N2O emissions from barley, canola, or maize crops (1.05–1.31 kg N2O–N ha−1) that were subsequently grown in different treatment plots at the same experimental sites that were fertilized with between 75 and 100 kg N ha–1 (Wagner-Riddle et al. 1997).
Another situation analogous to the alfalfa plough-down example that would be conducive to generating high concentrations of soil NO3− susceptible to denitrification losses occurs when fresh legume biomass is either green-manured (i.e., either physically incorporated into soil or used as mulch) or brown-manured (killed prior to maturity with a knock-down herbicide). Certainly higher N2O emissions have been observed coming from soil under a maize crop in the UK where 3.9 Mg ha−1 of over-wintering faba bean foliage containing 180 kg N ha−1 (C/N ratio = 12) had been green-manured prior to sowing (0.79 kg N2O–N ha−1 over 65 days) than detected coming from the nil residue control treatment (0.23–0.31 kg N2O–N ha−1; Baggs et al. 2003). Fluxes of N2O during the growth of lowland (wetland/flooded) rice in India were also considerably higher from sesbania (Sesbania aculeate) green-manured plots (11.5 kg N2O–N ha−1 over 119 days) receiving 40 Mg ha−1 of shoot material containing 176 kg N ha−1 (C/N ratio = 18) than where 6 Mg ha−1 of wheat stubble containing 27 kg N ha−1 (C/N ratio = 94) were either retained (6.6 kg N2O–N ha−1) or removed (5.0 kg N2O–N ha−1; Aulakh et al. 2001). While green-manuring may be a good strategy to economize (financially) on N fertilizer, it is clearly a risky practice with regards to GHG emissions. In the case of the study of Aulakh et al. (2001), losses of N2O from the green-manured plots were equivalent to where 120 kg N ha−1 was supplied to rice as N fertilizer, although a lower proportion of the applied N was calculated to be lost as N2O from the sesbania mulch (6.5%) than from the N fertilizer (8.8%).
There is a real risk of elevated N2O emissions from legume residues. Low C/N ratio of leguminous material can potentially stimulate N2O losses as they are a source of N for rapid mineralization and nitrification, and legume residues provide a source of easily decomposable C substrate for microorganisms to support the denitrification of NO3− that accumulates in soil. Clearly, there are situations where large amounts of labile legume organic N is returned to soil such as when legume-based pastures have been terminated prior to cropping, or where legumes are used for green-manure. Under these conditions, N2O emissions can be comparable to, or greater than, where crops receive N fertilizer (Wagner-Riddle et al. 1997; Aulakh et al. 2001). However, the senesced, vegetative stubble that typically remains after grain harvest of legume crops is unlikely to represent a major source of N2O loss above normal background soil emissions (Lemke et al. 2007) since the quantities of organic N returned to the soil tend to be relatively small and the C/N ratio of the residues are less favorable for rapid mineralization to build up high concentrations of soil NO3− (Kumar and Goh 2000; Fillery 2001; Peoples et al. 2009b).
2.2 Comparisons of energy use by legume-based and N-fertilized systems
Fossil energy consumed in pea, barley, and forage crops in Denmark and the amount of product dry matter (DM) harvested (Peoples et al. 2009b)
Direct energy in diesel use (MJ ha−1)
N fertilizer (kg N ha−1)
N fertilizer (MJ ha−1)
Seeds and non-N fertilizers (MJ ha−1)
Pesticides (MJ ha−1)
Total fossil energy use (MJ ha−1)
Harvested product (kg DM ha−1)
Energy input (MJ kg DM−1)
Comparisons of the amounts of N fertilizer used and energy consumed in the production of a range of legume and non-legume grain crops, and the amount of product dry matter (DM) harvested in the cropping systems of Switzerland (Köpke and Nemecek 2010) and North America (Zentner et al. 2004; Rathke et al. 2007)
N fertilizer applied (kg N ha−1)
Total energy use (MJ ha−1)
Harvested product (kg DM ha−1)
Energy input (MJ kg DM−1)
N fertilizer applied (kg N ha−1)
Total energy use (MJ ha−1)
Harvested product (kg DM ha−1)
Energy use efficiency (MJ kg DM−1)
Location and rotation with (+) or without (−) a legume crop
Canton Vaud, Switzerland
Castilla y Léon, Spain
Annual energy use
Saskatchewan, Canada #1a
Saskatchewan, Canada #2a
Saskatchewan, Canada #3a
Annual energy use
The largest energy savings occurred where a legume crop was grown every second year (field pea and soybean in Switzerland, lentil, Lens culinaris, at Swift Current Saskatchewan, and soybean at Lincoln, Nebraska) rather than just once in the rotation (Table 4). Whether this intensity of legume use is a wise strategy remains to be seen given the increased risk of accelerating the build-up of legume diseases or the development of herbicide resistance by weeds.
Recently, the influence of introducing grain legumes into a cereal-based cropping system in Canada has been evaluated by including the CO2 equivalent emissions (CO2e) derived from GHG release associated with farming activities, in addition to direct energy costs to compare the “C footprint” of different cropping sequences (Gan et al. 2011). Averaged across five site-years of data, the C footprint of durum wheat grain produced in a cereal–cereal–durum system was calculated to represent 0.42 kg CO2e per kilogram of grain harvested. This compared to estimates of 0.30 kg CO2e per kilogram of durum grain when the durum was preceded by a grain legume (chickpea, lentil, or pea) in the previous year. In other words, the C footprint was 28% lower than when the durum crop was grown following a cereal (Gan et al. 2011).
The reduced energy use and lower C footprint resulting from growing legumes largely reflected the removal of the need to apply N fertilizer and the subsequently lower N fertilizer requirements for the crops grown following the legumes. However, the total energy balance was also assisted by a lower use of agrichemicals since the diversification of the cropping sequence reduced the incidence of cereal pathogens and pests and changed weed populations, although it should be noted that the overall impact of legumes on energy use was greatly diminished if comparisons with N-fertilized systems were calculated on the basis of the amounts of biomass or grain produced.
2.3 Soil carbon sequestration and land use change
Soils contain large amounts of C in both inorganic and organic forms. Inorganic forms of C are derived from geologic or soil parent material sources and are usually present in soils as carbonates and bicarbonates. The amount of soil organic C (SOC) present in soil can represent from <20 to >200 Mg C ha−1 in the top 30 cm of soil (Arrouays et al. 2001; Hoyle et al. 2011). Soil organic C exists in several different pools of varying size. Plant roots, fresh residues, living microorganisms, and macrofauna represent <15% of the total SOC pool, while partially decomposed plant residues, humus (the product of the breakdown of plant residues and soil microbes), and very resistant forms of organic C such as charcoal represent the balance (Dalal and Chan 2001; Hoyle et al. 2011).
While the atmosphere contains around 750 Pg (1 Pg = 1015 g which is equivalent to 1 Gt) of C as CO2, globally the top meter of soil stores approximately 1,500 Pg in SOC and 900–1,700 Pg as inorganic C, and exchanges 60 Pg C each year with the atmosphere (Eswaran et al. 1993). The sheer size of the SOC pool and the annual flux of C passing through the soil are two reasons why so much focus has been given to the possible role sequestering C in soil might play in mitigating GHG emissions (Lal 2004; Soussana et al. 2010).
The amount of C accumulated in a soil is dependent upon the balance between C inputs and losses. In the absence of the transport and incorporation of large amounts of offsite organic wastes or biochar, new C can only be introduced to the soil via photosynthesis by plants. Consequently, any farm management practice that enhances total plant production and the retention of plant shoot and root residues, and/or reduces C losses can theoretically contribute to increasing soil C content (Hoyle et al. 2011). There is also an upper limit to the annual C inputs in plant residues, particularly in rainfed agriculture, where the availability of water and nutrient supply constrains photosynthesis and plant productivity.
Losses of C from soil result from leaching of dissolved and particulate C, wind and water erosion, and the microbial decomposition and associated mineralization processes that convert C in fresh plant residues and SOC into CO2 (Dalal and Chan 2001; Kindler et al. 2011). The rate of microbial decomposition is heavily influenced by climate (Christopher and Lal 2007) and soil texture, factors that provide physical protection for SOC (Soussana et al. 2004, 2010; Hoyle et al. 2011), the source of organic residues (Gregorich et al. 2001; Rochester 2011), and farming practices, such as cultivation that increases soil disturbance and exposes plant residues and SOC to microbial decomposition (Dalal and Chan 2001; Christopher and Lal 2007). Depending upon climatic conditions, between 50% and 75% of the C in plant residues can be expected to be respired as CO2 by microbes during the first year of decomposition (Hoyle et al. 2011).
Changes in land use could shift the relative balance between C inputs and losses in either direction depending on the nature of the change. All soils will eventually attain a dynamic equilibrium level when soil C gains equal soil C losses (i.e., a steady state when the rate of change in SOC is zero) which represents the upper limit of the amount of C that can be sequestered as defined by the inherent physiochemical properties of the different soil pools, and factors such as silt and clay content, clay mineralogy, and microaggregation (Soussana et al. 2004; Stewart et al. 2008; Chan et al. 2011). The following sections examine the potential impact that legumes and management can have on SOC.
2.3.1 Legume effects on soil carbon sequestration
Examples of the amounts (kg) of N per 1,000 kg of C and the ratio of C/N expressed on a mass basis of shoot residues of different plant species and selected components of the soil
Residues of different plant speciesa
Different soil componentsc
Soil organic C
Despite the widespread utilization of mixed pastures in Europe based on ryegrass (Lolium multiflorum) and clovers (Trifolium spp.) there are relatively few quantitative studies of the impact of the legume introduction on soil C accumulation. Soussana et al. (2004) used models and data from a large survey of SOC under different land uses and soil types in France (Arrouays et al. 2001) to show that the conversion of short-term N-fertilized grass leys to grass–legume mixtures could result in the accumulation of 10 Mg C ha−1 in the soil over a period of 20 years. Conant et al. (2001) in a review of soil C changes beneath temperate and tropical pastures also identified the inclusion of legumes as one of the many variables that can contribute to increased soil C stocks. Other factors found to influence the accumulation of SOC in pastures and rangelands include (1) climate and whether the pastures are rainfed or irrigated through effects on the net primary productivity of plants and C loss processes; (2) stocking rate and grazing management through defoliation and trampling effects on leaf area, photosynthesis, root biomass and soil microbial communities, and the impact of animal excreta on C and nutrient cycling; (3) the botanical composition of the pasture (i.e., the percentage of total pasture biomass present as grass or legumes); and (4) the age of the pasture and the initial state of the soil system since the rate of change in SOC tends to be greater where the initial soil C stocks are low (e.g., where SOC had been depleted by cropping) than where the soil is closer to its C equilibrium (Conant et al. 2001; Soussana et al. 2004; Klumpp et al. 2009; Soussana et al. 2010; Chan et al. 2011).
Conceptually, whether the forage legume is a perennial or annual could also be important. Although a long-term Australian study failed to detect major differences in the rate of SOC increase in the top 30 cm of soil between rainfed pastures containing the perennial legume alfalfa or annual clovers (Chan et al. 2011), alfalfa would be expected to have a higher potential for C allocation below 30 cm than clovers as a direct result of alfalfa’s much deeper rooting systems (Angus et al. 2001; Peoples and Baldock 2001). Certainly, other investigations have reported significantly greater gains in SOC where alfalfa or other perennial species such as siratro (Macroptilium atropurpureum) or desmanthus (Desmanthus virgatus) were grown compared to where annual pasture or crop legumes had been used (Dalal et al. 1995; Armstrong et al. 1999; Whitbread et al. 2000; Young et al. 2009). Soil C stocks have also been found to be substantially higher (130–134 Mg ha−1, 0–70 cm) when maize was grown in rotation with alfalfa [undersown beneath oats (Avena sativa) and grown for 2.5 years in every 4 years] than under maize monoculture (109–115 Mg ha−1; Gregorich et al. 2001). By employing a solid-state 13C nuclear magnetic resonance analytical technique in this experiment, they demonstrated that <15% of the C in maize residues was retained in soil compared to >50% of the residue C contributed by the alfalfa and oats (Gregorich et al. 2001).
Rotations based on alternating periods of legume-based pastures and cropping are common in the dryland farming systems of Australia (Peoples and Baldock 2001; Kirkegaard et al. 2011). Even though SOC might accumulate under legume-based pastures, total C stocks will inevitably decline when the land is returned to cropping (Dalal et al. 1995; Chan 1997; Persson et al. 2008). In the long term, whether rotating pastures with crops results in net C sequestration, helps maintains SOC stocks, or simply slows the rate of loss of SOC compared to continuously cropped soils will be influenced by the prevailing climatic effects on C inputs and C loss processes, and the frequency or duration of the pasture phase (Grace et al. 1995; Dalal and Chan 2001; Young et al. 2009; Chan et al. 2011).
The potential for soil C sequestration is likely to be greatest in intensively managed permanent pastures and grasslands (Soussana et al. 2004). In the USA, Wright et al. (2004) reported that at low-grazing intensity, the SOC concentration (0–15 cm) under a long-term N-fertilized (350 kg N ha−1 per year) Bermuda grass (Cynodon dactylon)/rye grass pasture in Texas increased by 39% over a 19-year period, whereas SOC was increased by 67% under a Bermuda grass/clover (Trifolium sp.) mixture receiving no N fertilizer. Not only was there a more rapid increase in SOC by changing from a heavily N-fertilized pure grass pasture to a mixed grass/clover sward but this would also have reduced N2O emissions (Ruz-Jerez et al. 1994). Similar legume effects on SOC were observed when yellow-flowering alfalfa (M. sativa ssp. falcata) was inter-seeded into temperate grassland in the range lands of North Dakota (Mortensen et al. 2004) where average annual rates of soil C accumulation (0–100 cm) were increased by 1.56, 0.65 and 0.33 Mg C ha−1 per year 4, 14, and 36 years after alfalfa had been introduced, respectively. These data illustrate the fact that as time passes, C sequestration rates will decrease as a new equilibrium between C inputs and losses is attained.
In South America, grass-only pastures based on Brachiaria (Brachiaria decumbens, Brachiaria humidicola, and Brachiaria brizantha) have been shown to accumulate more SOC than was originally present under the native savanna vegetation (Fisher et al. 2007). The potential to further increase the rates of soil C sequestration with forage legumes has been demonstrated by Fisher et al. (1994) who found that in the eastern savanna of Colombia, soil C accumulation (0–100 cm) was increased by 7.8 Mg ha−1 per year where Arachis pintoi had been introduced into the sward, above that achieved by pure grass alone, despite the legume contributing only 20% of the total root biomass. Another study undertaken in the south of Bahia in Brazil showed that the introduction of Desmodium ovalifolium into a Brachiaria sward approximately doubled the rate of soil C accumulation (0–100 cm) from 0.66 to 1.17 Mg C ha−1 per year over a 9-year period (Tarré et al. 2001).
In some cases, sub-optimal nutrition can severely limit the impact of legumes. A good example of this was in the acidic soils of southeastern Australia where the accumulation of SOC under permanent subterranean clover (Trifolium subterraneum) pastures was found to vary directly with the amount of superphosphate fertilizer applied (Williams and Donald 1957). It was proposed that the rate of build-up of organic matter was constrained by P and S deficiencies in the soils. Alleviating these constraints has also been shown to stimulate the productivity of subterranean clover and greatly increase the amounts of N2 fixed (Peoples et al. 1995b).
There is evidence from many different regions and environments that SOC concentrations can be increased when legumes are included in pastures (e.g., Conant et al. 2001; Wright et al. 2004; Boddey et al. 2009; Chan et al. 2011). The impact of forage legumes appear to be greatest in permanent pastures and with perennial legume species. The effects of perennial legumes on SOC are associated with (1) lower losses of C from their organic residues than from annual legumes as a result of a lower soil water content maintained under perennials reducing microbial activity and respiratory losses of the organic C (Angus et al. 2001; Young et al. 2009), and (2) higher potential inputs of C due to the capacity of perennials to respond to rainfall and grow outside an annual’s normal growing season (Peoples and Baldock 2001). Regardless of whether the legume is an annual or a perennial, a key factor contributing to the rate of SOC build-up will be the nutritional management of pastures (Williams and Donald 1957; Conant et al. 2001; Chan et al. 2011).
2.3.3 Cropping sequences
Cultivation and cropping leads to substantial losses of SOC principally via the decomposition of humus (Dalal and Chan 2001; Christopher and Lal 2007). The conversion of grassland to cropping has been reported to result in a decline in soil C stocks of between 25% and 43% at rates of up to 0.95 Mg C ha−1 per year (Soussana et al. 2004). Consequently, arable soils inevitably have lower levels of SOC than pastures (Arrouays et al. 2001). Until recently, there was a general consensus that a change from conventional tillage (CT) to reduced or zero tillage (ZT) systems that maintain at least 30% of the soil surface cover would lead to positive impacts on SOC in almost any cropping system as the tillage-induced losses of C would be avoided (Christopher and Lal 2007). This was challenged by Baker et al. (2007) who pointed out that in almost all the earlier studies of the effects of tillage the soil was sampled to <30 cm depth only, often <20 cm. Evidence was presented that where soils had been sampled to greater depths (e.g., 80 or 100 cm) more C was found at depth under CT and there was little or no difference between ZT and CT in total SOC down the soil profile (e.g., VandenBygaart et al. 2003). This led Baker et al. (2007) to conclude that the apparent accumulation of soil C observed under ZT compared to CT was largely an artifact of the sampling depth.
Rochester (2011), working in irrigated, minimum-tilled cotton (Gossypium hirsutum) cropping systems in Australia, found that after 10 years the SOC was 7.3 Mg C ha−1 higher to 90 cm (representing a 7% increase) under cropping sequences that included either vetch green-manures or legume crops with relatively low N harvest indices (i.e., low ratio of grain N/total plant N), such as faba bean, compared to non-legume alternatives (wheat–cotton, or continuous cotton). The rotations that included legumes returned 49% more stubble-C and 133% more stubble-N, and around 60% of the additional SOC was located below 30 cm (Rochester 2011).
The results of Diekow et al. (2005) indicate that the desired effects of legumes on SOC can also be achieved when legumes are intercropped with maize as cover-crops under ZT. After 17 years of ZT management, SOC (0–108 cm) ranged between 124 and 128 Mg C ha−1 under a continuous oat–maize sequence in either the absence or presence of N fertilizer (120–180 kg N ha−1), but reached 141 to 149 Mg C ha−1 where lablab (Lablab purpureum) or pigeon pea (Cajanus cajan) were present as inter-crops without N fertilizer. This was not significantly different (P < 0.05) to measures of SOC under the native grassland 31 years earlier (152 Mg C ha−1).
The cropping sequence studies described in this section demonstrated the potential contributions of N2-fixing legumes to SOC stocks under ZT or minimum tillage systems, although it was not always possible to discern from these studies whether the observed beneficial effects of legumes on SOC compared to continuous cereals resulted from a net increase in SOC stocks or simply reflected a slower decline in soil C reserves due to lower losses of organic C. An important discovery common to almost all the studies was that the impact of legumes on the accumulation of soil C under ZT was greatest in the subsoil below 30 cm depth. These observations differ from the original conclusions of Baker et al. (2007). Long-term experiments indicate that it can be difficult for legumes to influence SOC in CT systems (Freixo et al. 2002; Sisti et al. 2004; Boddey et al. 2010), but the data of Barthès et al. (2004) suggested that it might be possible to increase SOC under cultivation provided the inputs of legume organic C and N were greater than the increased losses of SOC stimulated by tillage.
It appears that the net N-balance of the system is a key driver of C stock changes in the soil. When a high N harvest index legume crop like soybean is the only legume present in a rotation, SOC stocks are not maintained because large quantities of N are exported from the field in the grain. By contrast, large amounts of organic C and N are returned to the soil where legume green-manures and cover-crops are utilized, or when legume crops with high vegetative residues are grown regularly.
2.3.4 Woody perennial legumes
It has been estimated that 27% of the total land area in South America is degraded. In Brazil alone, degraded land represents 236 million ha, approximately four times larger than the area dedicated to arable crops (Chaer et al. 2011). At least 50 million ha of the degraded areas in Brazil are former agricultural areas in the central savanna (Cerrado) region, which could potentially be reclaimed for food production. However, much of the remaining areas are located in the deforested hillsides in the Atlantic coastal region where there are few reclamation options. The land was first cleared for sugarcane (Saccharum spp.), then on a much wider scale for coffee (Coffea robusta), and in the last century for charcoal for iron founding (Dean 1995; Boddey et al. 2003). Some of the land has become so degraded that it has been completely abandoned, while in other areas the land is utilized by small landholders for only extremely low productivity crop production or for extensive cattle grazing (Szott et al. 1999). In both cases, it is common practice to burn off the vegetation at least once a year either to facilitate planting or to exploit grass regrowth for forage. Burning exacerbates the loss of nutrients and soil organic matter; erosion becomes a problem and the degradative processes are accelerated. Few attempts have been made to revegetate seriously degraded areas, but over the last 20 years a team at Embrapa Agrobiologia has developed a technology based on the use of fast-growing legume trees from the genus Acacia (Acacia mangium, Acacia holosericea, Acacia angustissima, and Acacia auriculiformis), Albizia lebbeck, Mimosa caesalpiniifolia, Pseudosamanea guachapele, Enterolobium contortisiliiquum, Sclerolobium paniculatum, and Sthryphnodendrum purpureum (Chaer et al. 2011; De Faria et al. 2011).
In cleared land and severely degraded soils, or where new tree legume species are being grown for the first time, populations of rhizobia capable of nodulating tree legumes and forming an effective symbioses tend to be extremely low and tree legumes commonly fail to fix N2 or prosper if planted without appropriate rhizobial inoculation (Galiana et al. 1998; Thrall et al. 2005). Consequently, considerable effort has been placed on isolating and selecting effective rhizobia for a number of woody legume species suitable for use in temperate or tropical environments (Franco and de Faria 1997; Galiana et al. 1998; Thrall et al. 2005).
Recently, three Brazilian studies have highlighted the potential effects of tree legume species on the soil C stocks where they have been used in degraded areas. The first study was at a sloping site where, in 1989, a large amount of the top 40 cm of soil was removed to construct an irrigation dam reducing the SOC stock to 44.5 Mg C ha−1. Originally, the slope was covered by Guinea grass (Panicum maximum). The SOC stocks (0–60 cm) were found to have been increased by 21 Mg C ha−1 (average rate of 1.4 Mg C ha−1 per year) over a period of 15 years by growing M. caesalpiniifolia and by 55 Mg C ha−1 (average rate of 3.7 Mg C ha−1 per year) with A. auriculiformis and P. guachapele (Boddey et al. 2009; Chaer et al. 2011).
The second study, near Angra dos Reis on the coast of Rio de Janeiro, was a steep slope (∼50°) which had been deforested and the top soil removed (Macedo et al. 2008). A recovery operation began in 1991 by planting A. mangium, A. holosericea, and M. caesalpiniifolia. Part of the deforested hillside was left unplanted while 1,000 m further east along the hillside was an area of the original forest. All three sites (unplanted, tree legumes, and original forest) were sampled to a depth of 60 cm. The SOC under the undisturbed Atlantic forest was 108 Mg C ha−1 while the SOC under the unplanted hill and tree legume hill was 65 and 88 Mg C ha−1, respectively.
A further study was undertaken on an experimental area established in degraded secondary forest near the town of Valença (Rio de Janeiro state; Torres et al. 2007). Replicated plots (25 × 50 m) of mixtures of different N2-fixing and non-N2-fixing legume tree species and non-legume trees were planted in different proportions: 0%, 25%, 50%, and 75% N2-fixing legumes. In 6 years, the C in tree biomass (including roots) and litter was estimated to represent 16 Mg C ha−1 where non-N2-fixing trees were planted, and 47 Mg ha−1 in the treatment with 75% N2-fixing legume trees. Soil C stocks (0–60 cm) under the plots with 50% legumes (84 Mg C ha−1) was significantly greater than where no legume was present (71 Mg C ha−1) representing an annual rate of SOC change of 2.17 Mg C ha−1 per year (Torres et al. 2007).
The limited data on tree legume effects on SOC from elsewhere in the world suggest that the Brazilian case studies described above may not be unique. The average annual rates of SOC accumulation in the topsoil (0–15 cm) from leucaena (Leucaena leucocephala) compared to grass pastures or cropping soils in tropical Australia were reported to range from 0.08 to 0.26 and 0.76 Mg C ha−1 per year following 38, 20, and 14 years of leucaena, respectively (Radrizzani et al. 2011). The applications of leucaena and Senna siamea residues (C/N = 13:1 and 18:1, respectively) to an Imperata cylindrical grass fallow in West Africa were also found to be more effective at increasing SOC (0–20 cm) than applications of similar amounts of residue C as maize stover (C/N = 58:1; Gaiser et al. 2011).
The case studies described here confirm the perceived benefits of using N2-fixing woody perennials to accumulate SOC in soil in addition to their capacity to provide a strong sink to sequester CO2 in their biomass. Interestingly, the increases in SOC stocks (1.4–2.2 Mg C ha−1 per year, 0–60 cm) observed in the Brazilian studies were achieved solely through litter fall from the canopy. This may have represented between 5 and 11 Mg DM ha−1 per year (Chaer et al. 2011). There is potential to more intensively manage some legume shrub and tree species by regularly harvesting foliage which could allow for up to 20 to 30 Mg DM ha−1 (Peoples et al. 1996) to be applied as green-manure to accelerate C accumulation in soil. However, the data of Radrizzani et al. (2011) remind us that the rates of change in SOC beneath woody perennial legume systems will inevitably decline over time.
3 A role for legumes to replace fossil resources?
Biomass can potentially be used to replace fossil hydrocarbons for heat, power, solid and liquid fuels, materials, or chemicals (Bessou et al. 2010). The global energy demand is expected to increase by about 45% by 2030 with the main increase occurring in non-OECD countries (IEA 2009). While fossil fuels are expected to still account for 80% of the world energy requirement in 2030 with oil remaining as the dominant energy source, biomass is projected to be the most important primary source of renewable energy. Biomass is predicted to provide about 9% of the total energy requirement and around 5% of the world road transport fuels (IEA 2009). This represents a 40% increase compared to 2006 in terms of million tons of oil equivalents (Mtoe).
Concerns about dwindling petroleum reserves and needs to supply sources of energy with lower GHG emissions are not the only drivers for these changes. The re-emergence in interest in biofuels and biomass feedstocks have also been encouraged by insecurities about on-going petroleum supplies in light of the recent instabilities in the oil-rich Arab world, and Japan’s nuclear crisis following the 2011 tsunami which has caused many countries to re-assess their reliance upon nuclear power as a source of low-C electricity (Fairley 2011).
There are also a number of concerns about the environmental credentials and socio-economic effects of present bioethanol and biodiesel production from crops (Pimentel 2003). Foremost of these concerns are (1) the implications for food availability and security where energy crops displace food production, (2) GHG emissions if the increased demand for cropping land for biomass crops either directly or indirectly results in the clearing of forested areas, and (3) supplying fertilizer inputs to support the growth of high yielding and high biomass crops. This final issue is one of the key factors contributing to the reduction of the C neutrality of biomass systems because the fossil fuels involved in fertilizer production and transport can effectively negate the whole of life-cycle energy benefits. The attraction of legumes is their ability to satisfy their own N requirements from symbiotic N2 fixation (Herridge et al. 2008). Although it should be noted that legume species differ enormously in their reliance upon N2 fixation for growth in the field, with dry bean (also known as common bean or French bean; Phaseolus vulgaris) often fixing the least, and soybean and faba bean fixing the most (Peoples et al. 2009a).
Clearly, it will be necessary to justify the sustainability of biomass production systems if they are to be seen as a viable alternative to fossil resources and before real progress can be made towards meeting the predicted demand. Biomass systems for energy production will also be required to be multifunctional contributing several components or aspects to society (IAASTD 2009). The following sections analyze the potential role of legumes in contributing to future biobased economies.
3.1 Legume biomass yield potential and constituents
Biomass production for bioenergy feedstock will ideally require a high net biomass per unit area with a low amount of fossil energy input resulting in low fossil energy requirement per kilogram of DM produced. Although legume grain yields have increased in most regions during the last 30 years, yield enhancements are small compared to those observed in wheat and maize. As a result, legume grain yields tend to be lower than cereals in many countries of the world (e.g., Tables 6 and 7; FAOStat 2010). Areas sown to crop legumes have also declined globally for almost all species except soybean in the last few decades (Jensen et al. 2010; FAOStat 2010). Globally, cereals were grown on almost 700 million ha of land in 2009 compared to a total of 193 million ha sown to pulses and legume oilseed crops such as soybean and groundnut (Arachia hypogea).
Second-generation biofuels, power and heat generated by combustion and production of industrial raw materials could be based on legume biomass and residues. However, the amount of legume stubble remaining after grain harvest is often lower than residual cereal straw biomass, which clearly would impact on the relative economics of using legume sources rather than cereals as feedstock.
Less focus has been placed on the use of legumes for biomass feedstock for energy and industrial raw materials. A comprehensive European inventory of crops for bioenergy did not include any legumes (Venendaal et al. 1997). Legumes have high contents of constituents other than carbohydrates, which may be relevant in biorefinery concepts (see Section 3.2), in which the different components could be used for a variety of biobased products. For example, legume biomass might be used to generate biogas (CH4) and N-rich biofertilizer via anaerobic digestion, and the grain utilized for biodiesel and/or protein feed.
Constituents of selected cereal and legume species expressed as percentage of dry matter
Crop and component
Other carbohydrates (C5, C6, a.o.) (%)
Grass–clover (30–50% clover)
Alfalfa (after flowering)
Legumes are lower yielding and have higher protein concentrations than cereals, which have resulted in less interest in their use as sole crops for biofuels. Legumes can be valuable components in mixtures with other species that might be suitable for biorefinery concepts. This is especially the case if the biorefinery is designed to exploit both carbohydrates and protein.
3.2 Legumes as biorefinery feedstocks for biofuels, materials, and chemicals
A biorefinery is defined as the sustainable processing of biomass into a spectrum of marketable products and energy (Cherubini et al. 2009) by the use of physical (fractionation, pressing), chemical (acid hydrolysis, synthesis, esterification), thermochemical (pyrolysis, gasification, combustion), and biochemical (enzymatic and fermentation) methods (De Jong et al. 2010). The aim is to optimize the sustainable use of specific biomass resources available in a given region to ensure both resource use efficiency and economic/environmental sustainability.
A biorefinery may be simple with only a single or few products such as bioethanol and heat or refined sugar and feed. Alternatively, the biorefinery could produce a spectrum of different biobased products in a way analogous to a petrochemical refinery. Different concepts for biorefineries have been described: well-known simple biorefineries produce sugar, potato starch, wheat starch, soybean oil, and protein. Dry milling refineries use cereals grains for bioethanol production and dried distillers grains with solubles (DDGS) for feed. Oleochemical biorefinery produce oils, lubricants, platform chemicals, and biodiesel from canola and soybean (De Jong et al. 2010). Lignocellulosic biorefineries have been used for many years with forestry biomass for the production of paper pulp, chemicals, and energy. During the past decade, there has been a rapid development of sugar platform biorefineries using different types of lignocellulosic biomass (straw, short rotation coppice, perennial energy crops) as feedstock for production of bioethanol, feed, and power (De Jong et al. 2010). A green biorefinery is another concept developed for green biomasses such as grass–clover, alfalfa, and sugar beet (Beta vulgaris) leaves to produce amino acids, feed, fibers, and residues for biogas production (Novalin and Zweckmair 2008; De Jong et al. 2010). Even though there is an increasing interest in biorefineries, examples of successful advanced biorefinery concepts which have developed further than the pilot scale are limited (De Jong et al. 2010).
A biorefinery is a key component in future biobased economies, which will contribute to the replacement of fossil-resource-based economies. Concepts are currently developing quickly worldwide, but soybean is the only legume used to a certain extend for protein feed and biodiesel. There is scope for utilizing other legumes species if their protein and other potentially valuable constituents can be extracted and converted into marketable products.
Renewable sources of energy derived from technologies such as solar panels or wind turbines will be able to supply electricity, but in reality the vast majority of the world’s transport systems are based on motor vehicles and aircraft which require liquid fuels and will do so for the foreseeable future. The recognition that sustainable sources of biofuels will need to be a key part of our global energy future is reflected in the trends in the annual output of bioethanol and biodiesel which has expanded more than 6-fold between 2000 and 2010 (IEA 2009; Fairley 2011).
Bioethanol production is based on the microbial fermentation of sugars into ethanol. Bioethanol produced from simple sugars (e.g., from sugar cane and sugar beet) and starch are termed first-generation bioethanol, whereas bioethanol derived from lignocellulose in straw, stover, perennial biomass crops [e.g., Miscanthus; willow (Salix spp.); reed canary grass (Phalaris arundinacea); mixed grass–clover swards; alfalfa] are termed second-generation bioethanol (Mabee et al. 2006).
Field pea grain has been studied as a potential feedstock either alone or as a supplement with maize grain for first-generation bioethanol production because of its high starch content (Table 10; Nichols et al. 2005; Pryor et al. 2008). Fermentation of whole peas and a dry-separated (starch and protein fraction separated by air classification of milled pea grain) pea starch fraction gave satisfactory ethanol yields (Nichols et al. 2005). The enriched starch fraction in combination with maize starch gave similar or greater ethanol yield than maize starch alone (Pryor et al. 2008). Improved or similar ethanol production occurred with pea starch, despite its less favorable amylase/amylopectin ratio since it has been shown that it is more difficult to convert amylose than amylopectin starch to fermentable sugars, and pea contains 30% to 50% amylose compared to 20% to 30% in maize starch (Pryor et al. 2008).
The consequences of reallocating land from food production to bioenergy purposes, and the overall sustainability of the first-generation technology for bioethanol production, remains controversial (Pimentel 2003; Pimentel and Patzek 2005; Fairley 2011). Hammerschlag (2006) found that the ratio of energy in a liter of ethanol to the non-renewable energy required to produce it with first-generation technologies varied across six different published studies. In one study, more non-renewable energy was required to produce ethanol from maize grain than was present in the final bioethanol product with an energy balance of 0.84. By contrast, another study with maize estimated an energy balance of 1.65 times more renewable energy generated than non-renewable energy used, when the energy content of the by-products were included in the calculations of the energy return on investment (Hammerschlag 2006). The use of non-renewable energy for fertilizers, especially N, represented from 10% to 20% of the total energy inputs. The lower starch yield per unit area of land by crop legumes compared to cereals will probably prevent their increased use for first-generation bioethanol. However, intercropping grain legumes with high starch-yielding non-legumes may be an alternative option (Hauggaard-Nielsen et al. 2009).
The second-generation conversion technology for lignocellulosic materials into bioethanol appears more promising in terms of the potential of using feedstock and land which is not in direct competition with food production. Lignocellulose conversion technology is more complex than first-generation bioethanol production, primarily due to the presence of both C6 and C5 sugars, which are imbedded in lignin and consequently not easily accessible by the cellulases and hemicellulases that are required to convert cellulose and hemicellulose into fermentable sugars. Consequently, a biomass pre-treatment process is required to open the lignocellulosic structure (Mabee et al. 2006). In recent years interest has increased in second-generation bioethanol from feedstock that is not in direct competition with food production since this concept could be more sustainable in terms of GHG emissions, fossil energy use, energy balance, and resource use. Hammerschlag (2006) reported energy of investment (bioethanol energy per unit non-renewable invested energy) to be up to 4.4 and 6.6:1 for lignocellulose-derived bioethanol from maize stover and poplar.
Vegetative biomass from grain and oilseed legumes is a possible source of feedstock for second-generation bioethanol, but DM yields tend to be lower per unit area and the stubble contains more protein and a lower content of cellulose than cereal alternatives (Table 10). Consequently, the ethanol yield will be lower.
Perennials are a promising option because of their efficient use of resources and lower requirements for farming operations than annual crops (Bessou et al. 2010). Alfalfa is an interesting candidate as a perennial legume feedstock for biofuel and bioproducts since it can yield between 4 and 18 Mg DM ha−1 per year (average of 8 Mg DM ha−1 from three to four annual harvests) for up to 4 years of growth (Samac et al. 2006). Alfalfa requires fertile, deep, and well-drained soils and adequate supply of water, although its deep rooting system makes alfalfa more resistant to dry periods than many other crops. Alfalfa stems containing 10–12% protein can be used for bioethanol production while the leaves with 26–30% protein can be used as a high-protein feed (Dale 1983) or further processed to a high-value protein product. New germplasm and cultivation methods (plant density and cutting regime) have been developed for alfalfa to provided modified stem/leaf ratios that are more suitable for bioethanol production (Lamb et al. 2003). Research has been done to determine how the polysaccharide composition of alfalfa stems can be modified by cultivation and harvest frequency in order to produce the most optimal biomass for conversion to bioethanol (Samac et al. 2006). Besides being a potential feedstock for bioethanol, stems are also evaluated as feedstock for the production of lactic acid, which can be used for bioplastic, as a replacement for petroleum-based plastics (Koegel et al. 1999).
Other perennial legumes, such as clovers, could be used as feedstock for second-generation bioethanol either grown as sole crops or in mixtures with grasses. Thomsen and Hauggaard-Nielsen (2008) found that the theoretical bioethanol potential (based on carbohydrate composition) of wheat straw and grass–clover crops were similar at 270 and 240 L per megagram of DM. With biomass yields of 5 Mg of wheat straw DM and 10 Mg grass–clover DM ha−1 in Denmark, the production would be 1.35 and 2.4 Mg bioethanol ha−1, respectively. If a grass–clover cover crop was undersown to wheat, a further 0.96 Mg bioethanol ha−1 could be produced from the autumn biomass growth of the cover crop (Thomsen and Hauggaard-Nielsen 2008).
Intensive agroforestry systems also have a potential role in producing large amounts of biomass. For example, densely planted tree legumes such as Calliandra calothyrsus and Gliricidia sepium in the Australian tropics yielded up to 20 to 30 Mg DM ha−1 as foliage and stem re-growth over an annual cutting cycle when periodically cut as hedgerows (Peoples et al. 1996). Some woody perennial legume species are also suitable for use on marginal or degraded lands (see Section 2.3.4).
The deep-rooted nature of both herbaceous and woody perennial legumes also offer an effective, low-cost method for (1) remediating excess soil N and lowering the risk of groundwater contamination by nitrate (Randall et al. 1997; Entz et al. 2001), and (2) reducing the risk of rising water tables and the development of dryland salinity (Angus et al. 2001; Lefroy et al. 2001).
Annual crop legumes do not seem particularly attractive for bioethanol production due to their low starch yield per unit area. Perennial legumes such as alfalfa, on the other hand, offer an interesting resource for future second-generation bioethanol production either as sole crop or in mixed cropping with high-yielding non-legume species.
Biodiesel is produced by the transesterification of the glyceride molecules in plant oils by methanol to produce glycerine and methyl esters (Mabee et al. 2006), which can readily be used in diesel engines. The production of glycerine and the need for methanol detract somewhat from the attractiveness of biodiesel. New chemical procedures are now in place allowing the production of liquid biofuels (such as aviation fuel) out of plant oils without esterification. The nature of the fatty acid composition controls critical physical properties, such as the cloud point (the temperature at which the diesel will turn cloudy and thus clog injection systems). A low concentration of palmitic (C16:0) and stearic (C18:0) acids and a high concentration of oleic (C18:1) acid is optimal (Kazakoff et al. 2011).
Brazil produced 58 million Mg of soybean in 2007, and extracted 5.7 million Mg of oil, part of which was used for biodiesel production (Elbersen et al. 2010). One megagram of soybean yields about 170 L of biodiesel; consequently, the potential of Brazilian biodiesel production from soybean is about 10 billion liters if all the oil was used for this purpose. In comparison, the global biodiesel production level in 2006 was 2.7 million liters, with Germany being the largest producer of about 1.2 million liters derived from canola (Mabee et al. 2006).
Soybean in Brazil and Argentina is estimated to obtain approximately 80% of its N from BNF (Herridge et al. 2008). In the USA (the world’s largest producer), soybean reliance upon BNF for growth is somewhat less (∼60%) due to the more fertile soils in the midwest and the residual N fertilizer from maize crops in the rotation. China may have even lower inputs of fixed N by soybean as yields are lower and N fertilizer use is higher (Herridge et al. 2008).
Fossil energy inputs, total energy yield, and energy balance for soybean diesel produced on 1 ha of land under standard Brazilian zero-till management systems
Units per hectare
1. Field preparation
Mineral oil adjuvant
Seeds for pasture
2. Crop establishment
3. Crop management
Field operations and transport
5. Farm labor
Soybean bioenergy produced
Total bioenergy yield
Fossil energy use
Agricultural energy costs
Transesterification (biodiesel production)
Total fossil energy use
Final energy balance for soybean biodiesela
Total energy balance including soy mealb
The fast-growing legume tree Pongamia pinnata (also called Millettia pinnata) may be a significant future source of oil for production of biodiesel since the seeds contain around 40% oil, with the predominant fatty acids being oleic, palmitic, stearic, and linoleic (Scott et al. 2008; Kazakoff et al. 2011). Pongamia oil is non-edible, but is not toxic to humans. Pongamia oil contains about 50–55% oleic acid, with about 7–10% palmitic and stearic acid.
The Pongamia trees are extremely drought tolerant, owing to their deep root system, waxy leaf, and favorable stress physiology. They are also salt tolerant, so they could be grown on margin lands and in soils unsuited for food production (Wilkinson et al. 2012). In addition to high oil content seeds, the Pongamia tree may supply biomass for other biobased applications. The seed pod (casing) is of equal mass to the single seed contained in it and has application in co-firing in electricity plants. The seed cake, after oil extraction, can yield protein concentrate for low quality animal feed supplement (especially ruminants), second generation bioethanol, biogas, or thermochemical conversion and production of biochar (see Section 3.2.4).
If soybean is planted solely for the purpose of biodiesel manufacture, there is unlikely to be significant GHG mitigation benefits. If the objective is to produce high-protein feed, and the oil is a by-product, then energy balance may be as high as 3.5:1 and could represent an important GHG mitigation benefit. The legume tree Pongamia pinnata offers an interesting possibility for future biodiesel production with potential applications for legume-based biorefineries.
3.2.4 Biogas and digestate for fertilizer from anaerobic digestion
Anaerobic digestion is a key technology for the sustainable use of organic biomasses from industrial and urban organic wastes, animal manures, crop residues, and whole energy crops (Amon et al. 2007). Anaerobic digestion is particularly well suited for heterogeneous feedstock. It sanitizes the feedstock and can be applied at scales from the farm to big industrial plants. The biogas (mixture of CH4 and CO2) produced can be converted to electricity, heat, or upgraded to liquid biofuel for vehicles (Amon et al. 2007; Lehtomäki et al. 2008). Within the European Union, biogas production increased 6-fold from 1995 to 2005 (Eurostat 2007). Simultaneously, the digest residues consisting of nutrients and recalcitrant C enables almost complete nutrient recycling in the system, including N. The digestate can be used as a fertilizer and enhance the synchrony of plant-available N and crop N demand since a major part of the organic N is mineralized to ammonium (Möller et al. 2008).
Comparisons of the methane (CH4) potential of grass or cereal sources to selected legumes and legume containing biomasses
CH4 potential (m3 kg−1 volatile solids)a
Lehtomäki et al. (2008)
Fresh Timothy-red cloverb mix (10% legume)
Vetch–oatc (50% legume)
Amon et al. (2007)
Fresh grass–clover (% legume not determined)
Legume biomass is well suited for the production of biogas when mixed with other species since the N and other nutrients in the digestate can be used as a valuable biofertilizer.
3.2.5 Thermochemical conversion for production of heat, syngas, biooil, and biochar
Pyrolysis of biomass involves the combustion of the biomass without oxygen and results in syngas, biooil, and biochar. The production ratio of these components depends on the biomass characteristics and the pyrolysis temperature (Bruun et al. 2011). The syngas and biooil can be combusted with oxygen or upgraded to biofuels for vehicles. The biochar, which contain the majority of nutrients except N and S, can be used to recycle nutrients and provide long-term C sequestration in soil since the C in the biochar is rather recalcitrant to microbial decomposition (Lehmann et al. 2006). Pyrolyzing straw from high biomass soybeans at 500°C resulted in around 70% biooil, 20% biochar, and 10% syngas (Boateng et al. 2010). Boateng et al. (2008) found that the pyrolysis of alfalfa stems produced a lower output of biooil, but slightly higher amounts of biochar than soybean, although the oil was found to have a higher energy content.
Legume tree or residue biomasses could be used in thermochemical conversion processes, but it is important to consider that the N and S may be lost from the system. However, in biorefinery concepts, the final conversion process may be a thermochemical or versatile biochemical process such as anaerobic digestion to efficiently recycle the remaining carbohydrates and nutrients in the digestate.
3.2.6 Materials and chemicals
In a biobased economy, there is a requirement to replace products other than energy carriers currently derived from fossil hydrocarbons. Biomass may contribute building blocks for chemicals, biomaterials, and biopharmaceuticals. For example, 56 Tg of textiles were produced worldwide in 1999 of which 54% was synthetic chemical fibers based on fossil hydrocarbons (Lorek and Lucas 2003). Traditionally, legumes have been considered as a source of dietary oil, protein, and fiber for humans and livestock, but legumes contain many constituents that are essentially similar to other sources of biomass—sugars, amino acids, phytochemicals, lignin, tannins, etc. (Fig. 4)—which can be used as building block chemicals to produce surfactants, biopolymers, glues, and a variety of industrial chemicals which are now produced in petrochemical refineries (De Jong et al. 2010). Some natural products are either found only in legumes or in high concentrations in legumes that are of potential use as nutri- or pharmaceuticals, or biopesticides in addition to industrial purposes, and there could be significant benefits in extracting some of the higher value compounds in a biorefinery (Dixon and Sumner 2003; Duranti et al. 2008). For example, there are several reports of a possible role for the use of legume seed proteins to control metabolic disorders. These include the cholesterol-lowering effect of soybean 7S globulin α′ subunit and the immobilization of insulin by lupin conglutin γ to control glycemia (Magni et al. 2004; Duranti et al. 2008). Legumes also produce isoflavones which reputably have estrogenic, antiangiogenic, antioxidant, and anti-cancer activities, and an ability to prevent osteoporosis and cardiovascular diseases (Dixon and Sumner 2003). Condensed tannins and polyphenols present in legume seed coats are antioxidants with potential health beneficial effects for cardiac health and immunity, and it has recently been reported that phenolic compounds from faba bean can inhibit human cancer cells (Dixon and Sumner 2003; Siah et al. 2011). Triterpene saponin, which is present in alfalfa, deters herbivore grazing, but these saponins also display allelopathic, antimicrobial, and anti-insect activity, which can be used in other contexts such as surfactants and foaming agents (Dixon and Sumner 2003). The variety of food and non-food products that have been successfully developed and marketed from soybean illustrates what may be possible for other legumes.
Legumes are known to contain proteins and bioactive substances, which could be extracted in future biorefineries and used as industrial chemicals, food ingredients or pharmaceuticals, surfactants and bioplastics.
4 Concluding remarks
Legumes are unique plants. They contribute many different functions and ecosystems services that are of great value for agriculture and society (Jensen and Hauggaard-Nielsen 2003; Crews and Peoples 2004; Peoples et al. 2009b; Köpke and Nemecek 2010; De Faria et al. 2011). Including legume food, forage, and tree crops in farming systems is one approach that can contribute to mitigating climate change. Our review of the literature indicates that the ability of the legumes to fix their own N via a symbiosis with rhizobia bacteria reduces emissions of fossil energy-derived CO2 and results in lower N2O fluxes compared to cropping and pasture systems that are fertilized with industrial N. Less quantitative data are available concerning N2O losses from legume residues following a legume phase in a cropping sequence. It was concluded that while the potential losses of N2O can be large from leguminous residues containing high concentrations N such as nodules, or fresh foliage, the contribution of N2O emissions from senesced vegetative residues remaining after grain harvest of a crop legume can be small. Further work is needed to better understand how the management and quality of legume residues affects N2O emissions in subsequent crops.
In addition to legumes resulting in lower GHG emissions, they also appear to play a key role in soil C sequestration. The inclusion of herbaceous legumes in pastures, and either as sole crops, green- or brown-manures, cover-crops, or intercrops in reduced tillage cropping systems, has been shown to enhance soil C accumulation. Woody perennial legume species have also been demonstrated to be extremely useful for revegetating cleared and degraded land to replenish soil organic C stocks.
In the short term, it is unlikely that sole crop annual legumes will be used as biorefinery feedstock due to their relatively low DM yield. Legumes are important components of future diversified and sustainable cropping systems, which are not in direct competition for land with food production. Many legumes can be produced on marginal/surplus lands and on degraded or drastically disturbed soils. Perennial legumes (alfalfa, clover, and various tree and shrub species) could have unique roles in generating biomass for biorefineries, without the requirement for N fertilization either as sole crops or in mixtures with grasses.
Advances in conversion/biorefinery technologies will be required which can add value to the by-products of energy generation by extracting and exploiting the high protein content of legume biomass. Examples of potential technologies and products suited for legume biomass include protein extraction for feed (e.g., soybean cake) or pharmaceuticals, renewable materials production, and anaerobic digestion for CH4 production with the simultaneous production of a biofertilizer containing nutrients for recycling.
Residues from arable crops provide an essential function in maintaining soil fertility, preventing soil erosion and structure in arable soil (Lal and Pimentel 2007). Consequently, the use of legume biomass for bioenergy, materials, and chemicals represents a significant trade-off since the contribution of legume residues to soil organic fertility and C sequestration would be significantly reduced. National strategies for using straw and other residues for biofuels will need to identify the regions that have soils with sufficient organic matter levels to allow the temporary utilization of the straw/stover for bioenergy that are also at low risk of erosion (Nelson 2002). The huge world acreage of soybean potentially could generate massive amounts of organic residues. In the USA, McMurtrey et al. (2005) showed that no soybean residues could be sustainably removed after growing conventional soybean types with conventional tillage practice, whereas between 7% and 30% of the residues could be removed with reduced tillage and zero-tillage scenarios, respectively.
Future sustainable agricultural systems require novel management and plant breeding solutions to assist society with climate change mitigation options for producing biofuels, materials, and chemicals. One of the key paradigms for future sustainable agriculture is multifunctionality of system and crops. Agriculture will need to supply several services from the use of the same piece of land, and the key principle to obtain this is diversity in time and space, involving cropping systems as well as crop species. Thus, legume species, with their multiple arrays of potential ecosystems services combined with their ability to reduce GHG emissions and encourage soil C sequestration, should be given careful consideration as important components of future sustainable food, fiber, and energy production systems for human prosperity.
Erik S. Jensen wishes to acknowledge that participation in the Fifth International Food Legumes Research Conference helped facilitate the preparation of this review. Mark B. Peoples is indebted for the support of the Grains Research and Development Corporation (GRDC) to continue research into the role of legumes in Australian farming systems. Peter M. Gresshoff thanks the Australian Research Council (ARC) for a Centre of Excellence grant, the University of Queensland Strategic Fund for continued support, Dr. Paul Scott for academic input, and the Bioenergy Research Pty Ltd for commercial partnership in Pongamia-related research efforts. Malcolm J. Morrison wishes to thank Agriculture and Agri-Food Canada for financial support, Dr. Ed Gregorich and Pat St George from Agriculture and Agri-Food Canada who assisted in the collection of the N2O data depicted in Fig. 2 along with Brian Couture and Randy Hodgins for field work and technical support.
- Amon T, Amon B, Kryvoruchko V, Machmüller A, Hopfner-Sixt K, Bodiroza V, Hrbek R, Fridel J, Pötsch E, Wagentristl H, Schreiner M, Zollitsch W (2007) Methane production through anaerobic digestion of various energy crops grown in sustainable crop rotations. Biores Technol 98:3204–3212Google Scholar
- Angus JF, Gaul RR, Peoples MB, Stapper M, van Hawarden AF (2001) Soil water extraction by dryland crops, annual pastures and lucerne in south-eastern Australia. Aust J Agric Res 52:183–192Google Scholar
- Armstrong RD, Kickoff BJ, Millar G, Whitbread AM, Standley J (1999) Changes in soil chemical and physical properties following legumes and opportunity cropping on a cracking clay soil. Aust J Exp Agric 39:445–456Google Scholar
- Arrouays D, Deslais W, Badeau V (2001) The carbon content of topsoil and its geographical distribution in France. Soil Use Manag 17:7–11Google Scholar
- Atkins CA (1984) Efficiencies and inefficiencies in the legume/Rhizobia symbiosis—a review. Plant Soil 82:273–284Google Scholar
- Aulakh MS, Khera TS, Doran JW, Bronson KF (2001) Denitrification, N2O and CO2 fluxes in rice–wheat cropping system as affected by crop residues, fertilizer N and legume green manure. Biol Fertil Soils 34:375–389Google Scholar
- Baggs EM, Stevenson M, Pihlatie M, Regar A, Cook H, Cadisch G (2003) Nitrous oxide emissions following application of residues and fertilizer under zero and conventional tillage. Plant Soil 254:361–370Google Scholar
- Baker JM, Ochsner TE, Venterea RT, Griffis TJ (2007) Tillage and carbon sequestration—what do we really know? Agric Ecosyst Environ 118:1–5Google Scholar
- Banks C (2007) Renewable energy from crops and agrowastes (CROPGEN). Final report. 32 p. http://www.cropgen.soton.ac.uk/deliverables/CROPGEN_PFAR2007.pdf (accessed 24 February 2011)
- Barthès B, Azontonde A, Blanchart E, Girardin C, Villenave C, Lesaint S, Oliver R, Feller C (2004) Effect of a legume cover crop (Mucuna pruriens var. utilis) on soil carbon in an Ultisol under maize cultivation in southern Benin. Soil Use Manag 20:231–239Google Scholar
- Barton L, Kiese R, Gatter D, Butterbach-Bahl K, Buck R, Hinz C, Murphy DV (2008) Nitrous oxide emissions from a cropped soil in a semi-arid climate. Global Change Biol 14:177–192Google Scholar
- Barton L, Murphy DV, Kiese R, Butterbach-Bahl K (2010) Soil nitrous oxide and methane fluxes are low from a bioenergy crop (canola) grown in a semi-arid climate. Global Change Biol Bioenergy 2:1–15Google Scholar
- Barton L, Butterbach-Bahl K, Kiese R, Murphy DV (2011) Nitrous oxide fluxes from a grain–legume crop (narrow-leafed lupin) grown in a semiarid climate. Global Change Biol 17:1153–1166Google Scholar
- Bayer C, Mielniczuck J, Amado TJC, Martin-Neto L, Fernandes SBV (2000) Organic matter storage in a sandy clay loam Acrisol affected by tillage and cropping systems in southern Brazil. Soil Tillage Res 54:101–109Google Scholar
- Bergersen FJ, Brockwell J, Gault RR, Morthorpe L, Peoples MB, Turner GL (1989) Effects of available soil nitrogen and rates of inoculation on nitrogen fixation by irrigated soybeans and evaluation of δ15N methods for measurement. Aust J Agric Res 40:761–780Google Scholar
- Bertelsen F, Jensen ES (1992) Gaseous nitrogen losses from field plots grown with pea (Pisum sativum L.) or spring barley (Hordeum vulgare L.) estimated by 15N mass balance and acetylene inhibition techniques. Plant Soil 142:287–295Google Scholar
- Bessou C, Ferchaud F, Gabrielle B, Mary B (2010) Biofuels, greenhouse gases and climate change. A review. Agron Sustain Dev. doi:10.1051/agro/2009039
- Boateng AA, Mullen CA, Goldberg NM, Hicks K, Devine TE, Lima IM, McMurtrey JE (2010) Sustainable production of bioenergy and biochar from the straw of high-biomass soybeans lines via fast-pyrolysis. Environ Prog Sustain Energ 29:175–183Google Scholar
- Boateng AA, Mullen CA, Goldberg NM, Hicks KB, Jung HG, Lamb JF (2008) Production of bio-oil from alfalfa stems by fluidized-bed fast pyrolysis. Ind Eng Chem Res 47:4115–4122Google Scholar
- Boddey RM, Xavier DF, Alves BJR, Urquiaga S (2003) Brazilian agriculture: the transition to sustainability. J Crop Prod 9:593–621Google Scholar
- Boddey RM, de Soares B, Alves BJR, Urquiaga S (2008) Bio-ethanol production in Brazil. In: Pimentel D (ed) Biofuels, solar and wind as renewable energy systems: benefits and risks. Springer, New York, pp 321–356Google Scholar
- Boddey RM, Alves BJR, Soares LHB, Jantalia CP, Urquiaga S (2009) Biological nitrogen fixation and the mitigation of greenhouse gas emissions. In: Emerich DW, Krishnan HB (eds) Agronomy Monograph 52. Nitrogen Fixation in Crop Production, Am. Soc. Agron., Crop Sci. Soc. Am., and Soil Sci. Soc Am. Madison, Wisconsin, USA, pp. 387–413Google Scholar
- Boddey RM, Jantalia CP, Zanatta JA, Conceição PC, Bayer C, Mielniczuk J, Dieckow J, dos Santos HP, Denardin JE, Aita C, Alves BJR, Urquiaga S (2010) Carbon accumulation at depth in Ferralsols under zero-till subtropical agriculture in southern Brazil. Global Change Biol 16:784–795Google Scholar
- Bouwman AF (1996) Direct emissions of nitrous oxide from agricultural soils. Nutr Cycl Agroecosyst 46:53–70Google Scholar
- Brehmer B, Struik PC, Sanders J (2008) Using an energetic and exergetic life cycle analysis to assess the best application of legumes within a biobased economy. Biomass Bioenerg 32:1175–1186Google Scholar
- Breitenbeck GA, Bremner JM (1989) Ability of free-living Bradyrhizobium japonicum to denitrify nitrate in soils. Biol Fertil Soils 7:219–224Google Scholar
- Bremer E, van Kessel C (1992) Seasonal microbial biomass dynamics after addition of lentil and wheat residues. Soil Sci Soc Am J 56:1141–1146Google Scholar
- Bruun EW, Hauggaard-Nielsen H, Ibrahim N, Egsgaard H, Ambus P, Jensen PA, Dam-Johansen K (2011) Influence of fast pyrolysis temperature on biochar labile fraction and short-term carbon loss in a loamy soil. Biomass Bioenerg 35:1182–1189Google Scholar
- Ceotto E (2008) Grasslands for bionenergy production. A review. Agron Sustain Dev 28:47–55Google Scholar
- Chalk PM (1998) Dynamics of biologically fixed N in legume–cereal rotations: a review. Aust J Agric Res 49:303–316Google Scholar
- Chan KY (1997) Consequences of changes in particulate organic carbon in vertisols under pasture and cropping. Soil Sci Soc Am J 61:1376–1382Google Scholar
- Chan KY, Conyers MK, Li GD, Helyar KR, Poile G, Oates A, Barchia IM (2011) Soil carbon dynamics under different cropping and pasture management in temperate Australia: results of three long-term experiments. Soil Res 49:320–328Google Scholar
- Chen S, Huang Y, Zou J (2008) Relationship between nitrous oxide emission and winter wheat production. Biol Fertil Soils 44:985–989Google Scholar
- Cherubini F, Jungmeir G, Wellisch M, Wilke M, Skiadas I, Van Ree R, de Jong E (2009) Towards a common classification approach for biorefinery systems. Biofuels Bioprod Bioref 3:534–546Google Scholar
- Christopher SF, Lal R (2007) Nitrogen management affects carbon sequestration in North American cropland soils. Crit Rev Plant Sci 26:45–64Google Scholar
- Ciampitti IA, Ciarlo EA, Conti ME (2008) Nitrous oxide emissions from soil during soybean [(Glycine max (L.) Merrill] crop phenological stages and stubbles decomposition period. Biol Fertil Soils 44:581–588Google Scholar
- Cleveland CC, Liptzin D (2007) C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochem 85:235–252Google Scholar
- Conant RT, Paustian K, Elliot ET (2001) Grassland management and conversion into grassland: effects on soil carbon. Ecol Applic 11:343–355Google Scholar
- Crews TE, Peoples MB (2004) Legume versus fertilizer sources of nitrogen: ecological tradeoffs and human needs. Agric Ecosyst Environ 102:279–297Google Scholar
- Crews TE, Peoples MB (2005) Can the synchrony of nitrogen supply and crop demand be improved in legume and fertilizer-based agroecosystems? A review. Nutr Cycl Agroecosyst 72:101–120Google Scholar
- Dalal RC, Chan KY (2001) Soil organic matter in rainfed cropping systems of the Australian cereal belt. Aust J Soil Res 39:435–464Google Scholar
- Dalal RC, Strong WM, Weston EJ, Cooper JE, Lehane KJ, King AJ, Chicken CJ (1995) Sustaining productivity of a vertisol at Warra, Queensland, with fertilizers, no-tillage, or legumes. 1. Organic matter status. Aust J Exp Agric 35:903–913Google Scholar
- Dale BE (1983) Biomass refining: protein and ethanol from alfalfa. Ind Eng Chem Prod Res Dev 22:466–472Google Scholar
- Danish Feed Analysis (2005) Feed tables 2005. Eds. J. Møller. 49 p. (in Danish)Google Scholar
- De Faria SM, Resende AS, Saggin Júnior OJ, Boddey RM (2011) Exploiting mycorrhizae and rhizobium symbioses to recover seriously degraded soils. In: Polacco JC, Todd CD (eds) Ecological aspects of plant nitrogen metabolism. Wiley-Blackwell, New York, pp 195–214Google Scholar
- De Jong E, van Ree R, Sanders JPM, Langeveld JWA (2010) Biorefineries: giving value to sustainable biomass use. In: Langeveld H, Sanders J, Meeusen M (eds) The biobased economy—biofuels, materials and chemicals in the post-oil era. Earthscan, LondonGoogle Scholar
- Dean W (1995) With Broadax and Firebrand: the destruction of the Brazilian Atlantic Forest. University of California Press, BerkeleyGoogle Scholar
- Diekow J, Mielniczuk J, Knicker H, Bayer C, Dick DP, Kogel-Knabner I (2005) Soil C and N stocks as affected by cropping systems and nitrogen fertilization in a southern Brazil Acrisol managed under no-tillage for 17 years. Soil Tillage Res 81:87–95Google Scholar
- Duke JA (1981) Handbook of legumes of world economic importance. Plenum, New YorkGoogle Scholar
- Duke JA (1983) Handbook of Energy Crops. http://www.hort.purdue.edu/newcrop/duke_energy/dukeindex.html (Accessed 23 February 2011).
- Duranti M, Consonni A, Magni C, Sessa F, Scarafoni A (2008) The major proteins of lupin seed: characterisation and molecular properties for use as functional and nutraceutical ingredients. Trends Food Sci Technol 19:624–633Google Scholar
- Elbersen HW, Bindraban PS, Blaauw R, Jongman R (2010) Biodiesel from Brazil. In: Langeveld H, Sanders J, Meeusen M (eds) The biobased economy—biofuels, materials and chemicals in the post-oil era. Earthscan, London, pp 283–301Google Scholar
- Entz MH, Bullied WJ, Forster DA, Gulden R, Vessey JK (2001) Extraction of subsoil nitrogen by alfalfa, alfalfa–wheat and perennial grass systems. Agron J 93:495–503Google Scholar
- Eswaran H, Vandenberg E, Reich P (1993) Organic carbon in soils of the world. Soil Sci Soc Am J 57:192–194Google Scholar
- Eurostat (2007) Gas and electric market statistics. European Communities, Office for Official Publications of the European Communities, LuxembourgGoogle Scholar
- Evans J, Scott G, Lemerle D, Kaiser A, Orchard B, Murray GM, Armstrong EL (2003) Impact of legume ‘break’ crops on the residual amount and distribution of soil mineral nitrogen. Aust J Agric Res 54:763–776Google Scholar
- FAOStat (2010) http://faostat.fao.org/ (Accessed 20 September 2010)
- Fillery IRP (2001) The fate of biologically fixed nitrogen in legume-based dryland farming systems: a review. Aust J Exp Agric 41:361–381Google Scholar
- Fisher MJ, Rao IM, Ayarza MA, Lascono CE, Sanz JI, Thomas RJ, Vera RR (1994) Carbon storage by introduced deep-rooted grasses in South American savannas. Nature 371:236–238Google Scholar
- Fisher MJ, Braz SP, dos Santos RSM, Urquiaga S, Alve BJR, Boddey RM (2007) Another dimension to grazing systems: soil carbon. Trop Grassl 41:65–83Google Scholar
- Franco AA, de Faria SM (1997) The contribution of N2-fixing tree legumes to land reclamation and sustainability in the tropics. Soil Biol Biochem 29:897–903Google Scholar
- Freixo AA, de Machado PLOA, dos Santos HP, Silva CA, de Fadigas FS (2002) Soil organic carbon and fractions of a Rhodic Ferrasol under the influence of tillage and crop rotation systems in southern Brazil. Soil Tillage Res 64:221–230Google Scholar
- Gaiser T, Stahr K, Bernard M, Kang BT (2011) Changes in soil carbon fractions in a tropical Acrisol as influenced by the addition of different residue materials. Agroforest Syst. doi:10.1007/s10457-011-9417-0
- Galiana A, Gnahoua GM, Chaumont J, Lesueur D, Prin Y, Mallet B (1998) Improvement of nitrogen fixation in Acacia mangium through inoculation with rhizobium. Agroforest Syst 40:297–307Google Scholar
- Gan Y, Liang C, Wang X, McConkey B (2011) Lowering carbon footprint of durum wheat by diversifying cropping systems. Field Crops Res 122:199–206Google Scholar
- Garcia-Plazaola JI, Becerril JM, Arrese-Igor C, Hernandez A, Gonzalez-Murua C, Aparicio-Tejo PM (1993) The contribution of Rhizobium meliloti to soil denitrification. Plant Soil 157:207–213Google Scholar
- Goossens A, De Visscher A, Boeckx P, Van Cleemput O (2001) Two-year field study on the emission of N2O from coarse and middle-textured Belgian soils with different land use. Nutr Cycl Agroecosyst 60:23–34Google Scholar
- Grace PR, Oades JM, Keith H, Hancock TW (1995) Trends in wheat yields and soil organic carbon in the permanent rotation trial at the Waite Agricultural Research Institute, South Australia. Aust J Exp Agric 35:857–864Google Scholar
- Gregorich EG, Drury CF, Baldock JA (2001) Changes in soil carbon under long-term maize in monoculture and legume-based rotation. Can J Soil Sci 81:21–31Google Scholar
- Gresshoff PM, Lohar D, Chan PK, Biswas B, Jiang Q, Reid D, Ferguson B, Stacey G (2009) Genetic analysis of ethylene regulation of legume nodulation. Plant Signal Behav 4:9Google Scholar
- Hauggaard-Nielsen H, Ambus P, Jensen ES (2003) The comparison of nitrogen use and leaching in sole cropped versus intercropped pea and barley. Nutr Cycl Agroecosyst 65:289–300Google Scholar
- Hauggaard-Nielsen H, Gooding M, Ambus P, Corre-Hellou G, Crozat Y, Dahlmann C, Dibet A, von Fragstein P, Pristeri A, Monti M, Jensen ES (2009) Pea–barley intercropping for efficient symbiotic N2-fixation, soil N acquisition and use of other nutrients in European organic cropping systems. Field Crop Res 113:64–71Google Scholar
- Heenan DP, McGhie WJ, Thompson F, Chan KY (1995) Decline in soil organic carbon and total nitrogen in relation to tillage, stubble management and rotation. Aust J Exp Agric 35:877–884Google Scholar
- Helgason BL, Janzen HH, Chantigny MH, Drury CF, Ellert BH, Gregorich EG, Lemke RL, Pattey E, Rochette P, Wagner-Riddle C (2005) Toward improved coefficients for predicting direct N2O emissions from soil in Canadian agroecosystems. Nutr Cycl Agroecosyst 72:87–99Google Scholar
- Hénault C, Devis X, Lucas JL, Germon JC (1998) Influence of different agricultural practices (type of crop, form of N-fertilizer) on soil nitrous oxide emissions. Biol Fertil Soils 27:299–306Google Scholar
- Herridge DF, Marcellos H, Felton WL, Turner GL, Peoples MB (1995) Chickpea increases soil-N fertility in cereal systems through nitrate sparing and N2 fixation. Soil Biol Biochem 27:545–551Google Scholar
- Herridge DF, Peoples MB, Boddey RM (2008) Marschner review: global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311:1–18Google Scholar
- Hoyle FC, Baldock JA, Murphy DV (2011) Soil organic carbon—role in Australian farming systems. In: Tow P, Cooper I, Partridge I, Birch C (eds) Rainfed farming systems. Springer, Heidelberg, in pressGoogle Scholar
- IAASTD (2009) Executive summary of the synthesis report. International Assessment of Agricultural Knowledge, Science and Technology for Development. Intergovernmental plenary Johannesburg, South Africa (7–11 April 2008). 34 pGoogle Scholar
- IBGE (2011) Instituto Brasileiro de Geografia e Estatística. Retrieved August 2011, from http://www.sidra.ibge.gov.br/bda/default.asp?t=5&z=t&o=1&u1=1&u2=1&u3=1&u4=1&u5=1&u6=1&u7=1&u8=1&u9=3&u10=1&u11=26674&u12=1&u13=1&u14=1 (Acessed 14 August 2011)
- IEA (2009) World Energy outlook 2008. International Energy Agency. 568 p. IEA, ParisGoogle Scholar
- IFA (2010) International Fertilizer Industry Association, Paris France. http://www.fertilizer.org/ifa/Home-Page/STATISTICS (Accessed 20 August 2010)
- IPCC (1996) Guidelines for National Greenhouse Gas Inventories? Intergovernmental Panel on Climate Change (IPCC)Google Scholar
- IPCC (2000) The science bases. http://www.ipcc.ch (Accessed 22 August 2010)
- IPCC (2006) IPCC Guidelines for National Greenhouse Gas Inventories, Prepared by the National Greenhouse Gas Inventories Programme, Inst. for Global Strategies (IGES), HayamaGoogle Scholar
- IPCC (2007) Climate change 2007: Synthesis report. Summary for Policymakers. Intergovernmental Panel on Climate Change (IPCC)Google Scholar
- Jantalia CP, dos Santos HP, Urquiaga S, Boddey RM, Alves BJR (2008) Fluxes of nitrous oxide from soil under different crop rotations and tillage systems in the south of Brazil. Nutr Cycl Agroecosyst 82:161–173Google Scholar
- Jenkinson DS (2001) The impact of humans on the nitrogen cycle, with focus on temperate agriculture. Plant Soil 228:3–15Google Scholar
- Jensen ES (1989) The role of pea cultivation in the nitrogen economy of soils and succeeding crops. In: Planquaert P, Haggar R (eds) Legumes in farming systems. Kluwer, Dordrecht, pp 3–15Google Scholar
- Jensen ES, Hauggaard-Nielsen H (2003) How can increased use of biological N2 fixation in agriculture benefit the environment? Plant Soil 252:177–186Google Scholar
- Jensen ES, Peoples MB, Hauggaard-Nielsen H (2010) Faba bean in cropping systems. Field Crops Res 115:203–216Google Scholar
- Jones SK, Rees RM, Skiba UM, Ball BC (2007) Influence of organic and mineral N fertiliser on N2O fluxes from a temperate grassland. Agric Ecosyst Environ 121:74–83Google Scholar
- Kamp T, Steindl H, Hantschel RE, Beese F, Munch J-C (1998) Nitrous oxide emissions from a fallow and wheat field as affected by increased soil temperatures. Biol Fertil Soils 27:307–314Google Scholar
- Karpenstein-Machan M (2001) Sustainable cultivation concepts for domestic energy production from biomass. Crit Rev Plant Sci 20:1–14Google Scholar
- Kaschuk G, Kuyper TW, Leffelaar PA, Hungria M, Giller KE (2009) Are the rates of photosynthesis stimulated by the carbon sink strength or rhizobial and arbuscular mycorrhizal symbioses? Soil Biol Biochem 41:1233–1244Google Scholar
- Kazakoff SH, Gresshoff PM, Scott PT (2011) Pongamia pinnata, a sustainable feedstock for biodiesel production. In: Halford N, Karp A (eds) Energy crops. Royal Society of Chemistry, London, pp. 233–254Google Scholar
- Kilian S, Werner D (1996) Enhanced denitrification in plots of N2-fixing faba beans compared to plots of a non-fixing legume and non-legumes. Biol Fert Soils 21:77–83Google Scholar
- Kindler R, Siemens J, Kaiser K, Walmsley DC, Bernhofer C, Buchmann N, Cellier P, Eugster W, Gleixner G, Grŭnswald T, Heim A, Ibrom A, Jones SK, Jones M, Klumpp K, Kutsch W, Larsen KS, Lehuger S, Loubet B, McKenzie R, Moors E, Osborne B, Pilegaard K, Rebmann C, Saunders M, Schmidt I, Schrumpf M, Seyfferth J, Skib U, Soussana JF, Sutton MA, Tefs C, Vowinckels B, Zeeman M, Kaupenjohann M (2011) Dissolved carbon leaching from soil is a crucial component of the net ecosystem carbon balance. Glob Change Biol 17:1167–1185Google Scholar
- Kirkby CA, Kirkegaard JA, Richardson AE, Wade LJ, Blanchard C, Batten G (2011) Stable soil organic matter: a comparison of CNPS ratios in Australian and international soils. Geoderma 163:197–208Google Scholar
- Kirkegaard J, Christen O, Krupinsky J, Layzell D (2008) Break crop benefits in temperate wheat production. Field Crops Res 107:185–195Google Scholar
- Kirkegaard JA, Peoples MB, Angus JE, Unkovich MJ (2011) Diversity and evolution of rainfed farming systems in Southern Australia. In: Tow P, Cooper I, Partridge I, Birch C (eds) Rainfed farming systems. Springer, Dordrecht, The Netherlands, pp 715–754Google Scholar
- Klumpp K, Fontaine S, Arrard E, Le Roux X, Gleixner G, Soussana JF (2009) Grazing triggers soil carbon loss by altering plant roots and their control on soil microbial community. J Ecol 97:876–885Google Scholar
- Klumpp K, Bloor JMG, Ambus P, Soussana JF (2011) Effect of clover density on N2O emissions and plant–soil N transfers in a fertilised upland pasture. Plant Soil 343:97–107Google Scholar
- Koegel RG, Sreenath HK, Straub RJ (1999) Alfalfa fibre as a feedstock for ethanol and organic acids. App Biochem Biotech 77-79:110–115Google Scholar
- Köpke U, Nemecek T (2010) Ecological services of faba bean. Field Crops Res 115:217–233Google Scholar
- Krupnik TJ, Six J, Ladha JK, Paine MJ, van Kessel C (2004) An assessment of fertilizer nitrogen recovery efficiency by grain crops. In: Mosier AR, Syers KJ, Freney JR (eds) Agriculture and the nitrogen cycle, the Scientific Committee on Problems of the Environment (SCOPE). Island, Covelo, pp 193–207Google Scholar
- Kumar K, Goh KM (2000) Crop residues and management practices: effects on soil quality, soil nitrogen dynamics, crop yield, and nitrogen recovery. Adv Agron 68:197–319Google Scholar
- Lal R (2004) Soil carbon sequestration to mitigate climate change. Geoderma 123:1–22Google Scholar
- Lal R, Pimentel D (2007) Biofuels from crop residues. Soil Tillage Res 93:237–238Google Scholar
- Lamb JFS, Sheaffer CC, Samac DA (2003) Population density and harvest maturity effects on leaf and stem yield in alfalfa. Agron J 295:635–641Google Scholar
- Langeveld JWA, Sanders JPM (2010) General introduction. Chapter 1. In: Langeveld H, Sanders J, Meeusen M (eds) The biobased economy—biofuels, materials and chemicals in the post-oil era. Earthscan, London, pp 3–18Google Scholar
- Lefroy EC, Stirzaker RJ, Pate JS (2001) The influence of tagasaste (Chamaecytisus profliferus Link.) trees on the water balance of an alley cropping system on deep sand in south-western Australia. Aust J Agric Res 52:235–246Google Scholar
- Lehmann J, Gaunt J, Rondon M (2006) Bio-char sequestration in terrestrial ecosystems—a review. Mitig Adapt Strat Glob Change 11:403–427Google Scholar
- Lehtomäki A, Viinikainen TA, Rintala JA (2008) Screening boreal energy crops and crop residues for methane biofuels production. Biomass Bioenerg 32:541–550Google Scholar
- Lemke RL, Zhong Z, Campbell CA, Zentner R (2007) Can pulse crops play a role in mitigating greenhouse gases from North American agriculture? Agron J 99:1719–1725Google Scholar
- Lorek S, Lucas R (2003) Towards sustainable market strategies. A case study on eco-textiles and green power. Wupperthal Institute Report no. 130, 68 pGoogle Scholar
- Lupwayi NZ, Kennedy AC (2007) Grain legumes in Northern Great Plains: impacts on selected biological soil processes. Agron J 99:1700–1709Google Scholar
- Lægreid M, Bøckman OC, Kaarstad O (1999) Agriculture, fertilizers and the environment. CABI, WallingfordGoogle Scholar
- Mabee W, Saddler J, Nielsen C, Nielsen LH, Jensen ES (2006) Renewable-based fuels for transport. In Larsen H, Petersen LS (eds) Risø Energy Report 5. Renewable Energy for Power and transport. pp 47–50. ISBN 87-550-3515-9, Risø National Laboratory, DenmarkGoogle Scholar
- Macedo MO, Resende AS, Garcia PC, Boddey RM, Jantalia CP, Urquiaga S, Campello EFC, Franco AA (2008) Changes in soil C and N stocks and nutrient dynamics 13 years after recovery of degraded land using leguminous nitrogen-fixing trees. Forest Ecol Manag 255:1516–1524Google Scholar
- Magid J, Henriksen O, Thorup-Kristensen K, Mueller T (2001) Disproportionately high N-mineralisation rates from green manures at low temperatures—implications for modelling and management in cool temperate agro-ecosystems. Plant Soil 228:73–82Google Scholar
- Mahmood T, Ali R, Malik KA, Shamsi SRA (1998) Nitrous oxide emissions from an irrigated sandy-clay loam cropped to maize and wheat. Biol Fertil Soils 27:189–196Google Scholar
- McCallum MH, Kirkegaard JA, Green T, Cresswell HP, Davies SL, Angus JF, Peoples MB (2004) Improved subsoil macro-porosity following perennial pastures. Aust J Exp Agric 44:299–307Google Scholar
- McMurtrey JE, Daughtry CST, Devine TE, Corp LA (2005) Spectral detection of crop residues for soil conservation from conventional and large biomass soybeans. Agron Sustain Dev 25:25–33Google Scholar
- Minchin FR, Pate JS (1973) The carbon balance of a legume and the functional economy of its root nodules. J Expl Bot 24:259–271Google Scholar
- Minchin FR, Summerfield RJ, Neves MCP (1980) Carbon metabolism, nitrogen assimilation, and seed yield of cowpea (Vigna unquiculata L. Walp.) grown in an adverse temperature regime. J Expl Bot 31:1327–1345Google Scholar
- Mortensen MC, Schuman GE, Ingram LJ (2004) Carbon sequestration in rangelands interseeded with yellow-flowering alfalfa (Medicago sativa ssp. Falcate). Environ Manage 33:S475–S481Google Scholar
- Mosier A (2001) Exchange of gaseous nitrogen compounds between agricultural systems and the atmosphere. Plant Soil 228:17–27Google Scholar
- Munier-Jolain NG, Salon C (2005) Are the carbon costs of seed production related to the quantitative and qualitative performance? An appraisal for legumes and other crops. Plant Cell Environ 28:1388–1395Google Scholar
- Murphy DV, Fillery IRP, Sparling GP (1998) Seasonal fluctuations of gross N mineralisation, ammonium consumption, and microbial biomass in a Western Australian soil under different land uses. Aust J Agric Res 49:523–535Google Scholar
- Möller K, Stinner W, Deuker A, Leitholf G (2008) Effects of different manuring systems with and without biogas digestion on nitrogen cycle and crop yield in mixed organic farming systems. Nutr Cyc Agroecosyst 82:209–232Google Scholar
- Nelson RG (2002) Resource assessment and removal analysis for corn stover and wheat straw in the Eastern and Midwestern United States. Rainfall and wind-induced soil erosion methodology. Biomass Bioenerg 22:349–363Google Scholar
- Nemecek T, von Richthofen J-S, Dubois G, Casta P, Charles R, Pahl H (2008) Environmental impacts of introducing grain legumes into European crop rotations. Eur J Agron 28:380–393Google Scholar
- Nichols NN, Dien BS, Wu YV, Cotta MA (2005) Ethanol fermentation of starch from field peas. Cereal Chem 82:554–558Google Scholar
- Novalin S, Zweckmair T (2008) Renewable resources—green biorefinery: separation of valuable substances from fluid-fractions by means of membrane technology. Biofuels Bioprod Bioref 3:20–27Google Scholar
- O’Hara GW, Daniel RM (1985) Rhizobial denitrification: a review. Soil Biol Biochem 17:1–9Google Scholar
- Oleskowicz-Popiel P (2010) Biogas and bioethanol production in organic farming. PhD thesis, Risø National Laboratory for Sustainable Energy, Risø-PhD-64(EN), ISBN 978-87-550-3839-4. 47 p. Risø DTUGoogle Scholar
- Peoples MB, Baldock JA (2001) Nitrogen dynamics of pastures: nitrogen fixation inputs, the impact of legumes on soil nitrogen fertility, and the contributions of fixed nitrogen to Australian farming systems. Aust J Exp Agric 41:327–346Google Scholar
- Peoples MB, Herridge DF (1990) Nitrogen fixation by legumes in tropical and subtropical agriculture. Adv Agron 44:155–223Google Scholar
- Peoples MB, Herridge DF, Ladha JK (1995a) Biological nitrogen fixation: an efficient source of nitrogen for sustainable agricultural production? Plant Soil 174:3–28Google Scholar
- Peoples MB, Lilley DM, Burnett VF, Ridley AM, Garden DL (1995b) Effects of lime and superphosphate to acid soils on growth and N2 fixation by subterranean clover in mixed pasture swards. Soil Biol Biochem 27:663–671Google Scholar
- Peoples MB, Palmer B, Lilley DM, Duc LM, Herridge DF (1996) Application of 15N and xylem ureide methods for assessing N2 fixation of three shrub legumes periodically pruned for forage. Plant Soil 182:125–137Google Scholar
- Peoples MB, Bowman AM, Gault RR, Herridge DF, McCallum MH, McCormick KM, Norton RM, Rochester IJ, Scammell GJ, Schwenke GD (2001) Factors regulating the contributions of fixed nitrogen by pasture and crop legumes to different farming systems of eastern Australia. Plant Soil 228:29–41Google Scholar
- Peoples MB, Angus JF, Swan AD, Dear BS, Hauggaard-Nielsen H, Jensen ES, Ryan MH, Virgona JM (2004a) Nitrogen dynamics in legume-based pasture systems. In: Mosier AR, Syers KJ, Freney JR (eds) Agriculture and the nitrogen cycle, the Scientific Committee on Problems of the Environment (SCOPE). Island, Covelo, pp 103–114Google Scholar
- Peoples MB, Boyer EW, Goulding KWT, Heffer P, Ochwoh VA, Vanlauwe B, Wood S, Yagi K, Van Cleemput O (2004b) Pathways of nitrogen loss and their impacts on human health and the environment. In: Mosier AR, Syers KJ, Freney JR (eds) Agriculture and the nitrogen cycle, the Scientific Committee on Problems of the Environment (SCOPE). Island, Covelo, pp 53–69Google Scholar
- Peoples MB, Brockwell J, Herridge DF, Rochester IJ, Alves BJR, Urquiaga S, Boddey RM, Dakora FD, Bhattarai S, Maskey SL, Sampet C, Rerkasem B, Khan DF, Hauggaard-Nielsen H, Jensen ES (2009a) Review article. The contributions of nitrogen-fixing crop legumes to the productivity of agricultural systems. Symbiosis 48:1–17Google Scholar
- Peoples MB, Hauggaard-Nielsen H, Jensen ES (2009b) The potential environmental benefits and risks derived from legumes in rotations. In: Emerich DW, Krishnan HB (eds) Agronomy Monograph 52. Nitrogen Fixation in Crop Production, Am. Soc. Agron., Crop Sci. Soc. Am., and Soil Sci. Soc Am. Madison, Wisconsin, USA, pp 349–385Google Scholar
- Persson T, Bergkvist G, Katterer T (2008) Long-term effects of crop rotations with and without perennial leys on soil carbon stocks and grain yields of winter wheat. Nutr Cycl Agroecosyst 81:193–202Google Scholar
- Pimentel D (2003) Ethanol fuels: energy balance, economics, and environmental impacts are negative. Nat Resour Res 12:127–134Google Scholar
- Pimentel D, Patzek TW (2005) Ethanol production using corn, switchgrass, and wood; biodiesel production using soybean and sunflower. Nat Resour Res 14:65–76Google Scholar
- Pinkerton A, Randall PJ (1994) Internal phosphorus requirements of six legumes and two grasses. Aust J Exp Agric 34:373–379Google Scholar
- Pregelj L, McLanders JR, Gresshoff PM, Schenk PM (2011) Transcription profiling of the isoflavone phenylpropanoid pathway in soybean in response to Bradyrhizobium japonicum inoculation. Funct Plant Biol 38:13–24Google Scholar
- Pryor SW, Lenling M, Wiesenborn DP (2008) Integrated use of field pea starch and corn for ethanol production. ASABE Paper No. 083999. ASABE, St. Joseph, MIGoogle Scholar
- Radrizzani A, Shelton HM, Dalzell SA, Kirchhof G (2011) Soil organic carbon and total nitrogen under Leucaena leucocephala pastures in Queensland. Crop Pasture Sci 62:337–345Google Scholar
- Randall GW, Huggins DR, Russelle MP, Fuchs DJ, Nelson WW, Anderson JL (1997) Nitrate losses through subsurface tile drainage in conservation reserve program alfalfa, and row crop systems. J Environ Qual 26:1240–1247Google Scholar
- Rathke G-W, Wienhold BJ, Wilhelm WW, Diepenbrock W (2007) Tillage and rotation effect on corn–soybean energy balances in eastern Nebraska. Soil Tillage Res 97:60–70Google Scholar
- Reddy N, Yang Y (2009) Natural cellulose fibers from soybean straw. Biores Technol 100:3593–3598Google Scholar
- Rochester IJ (2003) Estimating nitrous oxide emissions from flood-irrigated alkaline grey clays. Aust J Soil Res 41:197–206Google Scholar
- Rochester IJ (2011) Sequestering carbon in minimum-tilled clay soils used for irrigated cotton and grain production. Soil Tillage Res 112:1–7Google Scholar
- Rochester IJ, Peoples MB, Hulugalle NR, Gault RR, Constable GA (2001) Using legumes to enhance nitrogen fertility and improve soil condition in cotton cropping systems. Field Crops Res 70:27–41Google Scholar
- Rochette P, Janzen HH (2005) Towards a revised coefficient for estimating N2O emissions from legumes. Nutr Cycl Agroecosyst 73:171–179Google Scholar
- Rochette P, Angers DA, Bélanger G, Chantigny MH, Prévost D, Lévesque G (2004) Emissions of N2O from alfalfa and soybean crops in eastern Canada. Soil Sci Soc Am J 68:493–506Google Scholar
- Rosen A, Lindgren P-E, Ljunggren H (1996) Denitrification by Rhizobium meliloti. 1. Studies of free-living cells and nodulated plants. Swed J Agric Res 26:105–113Google Scholar
- Ruz-Jerez BE, White RE, Ball PR (1994) Long-term measurement of denitrification in three contrasting pastures grazed by sheep. Soil Biol Biochem 26:29–39Google Scholar
- Ryan PA (1994) The use of tree legumes for fuelwood production. In: Gutteridge RC, Shelton HM (eds) Forage tree legumes in tropical agriculture. Chapter 5.1. CABI, WallingfordGoogle Scholar
- Samac DA, Jung H-J, Lamb JFS (2006) Development of alfalfa (M. sativa L.) as a feedstock for ethanol and other bioproducts. In: Minteer S (ed) Alcoholic fuels. CRC, Boca Raton, pp 79–98Google Scholar
- Schwenke G, Haigh B, McMullen G, Herridge D (2010) Soil nitrous oxide emissions under dryland N-fertilised canola and N2-fixing chickpea in the northern grains region, Australia. Proc. 19th World Congress of Soil Science, Soil Solutions for a Changing World, Brisbane, Australia, pp 228–231Google Scholar
- Scott PT, Pregelj L, Chen N, Hadler JS, Djordjevic MA, Gresshoff PM (2008) Pongamia pinnata: an untapped resource for the biofuels industry of the future. BioEnergy Res 1:2–11Google Scholar
- Sheehan J, Camobreco V, Duffield D, Graboski M, Shapouri H (1998) Life Cycle Inventory of Biodiesel and Petroleum Diesel for Use in an Urban Bus. 1-285. U.S. Department of Energy's Office of Fuels Development and U.S. Department of Agriculture's Office of EnergyGoogle Scholar
- Siah S, Konczak I, Agboola S, Wood J, Blanchard C (2011) Phenolic content and potential health benefits of Australian grown faba beans. British J Nutr (in press)Google Scholar
- Sisti CPJ, dos Santos HP, Kochhann RA, Alves BJR, Urquiaga S, Boddey RM (2004) Change in carbon and nitrogen stocks in soil under 13 years of conventional or zero tillage in southern Brazil. Soil Tillage Res 76:39–58Google Scholar
- Smil V (2001) Enriching the earth. MIT Press, CambridgeGoogle Scholar
- Smith GB, Smith MS (1986) Symbiotic and free-living denitrification by Bradyrhizobium japonicum. Soil Sci Soc Am J 50:349–354Google Scholar
- Smith P, Martino D, Cai C, Gwary D, Janzen H, Kumar P, McCarl B, Ogle S, O’Mara F, Rice C, Scholes B, Sirotenko O (2007) Agriculture. In: Metz B, Davidson OR, Bosch PR, Dave R, Meyer LA (eds) Climate Change 2007, Mitigation. Contribution of Working Group III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
- Soares LH de B, Muniz LC, Figueiredo RS, Alves BJR, Boddey RM, Urquiaga S, Madari BE, Machado PLO de A (2007) Balanço energético de um sistema integrado lavoura-pecuária no Cerrado. Bol. Pesq.Desenvolv. No. 26, Embrapa Agrobiologia, Seropédica (available online at: www.cnpab.embrapa.br/publicacoes/download/bot026.pdf)
- Soussana JF, Loiseau P, Vuichard N, Ceschia E, Balesdent J, Chevallier T, Arrouays D (2004) Carbon cycling and sequestration opportunities in temperate grasslands. Soil Use Manag 20:219–230Google Scholar
- Soussana JF, Tallec T, Blanfort V (2010) Mitigating the greenhouse gas balance of ruminant production systems through carbon sequestration in grasslands. Animal 4:334–350Google Scholar
- Stehfest E, Bouwman L (2006) N2O and NO emissions from agricultural fields and soils under natural vegetation: summarizing available measurement data and modeling of global annual emissions. Nutr Cycl Agroecosyst 74:207–228Google Scholar
- Stewart CE, Plante AF, Paustian K, Conant RT (2008) Soil carbon saturation: linking concept and measurable carbon pools. Soil Sci Soc Am J 72:379–813Google Scholar
- Szott LT, Palm CA, Buresh RJ (1999) Ecosystem fertility and fallow function in the humid and subhumid tropics. Agrofor Syst 47:163–196Google Scholar
- Tarré R, Macedo R, Cantarutti RB, de Rezende PC, Pereira JM, Ferreira E, Alves BJR, Urquiaga S, Boddey RM (2001) The effect of the presence of a forage legume on nitrogen and carbon levels in soils under Brachiaria pastures in the Atlantic forest region of the South of Bahia, Brazil. Plant Soil 234:15–26Google Scholar
- Teira-Esmatges MR, Van Cleemput O, Porta-Casnellas J (1998) Fluxes of nitrous oxide and molecular nitrogen from irrigated soils of Catalonia (Spain). J Environ Qual 27:687–697Google Scholar
- Thomsen MH, Hauggaard-Nielsen H (2008) Sustainable bioethanol production combining biorefinery principles using combined raw materials from straw and clover–grass. J Ind Microbiol Biotech 35:303–311Google Scholar
- Thrall PH, Millsom DA, Jeavons AC, Waayers M, Harvey GR, Bagnall DJ, Brockwell J (2005) Seed inoculation with effective root-nodule bacteria enhances revegetation success. J Appl Ecol 42:740–751Google Scholar
- Torres AQA, Jantalia CP, Franco AA, Campello EFC, Resende AS, Urquiaga S, Macedo MO, Moreira JF, Alves TG (2007) Influência de espécies de leguminosas fixadoras de nitrogênio no estoque de C no solo em plantio consorciado no bioma Mata Atlântica (in Portuguese, with English abstract). Congresso Brasileiro de Ciência do Solo 5 to 10 August, Gramada, RS. 3 p. CD-ROMGoogle Scholar
- Udvardi MK, Price GD, Gresshoff PM, Day DA (1988) A dicarboxylate transporter on the peribacteroid membrane of soybean nodules. FEBS Lett 231:36–40Google Scholar
- VandenBygaart AJ, Gregorich EG, Angers DA (2003) Influence of agricultural management on soil organic carbon: a compendium and assessment of Canadian studies. Can J Soil Sci 83:363–380Google Scholar
- Venendaal R, Jørgensen U, Foster CA (1997) European energy crops. Biomass Bioenerg 13:147–185Google Scholar
- Wagner-Riddle C, Thurtell GW (1998) Nitrous oxide emissions from agricultural fields during winter and spring thaw as affected by management practices. Nutr Cycl Agroecosyst 52:151–163Google Scholar
- Wagner-Riddle C, Thurtell GW, Kidd GK, Beauchamp EG, Sweetman R (1997) Estimates of nitrous oxide emissions from agricultural fields over 28 months. Can J Soil Sci 77:135–144Google Scholar
- Wichern F, Eberhardt E, Mayer J, Joergensen RG, Müller T (2008) Nitrogen rhizodeposition in agricultural crops: methods, estimates and future prospects. Soil Biol Biochem 40:30–48Google Scholar
- Whitbread AM, Blair GJ, Lefroy RDB (2000) Managing legume leys, residues and fertilisers to enhance the sustainability of wheat cropping systems in Australia. 2. Soil physical fertility and carbon. Soil Tillage Res 54:77–89Google Scholar
- Wilkinson CS, Fuskhah E, Indrasumunar A, Gresshoff PM, Scott PT (2012) Growth, nodulation and nitrogen gain of Pongamia pinnata and Glycine max in response to salinity. BioEnergy Res (in review)Google Scholar
- Williams CH, Donald CM (1957) Changes in organic matter and pH in a podzolic soil as influenced by subterranean clover and superphosphate. Aust J Agric Res 8:179–189Google Scholar
- Wright AL, Hons FM, Rouquette FM Jr (2004) Long-term management impacts on soil carbon and nitrogen dynamics of grazed bermudagrass pastures. Soil Biol Biochem 36:1806–1816Google Scholar
- Yang L, Cai Z (2005) The effect of growing soybean (Glycine max. L.) on N2O emission from soil. Soil Biol Biochem 37:1205–1209Google Scholar
- Young RR, Wilson B, Harden S, Bernardi A (2009) Accumulation of soil carbon under zero tillage cropping and perennial vegetation on the Liverpool Plains, eastern Australia. Aust J Soil Res 47:273–285Google Scholar
- Zapata F, Danso SKA, Hardarson G, Fried M (1987) Time course of nitrogen fixation in field-grown soybean using Nitrogen-15 methodology. Agron J 79:172–176Google Scholar
- Zentner RP, Campbell CA, Biederbeck VO, Miller PR, Selles F, Fernandez MR (2001) In search of a sustainable cropping system for the semiarid Canadian prairies. J Sustain Agric 18:117–136Google Scholar
- Zentner RP, Lafond GP, Derksen DA, Nagy CN, Wall DD, May WE (2004) Effects of tillage method and crop rotation on non-renewable energy use efficiency for a thin Black Cherozem in the Canadian prairies. Soil Tillage Res 77:125–136Google Scholar
- Zhong Z, Lemke RL, Nelson LM (2009) Nitrous oxide emissions associated with nitrogen fixation by grain legumes. Soil Biol Biochem 41:2283–2291Google Scholar