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Published online 6 November 2007
Published in Agron J 99:1700-1709 (2007)
DOI: 10.2134/agronj2006.0313s
© 2007 American Society of Agronomy
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Symposium Papers

Grain Legumes in Northern Great Plains

Impacts on Selected Biological Soil Processes

Newton Z. Lupwayia,* and Ann C. Kennedyb

a Agriculture & Agri-Food Canada, Box 29, Beaverlodge, AB, Canada T0H 0C0
b USDA-ARS, 217 Johnson Hall, Washington State Univ., Pullman, WA 99164-6421

* Corresponding author (LupwayiN{at}agr.gc.ca)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MAJOR ZONES OF INTERACTION...
 SIGNIFICANCE OF SOIL BIOTA...
 NITROGEN FIXATION
 NITROGEN CYCLING
 NUTRIENT UPTAKE
 GREENHOUSE GAS EMISSION
 BIOLOGICAL PEST CONTROL
 CONCLUSIONS
 REFERENCES
 
Cropping systems in the Northern Great Plains have shifted from fallow-based to legume-based systems. The introduction of grain legumes has impacted soil organisms, including both symbiotic and nonsymbiotic N-fixing bacteria, pathogens, mycorrhizae and fauna, and the processes they perform. These changes occur through effects of legume seed exudates, rhizosphere exudates, and decomposing crop residues. The legume–Rhizobium symbiosis results in dinitrogen (N2) fixation that adds plant available N into the soil system. It is estimated that about 171 million kg N2 was fixed by field pea (Pisum sativum L.), lentil (Lens culinaris Medik.), dry bean (Phaseolus vulgaris L.), and chickpea (Cicer arietinum L.) crops in the Canadian Prairies in 2004, representing 7% of the total fertilizer-N (2580 million kg) used by Canadian prairie farmers in that year. Similarly, an estimated 40 million kg N2 was fixed by field pea, lentil, and dry bean (including chickpea) crops in U.S. agroecosystems in 2004. Some of the fixed N2 is recycled for the benefit of nonlegume crops grown after grain legumes. Many other associations benefit from the legume in a cropping system, including mycorrhizal associations that improve plant nutrient and water uptake, changes in the pathogen load and disease development, and overall changes in the soil community. Legumes contribute to greenhouse gas (N2O and CO2) emissions during nitrification and denitrification of fixed N. However, because less fertilizer-N is used in legume-based cropping systems, overall greenhouse gas emissions are usually less than those in fertilized monoculture cereals. Therefore, grain legumes in Northern Great Plains have positive effects on agriculture by adding and recycling biologically fixed N2, enhancing nutrient uptake, reducing greenhouse gas emissions by reducing N fertilizer use, and breaking nonlegume crop pest cycles.

Grain Legumes in Northern Great Plains

Impacts on Selected Biological Soil Processes

Newton Z. Lupwayia,* and Ann C. Kennedyb

a Agriculture & Agri-Food Canada, Box 29, Beaverlodge, AB, Canada T0H 0C0
b USDA-ARS, 217 Johnson Hall, Washington State Univ., Pullman, WA 99164-6421

* Corresponding author (LupwayiN{at}agr.gc.ca)

Received for publication November 8, 2006.
Cropping systems in the Northern Great Plains have shifted from fallow-based to legume-based systems. The introduction of grain legumes has impacted soil organisms, including both symbiotic and nonsymbiotic N-fixing bacteria, pathogens, mycorrhizae and fauna, and the processes they perform. These changes occur through effects of legume seed exudates, rhizosphere exudates, and decomposing crop residues. The legume–Rhizobium symbiosis results in dinitrogen (N2) fixation that adds plant available N into the soil system. It is estimated that about 171 million kg N2 was fixed by field pea (Pisum sativum L.), lentil (Lens culinaris Medik.), dry bean (Phaseolus vulgaris L.), and chickpea (Cicer arietinum L.) crops in the Canadian Prairies in 2004, representing 7% of the total fertilizer-N (2580 million kg) used by Canadian prairie farmers in that year. Similarly, an estimated 40 million kg N2 was fixed by field pea, lentil, and dry bean (including chickpea) crops in U.S. agroecosystems in 2004. Some of the fixed N2 is recycled for the benefit of nonlegume crops grown after grain legumes. Many other associations benefit from the legume in a cropping system, including mycorrhizal associations that improve plant nutrient and water uptake, changes in the pathogen load and disease development, and overall changes in the soil community. Legumes contribute to greenhouse gas (N2O and CO2) emissions during nitrification and denitrification of fixed N. However, because less fertilizer-N is used in legume-based cropping systems, overall greenhouse gas emissions are usually less than those in fertilized monoculture cereals. Therefore, grain legumes in Northern Great Plains have positive effects on agriculture by adding and recycling biologically fixed N2, enhancing nutrient uptake, reducing greenhouse gas emissions by reducing N fertilizer use, and breaking nonlegume crop pest cycles.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MAJOR ZONES OF INTERACTION...
 SIGNIFICANCE OF SOIL BIOTA...
 NITROGEN FIXATION
 NITROGEN CYCLING
 NUTRIENT UPTAKE
 GREENHOUSE GAS EMISSION
 BIOLOGICAL PEST CONTROL
 CONCLUSIONS
 REFERENCES
 
CEREAL-FALLOW ROTATIONS have historically been the predominant cropping system in the semiarid Canadian Prairies and Northern Great Plains of the United States, mainly to reduce the risk of crop failure resulting from soil moisture deficits (Spratt et al., 1975; Grant et al., 2002). It has long been recognized that fallow-based rotations reduce soil organic matter, primarily because little plant C is returned to the soil, but also due to increased soil erosion during the fallow phase (see Janzen, 2001, for a historical perspective of concerns about organic matter loss). Soils in southern Saskatchewan and the Palouse region of the U.S. Pacific Northwest, lost about 50% of the original organic matter after more than 80 yr of wheat-fallow cropping (Campbell and Souster, 1982; Papendick and Parr, 1997; Schnitzer et al., 2006). With the advent of conservation tillage systems (minimum- or zero-tillage) in the 1970s, more soil moisture was conserved than what was possible under conventional-tillage. Continuous cropping became a viable option for producers because soil moisture was conserved in such tillage systems; consequently, fallow acreages in Canada and the United States began to decline (Fig. 1 ). Since monoculture cereal cropping often results in pest buildup (Pedersen and Hughes, 1992; Bailey et al., 2001), other crops were sought to include in rotations, as crop diversification was required (see Tanaka et al., 2002, for a historical perspective of cropping systems). Pulse crops became attractive rotation crops, and their acreages increased (Fig. 2 ). In the Canadian Prairies, field pea is grown on the greatest acreage, while lentil, chickpea, and dry bean are also grown but to a lesser extent (Fig. 2a). In the U.S. Northern Great Plains, dry bean, including chickpea, are the most common, but field pea and lentil are also grown (Fig. 2b).


Figure 1
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  		Fig. 1. Land area occupied by summer fallow in Canada and United States from 1971 to 2001. Source of data: Statistics Canada (1999) and USDA (2002), with permission.

 

Figure 2
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  		Fig. 2. Land area occupied by grain legume crops in Canada and United States from 1984 to 2004. Source of data: FAO (2005), with permission.

 
The introduction of these pulse crops to the previously fallow-based agricultural systems of the Northern Great Plains has many implications, including changes in soil biology and the resultant biological processes. In this paper we discuss the effects of pulse crops on soil microbiological and faunal relationships and some of the processes that occur during, or as a result of, these interactions. The interactions occur mostly in the zone around legume seeds (spermosphere) at planting, around roots (rhizosphere), and inside roots (in nodules or endophytically) during crop growth, and within and near decomposing crop residues (detritusphere) after harvest. In this paper, these zones of activity are described first, followed by a general discussion of the importance of soil biota in sustainable agriculture and the effects that legumes have. The impact of grain legumes on N2 fixation, N uptake, N cycling, greenhouse gas emissions, and biological pest control are then discussed. Examples from the Northern Great Plains are cited when available, otherwise examples from outside the region are given to illustrate some points. Similarly, examples on grain legumes will be cited where available, otherwise points will be illustrated using other legumes as examples.


   MAJOR ZONES OF INTERACTION BETWEEN LEGUMES AND SOIL ORGANISMS
TOP
 ABSTRACT
 INTRODUCTION
 MAJOR ZONES OF INTERACTION...
SIGNIFICANCE OF SOIL BIOTA...
 NITROGEN FIXATION
 NITROGEN CYCLING
 NUTRIENT UPTAKE
 GREENHOUSE GAS EMISSION
 BIOLOGICAL PEST CONTROL
 CONCLUSIONS
 REFERENCES
 
The spermosphere, rhizosphere, root nodules, and detritusphere are the major zones of interaction between legumes and soil microorganisms. The spermosphere is the soil zone surrounding, and influenced by, seeds. The size of the spermosphere is thought to extend anywhere from 5 to 10 mm from the seed (Short and Lacy, 1976; Stanghellini and Hancock, 1971). The term pathozone was coined to indicate the zone of influence of the spermosphere in terms of pathogen chemotaxis (Short and Wyllie, 1978; Gilligan and Bailey, 1997). For field pea, the spermosphere, if defined by the greatest distance that Fusarium solani f. sp. pisi germinated, is not more than 7 mm. The legume seed is an excellent location for microbial and macrofaunal growth and colonization. A seed progresses from a dormant, nonmetabolic state to, almost instantly, an explosive physiological response with concomitant microbial activity. The carbon released from the imbibing seed provides rich, readily available nutrients to the soil microflora. Exudates and mucilage are in abundant supply and in a constant state of flux in the spermosphere. There are many different types of interactions that can occur once imbibition of water by the seed begins. Some of the interactions are universal and occur across all species, and others are more species- and cultivar-specific (Nelson, 2004; Roberts and Ellis, 1989). These differences can change with seed and seedling maturation (Chanway et al., 1991). Exudation is greater at the emerging radicle than any other place on the seed. The influence will be felt by the entire plant as the microbial community on the seed can be passively carried along as the extending root pushes through soil for long distances. These interactions in the spermosphere can be significant to the plant, as well as the microbial community, as it sets up for the longer term and the effects of the more-influential rhizosphere microflora (Scher et al., 1984).

The rhizosphere is the volume of soil adjacent to, and influenced by, the plant root (Hiltner, 1904) and can extend to more than 5 mm away from the root. The root influences the rhizosphere through release of a variety of organic compounds which serve as sources of energy and nutrients for soil macro- and microbiota. The term rhizosphere effect describes the enhanced microbial growth and population densities in the rhizosphere, due to increased soluble C and nutrients, compared with the surrounding bulk soil (Elliott et al., 1984). These organic compounds are deposited in the rhizosphere through root exudation, sloughing-off of root cap cells, secretion of root mucilage, and senescence of root epidermis (Nguyen, 2003). Root exudates include carbohydrates, amino acids and amides, aliphatic acids, aromatic acids, phenolic compounds, fatty acids, sterols, vitamins, enzymes, and purines/nucleosides (Dakora and Phillips, 2002; Bertin et al., 2003).

One of the most widely studied beneficial plant–microbe interactions is the symbiotic relationship between legumes and Rhizobium spp. (The terms Rhizobium or rhizobia are here-in used collectively for the genera Rhizobium, Bradyrhizobium, Sinorhizobium, Mesorhizobium, Allorhizobium, and Azorhizobium, unless specified otherwise.) Interactions between rhizobia and legume roots result in formation of root nodules, in which rhizobia use energy from the host plant to transform (fix) atmospheric N2 into plant-available forms of N. Before Rhizobium can form nodules in legume roots to fix N2, the bacterium must be attracted to the roots through bidirectional host–bacterium communication (signaling). Legume root exudates contain chemical compounds, including flavonoids, that attract rhizobia to root hairs (Dakora and Phillips, 2002). Flavonoids are also involved in host specificity of rhizobia. They induce rhizobia to express nod genes that are essential for nodulation and host range. These genes encode enzymes that are involved in the synthesis and secretion of host-specific nodulation signals called Nod factors (Geurts et al., 2005). These factors, which are lipo-chito-oligosaccharides, signal back to the plant and induce deformation of the root hair that results in infection and formation of the root nodule.

After legume crop harvest, residues returned to soil are colonized by soil microorganisms because the residues are a source of C (and other nutrients) for microbial growth and respiration. The litter (crop residue) and the adjacent soil modified by the presence of litter have been called the detritusphere (Gaillard et al., 2003; Poll et al., 2006). The magnitude of the increase in abundance and activity of microorganisms in the detritusphere depends on the biochemical composition of the residues (Gaillard et al., 2003) and environmental factors (e.g., soil temperature and moisture).


   SIGNIFICANCE OF SOIL BIOTA AND EFFECTS OF LEGUMES
TOP
 ABSTRACT
 INTRODUCTION
 MAJOR ZONES OF INTERACTION...
 SIGNIFICANCE OF SOIL BIOTA...
NITROGEN FIXATION
 NITROGEN CYCLING
 NUTRIENT UPTAKE
 GREENHOUSE GAS EMISSION
 BIOLOGICAL PEST CONTROL
 CONCLUSIONS
 REFERENCES
 
Soil biota have a profound but often subtle effect on agriculture. The presence of a large and diverse soil microbial and faunal community is crucial to the productivity of any agroecosystem, regardless of management. The soil biota are responsible for many soil processes, which can include residue decomposition, nutrient cycling, organic matter transformations, degradation of agrochemicals, and building soil tilth and structure (Wood, 1991; Swift and Anderson, 1993). Beneficial soil organisms can enhance plant performance by increasing mineral solubilization (Chabot et al., 1996), N2 fixation (Chemining'wa and Vessey, 2006), production of plant hormones (Brown, 1972; Zahir et al., 2003), and suppression of harmful pathogens (Janvier et al., 2007). Often these organisms can be manipulated to produce beneficial effects for agriculture and the environment; for example, inoculation with rhizobia to increase plant-available N in legumes (Van Kessel and Hartley, 2000; Vessey, 2004), mycorrhizal associations to assist nutrient uptake (Sylvia, 1998; Vazquez et al., 2002; Feng et al., 2003), or biological control of plant pests to reduce chemical inputs (Cook and Baker, 1983; Paulitz, 1991). Soil biotic processes are key in producing and reducing greenhouse gases (Davidson, 1991; Drinkwater et al., 1998). However, their contributions to the complete nutrient budget are not totally understood.

The type and functional characteristics of the species in agroecosystems may be as important as the number of species (Grime, 1997; Hopper and Vitousek, 1997). Microfauna (e.g., protozoa and microbe-feeding nematodes) graze on microflora, and mesofauna (e.g., Collembola and oribatid mites) feed on certain soil fungi. These interactions affect nutrient cycling. Mineralization of N has been found to increase in the presence of microbial grazers due to release of ammonium from consumed rhizosphere bacteria (Alphei et al., 1996). Increasing the density of Collembola has been shown to reduce clover (Trifolium subterraneum L.) infection by arbuscular mycorrhizae, P uptake, and growth (Larsen and Jakobsen, 1996). Addition of low C:N ratio organic material (e.g., legume green manure) to soil increases the biomass of bacterivorous (bacteria-feeding) nematodes early in the decomposition process, whereas addition of high C:N ratio organic material (e.g., cereal straw) stimulates fungivorous nematodes late in the decomposition process (Ferris and Matute, 2003; Georgieva et al., 2005). Because of these observations, it has been suggested that nematodes may be useful indicators of substrate quality and nutrient release during residue decomposition (Griffiths, 1994).

The benefits of including a legume in a crop rotation are numerous and have been used for thousands of years to improve crop yields. Legumes in rotation may break a disease cycle, add N and C, and alter the biology of the system. Crop species diversity, cropping intensity, and crop rotation affect microbial activity and diversity (Thomas and Kevan, 1993). The plant community composition may, in fact, drive the soil biotic community (Halvorson et al., 2005). In Saskatchewan, Biederbeck et al. (2005) examined microbial populations and enzyme activities after 6 yr of monoculture wheat, fallow-wheat, or legume green manure-wheat rotations. In almost all cases (except urease activity), microbial populations and enzyme activities were higher in legume-based rotations than in fallow-wheat rotation or monoculture wheat (Table 1 ). Similarly, in fields with prior history of forage legumes in the crop rotation in Ontario, there were increases in activities of the soil enzymes dehydrogenase, urease, glutaminase, phosphatase, arylsulfatase, and ß-glucosidase (Bergstrom et al., 1998). While these examples are from forage or cover crop legumes, it appears likely that rotations containing grain legumes will also result in greater microbial activity. In Alberta, microbial diversity of soils under wheat (Triticum aestivum L.) preceded by red clover (Trifolium pratense L.) or field pea was higher than in wheat preceded by summer fallow or continuous wheat (Lupwayi et al., 1998). A no-till corn (Zea mays L.)-soybean [Glycine max (L.) Merr.] rotation in Missouri had higher populations of earthworm [Aporrectodea trapezoids (Dugés)] than a no-till wheat-corn rotation (Hubbard et al., 1999). Different crops in a rotation, including legumes, were shown to stimulate nonpathogenic strains of Fusarium oxysporum, which leads to suppression of Fusarium wilt (Edel et al., 1997).


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  		Table 1. Effects of legume green manure on soil microbial populations and enzyme activities in the 0- to 10-cm depth after 6 yr (sampled after the wheat phase of the rotations). (Reprinted with modification from Biederbeck et al., 2005, with permission from Elsevier.){dagger}

 
Legumes may exhibit different effects on the soil biota due to the fact that plants and their seed and root exudates drive the soil biotic activity and community structure near the seed and root. Legume exudates differ in amount and composition from the exudates of other crop species, thus the rhizosphere communities may be different (Duineveld et al., 1998; Ibekwe and Kennedy, 1998; Ohtonen et al., 1999). Field pea and oat (Avena sativa L.) seeds exude very different profiles of amino acids, with field pea excreting 22 amino acids while oat excreted only 14 (Powell and Matthews, 1981). Legumes like lupin (Lupinus albus L.) and chickpea exude large amounts of organic acids into the rhizosphere, particularly in low-P soils, and these acid exudates mobilize P from pools of otherwise unavailable soil P (Veneklaas et al., 2003). Differences between legumes and other crops in the biochemical composition of their residues also affect the composition of decomposer soil biota. Changes in the diversity and function of the members in a soil food web will influence the productivity of a soil (Thomas and Kevan, 1993). Some of the microbiological processes that are influenced by legume crops include N2 fixation, N cycling, nutrient uptake, greenhouse gas emissions, and biological pest control.


   NITROGEN FIXATION
TOP
 ABSTRACT
 INTRODUCTION
 MAJOR ZONES OF INTERACTION...
 SIGNIFICANCE OF SOIL BIOTA...
 NITROGEN FIXATION
NITROGEN CYCLING
 NUTRIENT UPTAKE
 GREENHOUSE GAS EMISSION
 BIOLOGICAL PEST CONTROL
 CONCLUSIONS
 REFERENCES
 
Grain legumes, in symbiosis with rhizobia, fix up to 450 kg N2 ha–1 (Unkovich and Pate, 2000). On the lower end of this scale are chickpea (0–141 kg ha–1), dry bean (0–165 kg ha–1), and lentil (5–191 kg ha–1), and on the upper end are lupin (Lupinus spp.) (19–327 kg ha–1), faba bean (Vicia faba L.) (12–330 kg ha–1) and soybean (0–450 kg ha–1). In the Canadian prairies, Biederbeck et al. (1996) estimated that field pea fixed 90 kg N2 ha–1, lentil fixed 56 kg ha–1, and dry bean fixed 30 kg ha–1 in 1994. In Saskatchewan, five chickpea varieties fixed an average of 26 kg N2 ha–1 per year in three seasons (Thavarajah et al., 2005). If these N2 fixation rates are multiplied by the respective land areas occupied by these crops in 2004 (Fig. 2a), it is estimated that 124.5, 40.3, 4.8, and 1.3 million kg N2 were fixed by field pea, lentil, dry bean, and chickpea crops, in that order, in Canadian prairie agroecosystems in 2004. Similarly, 18.2, 6.6, and 15.2 kg N2 were fixed by field pea, lentil, and dry bean (including chickpea) crops, in that order, in U.S. agroecosystems in 2004 if the same N2 fixation rates are assumed. In Canada, the total 171 million kg N2 fixed by pulse crops in 2004 represented 6.6% of the total fertilizer-N (2580 million kilograms) used by prairie farmers in that year (Canadian Fertilizer Institute, 2005).

The increase in pulse acreages in the Northern Great Plains has led to reexamination of inoculant formulations and methods of delivery for N2–fixing bacteria. Direct application of peat powder inoculant to seed was the most common method until an easier method of seed application with liquid inoculants was introduced (Hynes et al., 1995). Research has since shown that soil inoculation (i.e., direct application of inoculant to the soil in the vicinity of the legume seed) is usually more effective than seed inoculation (Kyei-Boahen et al., 2002; Clayton et al., 2004a, 2004b; Gan et al., 2005a, 2005b). The advantage of using granular inoculants is especially pronounced under soil stress conditions like soil acidity, low soil moisture, or cool, wet soils. Under moisture stress, granular inoculant applied to the soil was more effective in maintaining field pea yield than seed-applied inoculants (Miller et al., 2002). Under cool, wet conditions in the spring, the rhizobial population in field pea rhizosphere continued to increase when granular inoculant was used, but with the seed-applied liquid inoculant, the populations declined for a period of time before recovering (Hynes et al., 2001). If soil inoculation is more effective than seed inoculation, the effectiveness of soil inoculation with liquid inoculant is also worth investigating.

The distribution and diversity of specific strains of N2–fixing bacteria vary with environmental conditions and presence or absence of legume hosts (Strain et al., 1994). Management, the environment, as well as the plant community, can influence Rhizobium, and thus impact the diversity of this group of microorganisms (Turco and Bezdicek, 1987; Hirsch et al., 1993; Strain et al., 1994; Ferreira et al., 2000). Crop rotations in Brazil containing soybean resulted in higher populations and greater diversity and activity of Bradyrhizobium than those without soybean, even though more than 15 yr had passed since inoculation (Ferreira et al., 2000). However, research in the Canadian prairies has shown that field pea tend to respond to inoculation even in soils that contain infective and effective indigenous strains of Rhizobium leguminosarum bv. viciae, (Chemining'wa and Vessey, 2006).


   NITROGEN CYCLING
TOP
 ABSTRACT
 INTRODUCTION
 MAJOR ZONES OF INTERACTION...
 SIGNIFICANCE OF SOIL BIOTA...
 NITROGEN FIXATION
 NITROGEN CYCLING
NUTRIENT UPTAKE
 GREENHOUSE GAS EMISSION
 BIOLOGICAL PEST CONTROL
 CONCLUSIONS
 REFERENCES
 
Nitrogen is recycled mostly during decomposition of above- and belowground crop residues. Nitrogen cycling is mainly mediated by soil microorganisms, and the rate and pattern of N release from crop residues is regulated by soil microbial activity and residue quality. Environmental conditions like soil moisture and temperature affect N mineralization by influencing soil microbial activity (Vigil and Kissel, 1995; Agehara and Warncke, 2005). Mineralization of N is usually positively correlated with residue N concentration and negatively correlated with C:N, lignin:N and polyphenol:N ratios (Lupwayi and Haque, 1999; Lupwayi et al., 2006).

Most of the N in legume crops is in the grain and is removed from the farm at harvest in the high-protein legume seeds. This removal of N through grain harvest means that (i) little N is returned to the soil with pulse crop residues (e.g., 22 kg N ha–1 in field pea residues in northwestern Alberta, Soon and Clayton, 2002); and (ii) the crop residues have wide C:N, lignin:N, and polyphenol:N ratios, and therefore decompose slowly, which means that the little N that they contain is released even more slowly or immobilized by the decomposing microflora. For example, field pea cut at flowering stage had an average C:N ratio of 20 and lignin:N ratio of 2, but the residues after grain harvest had a C:N ratio of 63 and a lignin:N ratio of 14 (Lupwayi et al., 2006). The difference between fixed N and N contained in the harvested grain (i.e., the amount of fixed N that remains after crop harvest) is the N balance, which can be positive (net N credit) or negative (net N deficit). In the Canadian prairies, Biederbeck et al. (1996) estimated net N credits of 18 kg N ha–1 for field pea, 9 kg ha–1 for lentil, and 0 kg ha–1 for dry bean in 1994. In a rotational benefits study in Manitoba, field pea provided the largest and most consistent apparent N benefit (11–14 kg N ha–1 per 1000 kg grain yield) to the following wheat crop, the benefits of chickpea and common bean were inconsistent, and soybean provided virtually no benefit (Przednowek et al., 2004).

Net N credits do not indicate how much of the crop residue N will actually be released to the crops(s) grown after a grain legume crop. 15Nitrogen studies have shown that a succeeding crop can recover 2 to 26% of the N applied through grain legume residues (Mohr et al., 1998; Giller et al., 1997; Fillery, 2001). Bremer and Van Kessel (1992) estimated that only 7% of N in lentil straw was mineralized in the following growing season and concluded that lentil straw was not a significant source of soil N. Soon and Arshad (2002) and Lupwayi et al. (2006) reported net N mineralization from pea straw of 6 kg N ha–1 and 4 to 18 kg N ha–1, respectively. However, N benefits from pulse crop residues are usually still greater than those from cereal residues, where N is mostly immobilized. The N contribution by decomposing legume roots is usually not added to these estimates due to methodological difficulties.

Nitrogen sparing is another way in which legume crops contribute N to intercropped or rotation crops. Since part of their N requirement is met by N2 fixation, legumes utilize less of the available soil N than cereals, thereby sparing or conserving inorganic N for the intercrop or following crop (Chalk et al., 1993; Herridge et al., 1995). However, N sparing is not universal because legumes sometimes take up as much or even more soil inorganic N than comparable nonlegume crops (Unkovich and Pate, 2000).

Even when legume crop residues result in short-term N immobilization, they increase soil organic matter when used in crop rotations. Soil organic matter improves the soil physical structure that may reduce soil erosion and increase water and nutrient retention. Grain legumes also increase biological diversity in ecosystems.


   NUTRIENT UPTAKE
TOP
 ABSTRACT
 INTRODUCTION
 MAJOR ZONES OF INTERACTION...
 SIGNIFICANCE OF SOIL BIOTA...
 NITROGEN FIXATION
 NITROGEN CYCLING
 NUTRIENT UPTAKE
GREENHOUSE GAS EMISSION
 BIOLOGICAL PEST CONTROL
 CONCLUSIONS
 REFERENCES
 
Mycorrhizae
Mycorrhizae are nonpathogenic fungi that form symbiotic associations with plant roots. Mycorrhizal fungi associate with roots of pulse crops, and terms like mycorrhizosphere (Linderman, 1988) and hyphosphere (Li et al., 1991) have been used to describe portions of the rhizosphere in which this association occurs (Linderman, 1988). The beneficial relationship between the two can increase the uptake of nutrients and water in plants, and can influence N2 fixation in legumes by improving host nutrition (Ocampo, 1986). Hamel (2004) has reviewed the impact of mycorrhizae on crop N and P nutrition. This relationship in turn can also influence other microorganisms in the community by altering nutrient status and other interactions (Johnson et al., 1992). Mycorrhizal associations have the greatest impact on plant growth in stressed environments, P-deficient soils, eroded sites, and acidic or reclaimed lands (Barea, 1991). Crop rotations, especially those with legumes, can increase root colonization by mycorrhizae (Douds et al., 1997). Cover crops, such as vetches (Vicia spp.), have been shown to increase the vesicular arbuscular mycorrhizae (VAM) inoculum potential for subsequent crops (Boswell et al., 1998; Galvez et al., 1995). Borie et al. (2002) demonstrated that lupin residues increased mycorrhizal colonization of wheat more than wheat residues, and mycorrhizal wheat acquired more P but less Zn, Cu, Mn, and Al in an acid soil. The interaction involving mycorrhizal fungi and rhizobia may also influence plant growth by increasing N and P acquisition (Xavier and Germida, 2002).

Endophytic Rhizobia
Roots of nonlegume crops grown in rotation with legumes contain endophytic rhizobia. When barley (Hordeum vulgare), wheat, and canola (Brassica rapa L.) were each grown in monoculture or in rotation with field pea in northern Alberta, populations of endophytic rhizobia up to 7244 cells g–1 root DM were observed in field pea-based rotations, but <10 cells g–1 root DM were observed in monoculture (Lupwayi et al., 2004a). These endophytic rhizobia and other bacteria have been found to increase yields of nonlegume crops (Biswas et al., 2000; Riggs et al., 2001), but there is no conclusive evidence that the benefits involve symbiotic N2 fixation (James, 2000; Yanni et al., 2001). These bacteria increase yields by stimulating plant growth, increasing disease resistance, or improving the plant's ability to withstand environmental stresses like drought (Dobbelaere et al., 2003). The rhizobia act as plant growth-promoting rhizobacteria (PGPR) that have been shown to expand the root architecture of the crop, enabling it to accumulate more N, P, K, Ca, Mg, Na, Zn, and Mo than control plants (Yanni et al., 2001). Therefore, rhizobia contribute to the rotational benefits of legumes in cropping systems in more ways than fixing N. Even in legumes, seed treatment with rhizobia has been shown to reduce disease incidence. In field experiments in southern Alberta, treatment of field pea and lentil seed with Rhizobium leguminosarum bv. viciae reduced the incidence of damping-off, a disease caused by soilborne pathogens Pythium spp. (Huang and Erickson, 2007). However, the relative roles of crop protection and crop nutrition in the effects of rhizobia (as PGPR) on nonlegume crops require clarification.


   GREENHOUSE GAS EMISSION
TOP
 ABSTRACT
 INTRODUCTION
 MAJOR ZONES OF INTERACTION...
 SIGNIFICANCE OF SOIL BIOTA...
 NITROGEN FIXATION
 NITROGEN CYCLING
 NUTRIENT UPTAKE
 GREENHOUSE GAS EMISSION
BIOLOGICAL PEST CONTROL
 CONCLUSIONS
 REFERENCES
 
Legumes contribute to N2O emissions because the atmospheric N2 fixed by the legume during Rhizobium symbiosis is nitrified and denitrified like fertilizer-N (Rochette et al., 2004). Also, rhizobia in root nodules are capable of denitrification as well as N2 fixation. While high rates of denitrification by Rhizobium species have been shown in laboratory studies, losses of N occurring in the field due to denitrification by these species are inconsistent or not well documented (O'Hara and Daniel, 1985). Therefore, the ecological implications of denitrification by rhizobia are not well understood.

Greenhouse gases (mainly CO2 and N2O) are also produced during microbial utilization of organic compounds in the spermosphere, rhizosphere, and detritusphere. Nitrous oxide emissions, in particular, occur during nitrification (in well aerated soil) or denitrification (in poorly aerated soil) of soil N from inorganic or organic sources. The time of gas sampling in relation to the time of residue placement is important in assessing the effects of legume residues on greenhouse gas emissions. When sampling was done only in the following crop in rotation (i.e., months after residue placement in the preceding season), Lupwayi et al. (1999) reported less CO2 evolution in plots preceded by legume crops than in monoculture wheat. When sampling started at the time of residue placement, results showed a peak of CO2 evolution within weeks of placement, and the peak was greater and earlier with legume (especially green manure) residues than other residues (Lupwayi et al., 2004b). Similar results were reported by Schomberg and Steiner (1997) and Sarrantonio (2003). Huang et al. (2004) and Toma and Hatano (2007) found that both N2O and CO2 emissions were negatively correlated with the C to N ratio of crop residues (i.e., pulse crop residues may produce more N2O and CO2 than cereal residues if the pulse residue C to N ratio is narrower than that of cereal residue). When crop rotations that included legume crops were compared with rotations that had no legume crops in research results collated from N2O measurements in Alberta, Saskatchewan, Ontario, and Quebec over a 10-yr period, Helgason et al. (2005) reported higher N2O emissions from systems with field pea in rotation than from nonlegume systems even though the nonlegume plots received substantially more N fertilization than did the legume system.

Since legume crops are grown with little or no fertilizer-N, emissions of N2O are expected to be less in a legume crop than in a fertilized cereal crop even though legume root exudates may result in increased gas emissions. This was the case in the Canadian study quoted above (Helgason et al., 2005) when emissions were compared in paired legume (receiving 0 or 5 kg ha–1 fertilizer-N yr–1) vs. nonlegume (receiving 0–190 kg N ha–1 yr–1) crops. In Quebec, Rochette et al. (2004) reported greater N2O emissions under fertilized timothy grass (Phleum pratense L.) than under alfalfa and soybean, and Gregorich et al. (2005) found similar results (legume-based systems vs. fertilized annual crops) in eastern Canada and northeastern United States. In addition, the reduced use of fertilizer-N in legume-based cropping systems means less burning of fossil fuel (CO2 emission) in manufacturing, transporting, and applying fertilizer-N. In Saskatchewan, Zentner et al. (2001) reported 24% less total energy requirement in a lentil-wheat rotation compared with a wheat-wheat system because lentil N reduced fertilizer-N requirements for subsequent wheat. In Michigan, Robertson et al. (2000) calculated the global warming potentials associated with several fertilizer-based and legume-based cropping systems by weighting each gas (CO2, N2O, and CH4) emitted in each cropping system on the basis of its potency as a greenhouse gas, and aggregating the results. In a corn-soybean-wheat rotation, the tilled and fertilized system had a net GWP of 114, the organic with legume cover crop system 41, and the no-till fertilized system 14 CO2 equivalents (g m–2 yr–1) (Table 2 ). The difference between the first two systems was mainly due to fossil fuel required to produce fertilizer-N and the use of lime. Using similar accounting on a 20-yr field experiment in Ontario, Meyer-Aurich et al. (2006) reported that diversifying corn rotations with soybean and wheat underseeded with red clover (corn-corn-soybean-wheatred clover rotation) resulted in mitigation of about 1300 kg CO2 equivalents per hectare per year, and that adding alfalfa into a corn rotation (corn-corn-alfalfa-alfalfa rotation) could mitigate more than 2000 kg CO2 equivalents per hectare per year. The contribution of legumes to greenhouse gas emissions were more than offset by reduced emissions from less fertilizer manufacture and use, and increased soil carbon sequestration. Crews and Peoples (2004) also concluded that obtaining N from legumes is potentially more sustainable than from industrial sources. Therefore, the effects of legumes on greenhouse gas emissions depend on the level at which they are examined (i.e., crop level, farm level, or national level, Table 3 ). It is clear that the reduced use of N fertilizers in legume crops results in less gas emissions than fertilized nonlegume crops at farm and national levels due to reduced fuel use in manufacturing, transportation, and application of the fertilizer.


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  		Table 2. Relative greenhouse gas global warming potentials (GWPs in g CO2 equivalents m–2 yr–1, based on Intergovernmental Panel on Climate Change conversion factors) for different management systems of a corn-soybean-wheat rotation in Michigan from 1991 to 1999. Source: Robertson et al. (2000).

 

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  		Table 3. Greenhouse gas emissions from legume and nonlegume crops at crop, farm, or national levels.

 

   BIOLOGICAL PEST CONTROL
TOP
 ABSTRACT
 INTRODUCTION
 MAJOR ZONES OF INTERACTION...
 SIGNIFICANCE OF SOIL BIOTA...
 NITROGEN FIXATION
 NITROGEN CYCLING
 NUTRIENT UPTAKE
 GREENHOUSE GAS EMISSION
 BIOLOGICAL PEST CONTROL
CONCLUSIONS
 REFERENCES
 
Legume and nonlegume losses from disease and injury, which can be due to bacteria, fungi, viruses, protozoa, nematodes, and other macrofauna, are found throughout agricultural ecosystems. They can have a large impact on plant growth and can be a determining factor in plant productivity (Burdon, 1987). Soilborne pathogens may affect plant competitiveness and plant succession (Van der Putten and Peters, 1997).

The production of amino acids by legume seeds is thought to play a part in the success of plant beneficial microorganisms; however, not all spermosphere environments support biocontrol agents. The biocontrol efficacy of Pseudomonas putida N1R on Pythium ultimum was due to the competitiveness of the P. putida N1R for the seed exudates. Damping off caused by Pythium did not succeed when N1R could interfere with the stimulation of Pythium by the exudates (Paulitz, 1991). Pseudomonas cepacia was an effective biocontrol agent against Pythium ultimum when the bacterium was applied to seed and colonized the spermosphere (Parke, 1990). Long-chain saturated fatty acids from seeds stimulate the germination of sporangia of Pythium ultimum (Nelson, 1990). Enterobacter cloacae, a biocontrol agent used to suppress Pythium, reduces the response of Pythium to the germinating seed by metabolizing long-chain fatty acid seed exudates (Nelson, 1990). The inactivation of the pathogen by E. cloacae occurs with many different plant species, but was not evident with corn or field pea due to their high rate of exudation relative to other plant species. The presence of high levels of sugars may reduce the metabolism of the long-chain fatty acids, and thus reduce the biocontrol efficacy (Kageyama and Nelson, 2003). Legumes have been shown to stimulate several nonpathogenic strains of F. oxysporum. An increase in the nonpathogenic strains reduces the impact of Fusarium wilt (Edel et al., 1997).

Growing the same crop continuously on the same piece of land fosters buildup of pests (pathogens, insects, and weeds) to which the crop is susceptible. Rotating crops with nonhost crops interrupts the pest cycle. For cereals, rotations with legumes are particularly attractive because the legumes are likely to contribute N to the soil–plant system as well as interrupt pathogen cycles. In Saskatchewan, sporulation of the soilborne pathogen Cochliobolus sativus, which causes common root rot in cereals, on several hosts sampled in the fall was found to be in the order: cereal crops > pulse crops > oilseed crops, forage grasses, and forage legumes (Duczek et al., 1996). Stevenson and Van Kessel (1996) found that the incidence of wheat common root rot had a score of 0.99 (on a 0–4 scale) in a field pea-wheat rotation compared with 3.19 in wheat monoculture. Bailey et al. (2001) found similar results. Downy brome (Bromus tectorum L.) weed populations in Alberta were lower in lentil-based and canola-based wheat rotations than in continuous wheat, possibly due to the greater use of selective herbicides in these rotations (Blackshaw et al., 1994). These pest control benefits of legumes do not always occur, and opposite effects on Pythium spp. have been reported in wheat in Australia (Pankhurst et al., 1995). However, the increased microbial diversity and activity in legume spermosphere, rhizosphere, or detritusphere usually promotes biological pest control (Janvier et al., 2007).


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MAJOR ZONES OF INTERACTION...
 SIGNIFICANCE OF SOIL BIOTA...
 NITROGEN FIXATION
 NITROGEN CYCLING
 NUTRIENT UPTAKE
 GREENHOUSE GAS EMISSION
 BIOLOGICAL PEST CONTROL
 CONCLUSIONS
REFERENCES
 
The impacts of grain legumes on soil biota begin from the time seed is planted and continue after crop harvest. The altered soil biology has mostly beneficial effects to agriculture by adding and recycling biologically fixed N2, enhancing nutrient uptake, reducing greenhouse gas emissions by reducing N fertilizer use, and breaking crop pest cycles. Soil inoculation with granular rhizobial inoculant seems to be more effective in increasing N2 fixation than seed inoculation, but there is need to also investigate soil inoculation using liquid inoculant. Most studies on the contribution of pulse crops to the N economy of the following crop are conducted in only one subsequent crop. Multiyear studies are required to show whether net N immobilization (if it occurs) in the first year of residue decomposition changes to net N mineralization in later years as the C:N ratio narrows. The role of N rhizodeposition in contribution of N to subsequent crops needs further study because usually only contributions from aboveground legume residues are quantified. The increased microbial diversity and activity when legume crops are grown usually mitigates disease through enhanced biological pest control. However, there is need to separate pest control effects resulting from broken pest cycles or increased biological activity from those resulting from pesticides used in the legume phase of crop rotations. It is also unclear how many years the pest control benefits last after a legume crop. Grain legume crops have increased the sustainability of the wheat-dominated cropping systems of the Northern Great Plains, but further research in the issues outlined here will enhance their impact.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MAJOR ZONES OF INTERACTION...
 SIGNIFICANCE OF SOIL BIOTA...
 NITROGEN FIXATION
 NITROGEN CYCLING
 NUTRIENT UPTAKE
 GREENHOUSE GAS EMISSION
 BIOLOGICAL PEST CONTROL
 CONCLUSIONS
 REFERENCES
 





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