Multiple benefits of legumes for agriculture sustainability: an overview

Abstract

Food security, lowering the risk of climate change and meeting the increasing demand for energy will increasingly be
critical challenges in the years to come. Producing sustainably is therefore becoming central in agriculture and food
systems. Legume crops could play an important role in this context by delivering multiple services in line with sustainability
principles. In addition to serving as fundamental, worldwide source of high-quality food and feed, legumes
contribute to reduce the emission of greenhouse gases, as they release 5–7 times less GHG per unit area compared
with other crops; allow the sequestration of carbon in soils with values estimated from 7.21 g kg−1 DM, 23.6 versus
21.8 g C kg−1 year; and induce a saving of fossil energy inputs in the system thanks to N fertilizer reduction, corresponding
to 277 kg ha−1 of CO2 per year. Legumes could also be competitive crops and, due to their environmental
and socioeconomic benefits, could be introduced in modern cropping systems to increase crop diversity and reduce
use of external inputs. They also perform well in conservation systems, intercropping systems, which are very important
in developing countries as well as in low-input and low-yield farming systems. Legumes fix the atmospheric
nitrogen, release in the soil high-quality organic matter and facilitate soil nutrients’ circulation and water retention.
Based on these multiple functions, legume crops have high potential for conservation agriculture, being functional
either as growing crop or as crop residue.

Full text

Stagnari et al. Chem. Biol. Technol. Agric. (2017) 4:2
DOI 10.1186/s40538-016-0085-1
REVIEW
Multiple benets oflegumes
foragriculture sustainability: an overview
Fabio Stagnari1*, Albino Maggio2, Angelica Galieni1 and Michele Pisante1
Abstract
Food security, lowering the risk of climate change and meeting the increasing demand for energy will increasingly be
critical challenges in the years to come. Producing sustainably is therefore becoming central in agriculture and food
systems. Legume crops could play an important role in this context by delivering multiple services in line with sus-
tainability principles. In addition to serving as fundamental, worldwide source of high-quality food and feed, legumes
contribute to reduce the emission of greenhouse gases, as they release 5–7 times less GHG per unit area compared
with other crops; allow the sequestration of carbon in soils with values estimated from 7.21 g kg−1 DM, 23.6 versus
21.8 g C kg−1 year; and induce a saving of fossil energy inputs in the system thanks to N fertilizer reduction, corre-
sponding to 277 kg ha−1 of CO2 per year. Legumes could also be competitive crops and, due to their environmental
and socioeconomic benefits, could be introduced in modern cropping systems to increase crop diversity and reduce
use of external inputs. They also perform well in conservation systems, intercropping systems, which are very impor-
tant in developing countries as well as in low-input and low-yield farming systems. Legumes fix the atmospheric
nitrogen, release in the soil high-quality organic matter and facilitate soil nutrients’ circulation and water retention.
Based on these multiple functions, legume crops have high potential for conservation agriculture, being functional
either as growing crop or as crop residue.
Keywords: Soil fertility, Conservation agriculture, Sustainable agricultural systems, Food security, Climate change,
Greenhouse gas, Energy
© The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License
(http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium,
provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license,
and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/
publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Introduction
Global population will hit 9.6 billion people by 2050 [108]
and will face global challenges among which achiev-
ing food security, lowering the risk of climate change
by reducing the net release of greenhouse gases into
the atmosphere and meeting the increasing demand
for energy are the most critical ones. In particular, the
impact of climate change and associated biotic and abi-
otic stresses to which crop systems will be increasingly
exposed pose serious implications for global food pro-
duction [119].
To meet these challenges, a policy framework needs to
be developed in which the sustainability of production/
consumption patterns becomes central. In this context,
food legumes and legume-inclusive production systems
can play important roles by delivering multiple services
in line with sustainability principles. Indeed, legumes
play central roles [112]: (1) at food-system level, both for
human and animal consumption, as a source of plant pro-
teins and with an increasingly importance in improving
humans health [106]; (2) at production-system level, due
to the capacity to fix atmospheric nitrogen making them
potentially highly suitable for inclusion in low-input
cropping systems, and due to their role in mitigating
greenhouse gases emissions [53]; and (3) at cropping-
system levels, as diversification crops in agroecosystems
based on few major species, breaking the cycles of pests
and diseases and contributing to balance the deficit in
plant protein production in many areas of the world,
including Europe [43, 48, 72, 78, 116].
Leguminosae family comprises 800 genera and 20,000
species [54] and represents the third largest family of
flowering plants. Some legumes are considered weeds of
Open Access
*Correspondence: fstagnari@unite.it
1 Faculty of Biosciences and Technologies for Agriculture Food
and Environment, University of Teramo, Coste Sant’Agostino, Teramo, TE,
Italy
Full list of author information is available at the end of the article
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Page 2 of 13
Stagnari et al. Chem. Biol. Technol. Agric. (2017) 4:2
cereal crops, while others are major grain crops; these
latter species are known as grain legumes, or pulses,1 and
represent the focus of this review. For some of these spe-
cies, the trends for word acreage and yield are available,
as reported in Table1.
Despite the growing trends observed during the
50-year period between 1974 and 2014 for some
warm-season legumes (e.g. soybean, cowpea, dry bean,
groundnut, and pigeon pea), the acreages of several
temperate legumes (e.g. pea, faba bean, lupin, french
bean and vetch) have declined worldwide with differ-
ences between world Regions (Table3). In any case,
food legumes occupy a minimal part of arable land,
mostly dominated by cereal crops [99]; soybean rep-
resents the most important and cultivated legume,
acreage of which reached 117.72 million ha in 2014
(steadily increased over years, see also Table3), which
is about that of the other grain legumes, but still far
below the major cereals (e.g. rice, wheat, maize). Such
trend is mainly associated to the expansion of more
specialized and intensive production systems [82].
1 Soybean and groundnuts are not defined by FAO as ‘pulse crops’.
Market forces stimulating specialization of cropping
systems as non-marketable benefits of diversification,
like cultivation/introduction of legumes in the farm-
ing system, do not deliver immediate and/or apparent
profits [82]. This is, however, not equally perceived
throughout the globe, and there is indeed a remarkable
diversity in grain legumes’ production trends across
the world (Table3).
e European decline in grain legume’s produc-
tion is not mirrored by other regions of the world such
as Canada or Australia, where legume’s cultivation
has been increasing over the last few decades. In these
areas, monoculture of cereals, which relies on frequent
summer-fallowing and use of mechanical tillage, has
been replaced by extended and diversified crop rotations
together with the use of conservation tillage [122]. Fur-
thermore, supply chains and markets are inadequately
developed for most legume crops (see also [66], for
France) with the exception of soybean, for which the
global market is well developed [85]. Nevertheless, soy-
bean areas in Europe are constrained by climatic factors
although there is considerable potential to develop new
varieties suitable to flourish under cool growing condi-
tions [123].
Table 1 Trends forword acreage (million ha) andyield (t ha−1) forlegume crops included inFAOSTAT classication start-
ing from1974 to2014 [23]; the major three cereal crops are also reported, forcomparison
In Table2, for each legume crop, item name and code as well as FAO denitions are reported
a Data are referred to year 2013 (2014 data not available)
Harvested area (Million ha) Yield (t ha−1)
1974 1984 1994 2004 2014 1974 1984 1994 2004 2014
Legume crops
Bambara bean 0.05 0.05 0.09 0.12 0.37 0.67 0.66 0.64 0.65 0.77
Dry bean 23.9 26.3 26.7 27.3 30.14 0.53 0.6 0.65 0.67 0.83
Faba bean 3.98 3.32 2.48 2.65 2.37 1.07 1.29 1.45 1.62 1.82
Chickpea 10.6 9.85 9.96 10.5 14.8 0.56 0.67 0.71 0.8 0.96
Cowpea 4.7 3.66 7.35 9.18 12.52 0.35 0.31 0.38 0.45 0.45
Groundnut 19.9 18.2 22 23.7 25.68 0.94 1.1 1.3 1.54 1.65
Lentil 2.03 2.56 3.43 3.85 4.52 0.61 0.68 0.81 0.93 1.08
Lupin 0.76 1.06 1.56 1.05 0.76 0.84 1.05 0.78 1.18 1.3
Pea 8.13 8.91 7.65 6.34 6.87 1.22 1.3 1.88 1.85 1.65
Pigeon pea 3.04 3.61 4.24 4.72 6.67 0.54 0.78 0.74 0.7 0.73
Soybean 37.4 52.9 62.5 91.6 117.72 1.41 1.71 2.18 2.24 2.62
French bean 0.22 0.17 0.22 0.23 0.20a5.76 6.93 7.44 9.04 9.32a
Vetch 1.52 1.29 0.93 0.89 0.52 1.24 1.21 1.12 1.43 1.71
Pulses, nes 5.67 5.65 5.33 4.27 6.1 0.54 0.58 0.65 0.82 0.84
Vegetables, leguminous nes 0.14 0.18 0.18 0.25 0.24a5.41 5.09 5.18 6.54 6.86a
Major cereal crops
Wheat 222.12 230.77 215.12 216.57 221.62 1.62 2.22 2.45 2.92 3.29
Maize 119.86 127.76 137.99 147.45 183.32 2.56 3.53 4.12 4.94 5.66
Rice (paddy) 136.89 144.24 147.29 150.58 163.25 2.43 3.23 3.66 4.03 4.54
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Stagnari et al. Chem. Biol. Technol. Agric. (2017) 4:2
e low diffusion of legumes’ cultivation is also due to
reduced and unstable yields and susceptibility to biotic
and abiotic stress conditions; the average yields for
unit area have increased (soybean +86%, lentil +77%,
groundnut +75%, chickpea +70%) less than cereal crops
(+104%, on average) (Table1). Moreover, legume cultiva-
tion depends not only on the effect of farmers’ choices,
although they play a central role for such decision, but
also on policymakers who have the responsibility to pro-
vide effective strategies to support the integration of leg-
umes into cropping systems. is aspect is particularly
relevant if the overall objective for future agricultural sys-
tems is to promote sustainability, improve resource use
efficiency and preserve the environment [82].
Grain legumes impacts onatmosphere andsoil
quality
Among the many important benefits that legumes deliver
to society, their role in contributing to climate change
mitigation has been rarely addressed. Legumes can (1)
lower the emission of greenhouse gases (GHG) such as
carbon dioxide (CO2) and nitrous oxide (N2O) compared
Table 2 Denition oflegume crops focused inTable1 andcorresponding item name inFAOSTAT
Legume crop Scientic name Corresponding FAO item name andcode FAO denition
Bambara bean Voandzeia subterranea Bambara bean [203] Bambara groundnut, earth pea. These beans
are grown underground in a similar way to
groundnuts
Dry bean – Beans, dry [176] Phaseolus spp.: kidney, haricot bean (Ph. vulgaris);
lima, butter bean (Ph. lunatus); adzuki bean (Ph.
angularis); mungo bean, golden, green gram (Ph.
aureus); black gram, urd (Ph. mungo); scarlet run-
ner bean (Ph. coccineus); rice bean (Ph. calcara-
tus); moth bean (Ph. aconitifolius); tepary bean
(Ph. acutifolius). Several countries also include
some types of beans commonly classified as
Vigna (angularis, mungo, radiata, aconitifolia)
Faba bean Vicia faba Broad beans, horse beans, dry [181] Vicia faba: horse-bean (var. equina); broad bean
(var. major); field bean (var. minor)
Chickpea Cicer arietinum Chick peas [191] Chickpea, Bengal gram, garbanzos (Cicer arieti-
num).
Cowpea Vigna ungiculanta Cow peas, dry [195] Cowpea, blackeye pea/bean (Vigna sinensis; Doli-
chos sinensis)
Groundnut Arachis hypogaea Groundnuts, with shell [242] Arachis hypogaea. For trade data, groundnuts in
shell are converted at 70% and reported on a
shelled basis
Lentil Lens esculenta Lentils [201] Lens esculenta; Ervum lens
Lupin – Lupins [210] Lupinus spp. Used primarily for feed, though in
some parts of Africa and in Latin America some
varieties are cultivated for human food
Pea – Peas, dry [187] Garden pea (Pisum sativum); field pea (P. arvense)
Pigeon pea Cajanus cajan Pigeon peas [197] Pigeon pea, cajan pea, Congo bean (Cajanus cajan)
Soybean Glycine max Soybeans [236] Glycine soja
French bean – String beans [423] Phaseolus vulgaris; Vigna spp. Not for shelling
Vetches Vicia sativa Vetches [205] Spring/common vetch (Vicia sativa). Used mainly
for animal feed
Pulses, nes – Pulses, nes [211] Including inter alia: lablab or hyacinth bean
(Dolichos spp.); jack or sword bean (Canavalia
spp.); winged bean (Psophocarpus tetragonolo-
bus); guar bean (Cyamopsis tetragonoloba); velvet
bean (Stizolobium spp.); yam bean (Pachyrrhizus
erosus); Vigna spp. other than those included in
176 and 195; other pulses that are not identified
separately because of their minor relevance at
the international level. Because of their limited
local importance, some countries report pulses
under this heading that are classified individually
by FAO
Vegetables, leguminous nes – Vegetables, leguminous nes [420] Vicia faba. For shelling
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Stagnari et al. Chem. Biol. Technol. Agric. (2017) 4:2
with agricultural systems based on mineral N fertiliza-
tion, (2) have an important role in the sequestration of
carbon in soils, and (3) reduce the overall fossil energy
inputs in the system.
Greenhouse gas emissions
e introduction of legumes into agricultural rota-
tions help in reducing the use of fertilizers and energy
in arable systems and consequently lowering the GHG
emissions [52]. N fertilizer savings across Europe [51],
in rotations including leguminous crops, range around
277kgha−1 of CO2 per year (1kgN=3.15kg CO2, [42].
It has been reported that half of the CO2 generated dur-
ing NH3 production would be reused if the NH3 was
converted to urea. is is, however, only a time shift of
CO2 release in the atmosphere since, once the urea is
applied to the soil, the hydrolyzation activity by urease
will release CO2 originally captured during urea produc-
tion [39]. Considering an efficiency of 2.6–3.7 kg CO2
generated per kilogram of N synthesized, the annual
global fertilizer leads to a release of 300Tg of CO2 into
the atmosphere each year [42]. Some studies indicate
that at global scale, the amount of CO2 respired from
the root systems of N2-fixing legumes could be higher
than the CO2 generated during N-fertilizer production
[42]. However, it is important to emphasize that the
CO2 respired from nodulated roots of legumes comes
from the atmosphere through the photosynthesis activ-
ity. Conversely, all the CO2 released during the process
of N-fertilizer synthesis derives from fossil energy, thus
determining a net contribution to atmospheric amount
of CO2 [42].
N2O represents about 5–6% of the total atmospheric
GHG, but it is much more active2 than CO2 [21]. Agricul-
ture represents the main source of anthropogenic N2O
emissions (about 60%; [84], due to both animal and crop
production [38]). A majority of these emissions result
from the application of nitrogen fertilizers [84]: every
100kg of N fertilizer about 1.0kg of N is emitted as N2O
[42], although different amounts depend on several fac-
tors including N application rate, soil organic C content,
soil pH, and texture [78, 88]. Denitrification processes are
the most important source of N2O in most cropping and
pasture systems [76, 88, 102].
In the recent years, several studies have focalized on
the role of legumes in the reduction of GHG emissions.
Jeuffroy et al. [44] demonstrated that legume crops
2 N2O absorbs approximately 292 times as much infra-red radiation per
kilogram as CO2.
Table 3 Trend forRegion Δ acreage (%) duringthe 50-year period starting from1974 to2014 forlegume crops included
inFAOSTAT classication [23]; the major three cereal crops are also reported, forcomparison
In Table2, for each legume crop, item name and code as well as FAO denitions are reported
a Data are referred to year 2013 (2014 data not available)
Δ harvested area 1974–2014 (%)
Africa Northern America South America Asia Europe Oceania
Legume crops
Bambara bean +612 – – – – –
Dry bean +207 +16 −20 +25 −84 +1778
Faba bean +7 Disappeared −53 −59 −54 +75,085
Chickpea +30 Appeared +1+37 −35 –
Cowpea +168 Appeared Appeared +402 +153 –
Groundnut +69 −10 −22 +6+16 −39
Lentil −20 +3376 −75 +72 −45 Appeared
Lupin −82 – +577 −89 −64 +315
Pea +49 +1119 +7−21 −63 +578
Pigeon pea +226 – −83 +108 – –
Soybean +642 +71 +882 +116 +291 −10
French bean Appeareda−39a+129a+66a−18a+122a
Vetch +109 – – −73 −80 +4757
Pulses, nes +20 – −69 −15 +73 +7648
Vegetables, leguminous nes +180aAppeareda+118a+23a−31a−52a
Major cereal crops
Wheat +11 −20 +16 +39 −33 +51
Maize +98 +29 +45 +76 +21 +31
Rice (paddy) +185 +15 −16 +16 −28 +2
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Page 5 of 13
Stagnari et al. Chem. Biol. Technol. Agric. (2017) 4:2
emit around 5–7 times less GHG per unit area com-
pared with other crops. Measuring N2O fluxes, they
showed that peas emitted 69kg N2Oha−1, far less than
winter wheat (368 kg N2O ha−1) and rape (534 kg
N2O ha−1). Clune et al. [19] reviewed different life
cycle-assessment (LCA) studies on GHG emissions
carried out from 2000 to 2015 around the world
(despite the used literature was predominately Euro-
pean centric) highlighting that pulses have a very low
Global Warming Potential (GWP) values (0.50–0.51kg
CO2 eqkg−1 produce or bone-free meat3). In a compar-
ison between vetch and barley under Mediterranean
environments and alkaline soil, N2O emissions were
higher for barley than vetch; furthermore, the N2O
fluxes derived from the synthetic fertilizers added to
the crops were 2.5 times higher in barley compared
with vetch [29]. In two field experiments conducted in
a black Vertosol in sub-tropical Australia, Schwenke
etal. [95] demonstrated that the cumulative N2O emis-
sions from N-fertilized canola greatly exceeded those
from chickpea, faba bean and field pea (385 vs. 166, 166
and 135g N2O-Nha−1, respectively). e same authors
highlighted that grain legumes significantly reduced
their emission factors suggesting that legume-fixed N is
a less-emissive form of N input to the soil than ferti-
lizer N.
Nevertheless, it is important to highlight that the
influence of legumes in reducing GHG depends also on
the management of agro-ecosystems in which they are
included. When faba bean was grown as mono crop-
ping, it led to threefold higher cumulative N2O emissions
than that of unfertilized wheat (441 vs. 152g N2Oha−1,
respectively); conversely, when faba bean was mixed with
wheat (intercropping system), cumulative N2O emissions
fluxes were 31% lower than that of N-fertilized wheat
[96]. Anyway, the benefits derived from the introduction
of legumes in crop rotations become significant when
commercially relevant rates of N fertilizer are applied
[42].
e mitigation in terms of GHG emissions is also
obtained by adopting sustainable agricultural systems,
such as conservation tillage and conservation agriculture
systems, which are suitable for the cultivation of both
grain and green-manure legumes (see “Grain legumes
and conservation agriculture” section).
In conclusion, it is noteworthy to underline that field
tests and experimental analyses on GHG emissions, and
in particular on N2O, provided quite different results [89]
due to the influences of differences of several variables,
3 In the study of Clune et al. [19], each GWP value recorded from the
literature data was converted into a common functional unit and system
boundary in kg CO2 eqkg−1 bone-free meat (BFM), using the conversion
ratios identified in the literature.
including climatic, soil and management conditions [45,
78, 88].
In general, N2O losses from soils covered with leg-
umes are certainly lower than those from both N2O
fertilized grasslands and non-legume crops, as also indi-
cated by Jensen etal. [42] who report a mean of 3.22kg
N2O-N ha−1, calculated from 67 site years of data. In
addition, there is no direct association between N2O
emissions and biological nitrogen fixation [42], since
organic N from legume residues is decomposed, miner-
alized and rapidly immobilized by microorganisms [78].
Emissions of N2O could occur either during nitrifica-
tion or due to denitrification, being affected by timing
of mineralized N supply [20]: the asynchrony between N
supply and utilization from the following crops enhances
N loss, especially in winter/early spring in cold wet soils
[64].
Soil properties
Cultivation and cropping may cause significant SOC
losses through decomposition of humus [18]. Shifting
from pasture to cropping systems may result in loss of
soil C stocks between 25 and 43% [101].
Legume-based systems improve several aspects of
soil fertility, such as SOC and humus content, N and P
availability [42]. With respect to SOC, grain legumes
can increase it in several ways, by supplying biomass,
organic C, and N [27, 53], as well as releasing hydro-
gen gas as by-product of BNF, which promotes bacte-
rial legume nodules’ development in the rhizosphere
[49].
In sandy soils, the beneficial effect of grain legumes
after three years of study was registered in terms of
higher content of SOC compared with soils with oats
(7.21 g kg−1 DM, on average). Specifically, cultiva-
tion of pea exerted the most positive action to organic
carbon content (7.58 g kg−1, after harvest, on aver-
age), whereas narrow-leaved lupin had the least effect
(7.23 g kg−1, on average) [30]. In southern America
(Argentina), the intercropping of soybean with maize
at different rates favoured a SOC accumulation of
23.6g C kg−1 versus 21.8g C kg−1 of the sole maize;
the greatest potential for enhancing SOC stocks
occurred in the 2:3 (maize:soybean) intercrop configu-
ration [11]. Furthermore, just only amending the soil
with soybean residues allows to obtain an increase of
38.5% in SOC [11].
anks to BNF, legumes also affect significantly soil
N availability; by using legumes as winter crops in rice–
bean and rice–vetch combination, rice residue N con-
tent is enhanced by 9.7–20.5%, with values ranging from
1.87 to 1.93gNkg−1 soil [120]. It needs to be underlines
that a majority of studies on the role of legumes for soil
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Page 6 of 13
Stagnari et al. Chem. Biol. Technol. Agric. (2017) 4:2
N fertility have investigated the shoot N content. In this
regard, Carranca et al. [15] found that 7–11% of total
legume N was associated with root and nodules and an
allocation of 11–14kg N fixed t−1 belowground dry mat-
ter, representing half the amount of total aboveground
plant.
In intercropping cowpea–maize, Latati et al. [50]
found an increase in P availability at rhizosphere level
associated with significant acidification (−0.73U) than
in sole cropping. Wang etal. [115], assessing proper-
ties related to N and P cycling in the rhizosphere of
wheat and grain legumes (faba bean and white lupin)
grown in monoculture or in wheat/legume mixtures,
found that the less-labile organic P pools (i.e. NaOH-
extractable P pools and acid-extractable P pools) sig-
nificantly accumulated in the rhizosphere of legumes.
However, the P uptake and the changes in rhizosphere
soil P pools seem to depend also on legume species.
Compared with the unplanted soil, the depletion of
labile P pools (resin P and NaHCO3-P inorganic) was
the greatest in the rhizosphere of faba bean (54 and
39%) with respect to chickpea, white lupin, yellow lupin
and narrow-leafed lupin [31]. Of the less-labile P pools,
NaOH-P inorganic was depleted in the rhizosphere of
faba bean, while NaOH-P organic and residual P were
most strongly depleted in the rhizosphere of white
lupin [31].
Also in North Rift, Kenya Region, in well-drained,
extremely deep, friable clay, acid humic top soil, the
effects of cultivation and incorporation of lupine and gar-
den pea were significant in terms of soil-available P with
respect to fallow, with lupine showing higher P availabil-
ity than pea (from 20.3 to 31.0% higher).
Although there is a general agreement on the influence
of grain legumes on rhizosphere properties in terms of
N supply, SOC and P availability, the magnitude of the
impact varied across legume species, soil properties and
climatic conditions. Among these, soil type represents
the major factor determining plant growth, rhizosphere
nutrient dynamics and microbial community structure.
e pattern of depletion and accumulation of some
macro- and micronutrients differed also between crop-
ping systems (i.e. monoculture, mixed culture, narrow
crop rotations) as well as among soil management strate-
gies (i.e. tillage, no-tillage).
Role ofgrain legumes incropping systems
Legumes could be competitive crops, in terms of envi-
ronmental and socioeconomic benefits, with potential
to be introduced in modern cropping systems, which
are characterized by a decreasing crop diversity [24, 80]
and an excessive use of external inputs (i.e. fertilizers and
agrochemicals).
Grain legumes intocrop‑sequences
In the recent years, many studies have focused on the
sustainable re-introduction of grain legumes into crop
rotations,4 based on their positive effects on yield and
quality characteristics on subsequent crops [46, 82, 103].
However, assessment of the rotational advantages/disad-
vantages should be based on a pairwise comparison
between legume and non-legume pre-crops [82]. Some
experimental designs involving multi-year and multispe-
cies rotations do not provide information on yield bene-
fits to the subsequent species in the rotation sequence.
erefore, it is difficult to formulate adequate conclu-
sions [2].
e agronomic pre-crop benefits of grain legumes can
be divided into a ‘nitrogen effect’ component and ‘break
crop effect’ component. e ‘nitrogen effect’ component
is a result of the N provision from BNF [77], which is
highest insituations of low N fertilization to subsequent
crop cycles [82]. e second one (break crop effect)
includes non-legume-specific benefits, such as improve-
ments of soil organic matter and structure [34], phospho-
rus mobilization [98], soil water retention and availability
[2], and reduced pressure from diseases and weeds [87].
In this case, benefits are highest in cereal-dominated
rotations [82].
Several authors have reviewed the yield benefits of leg-
umes for subsequent cereal crops.
In Australia, Angus etal. [2] reported higher yield of
wheat after legumes (field peas, lupins, faba beans, chick-
peas and lentils) than those of wheat after wheat. In par-
ticular for a wheat–wheat yield of 4.0t ha−1, the mean
grain legume-wheat yield was 5.2tha−1 (+30% on aver-
age). Other studies from Australia quantified yield ben-
efits compared to pure cereal crop sequences at 40–50%
for low N levels and 10–17% for high N levels [3].
In Europe yields benefits of grain legumes have been
shown to strongly depend on climatic factors which
affect N dynamics in soils [52]. In temperate environ-
ments, cereals yield is on average 17 and 21% higher in
grain-legume based systems than wheat monocropping,
under standard and moderate fertilization levels, respec-
tively [40]. Conversely, yield benefits are lower in Medi-
terranean climates where water availability is the limiting
factor to cereal yields [46, 61, 62].
e yield advantage to subsequent cereal crops pro-
vided by legumes depends also on the species and
amounts of fixed N [114, 121]. Field pea and faba bean
4 According to Angus etal. [2], crop-sequences experiments can be classi-
fied into rotation experiments and break crop experiments. Rotation strictly
defined, refers to a recurring sequence of crops, forages and fallows, or
more loosely defined, to a cropping sequence that contains fallows, or crops
and forages in addition to the locally dominant species. A break crop gener-
ally refers to a single alternative crop followed by the dominant species.
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Page 7 of 13
Stagnari et al. Chem. Biol. Technol. Agric. (2017) 4:2
accumulate about 130 and 153kgNha−1 in their above-
ground biomass, respectively [77] and significant quan-
tities (30–60% of the accumulated total N) may also be
stored in belowground biomass [77]. Differences in BNF
patterns are also found between the same species. For
example, Mokgehle etal. [69] compared 25 groundnut
varieties for plant BNF at three differing agro-ecologies
in South Africa, highlighting N-fixed range between 76
and 188 kg ha−1, depending also on soil and environ-
mental conditions as well as on N-uptake. Other factors
influencing BNF include salinity and sodicity (alkalinity)
of soils, as observed in chickpea [83], common bean [22]
and faba bean [109].
It is, however, rather difficult to quantify the legume
dependent increase in N uptake in subsequent crops,
versus other sources of N [46, 77]. In temperate envi-
ronments of Australia, measurements of the additional
N-nitrate available to wheat crops following legumes
instead of cereals, averaged around 37kgNha−1 [17]. In
Denmark, nitrogen uptake in crops that follow legume
crops has been reported to increase by 23–59% after field
pea and narrow-leafed lupin on different soil types [40],
but only 14–15% for durum wheat following vetch in a
semi-arid Mediterranean environment [28]. Increased N
uptake of crops after grain legumes reached up to 61%
or 36kgha−1 for a vetch-barley rotation in Cyprus [74].
Further, some legume residues have beneficial effects on
some quality aspects of the subsequent crops in southern
Italy [104].
Among other beneficial effects brought about by leg-
umes, the production of hydrogen gas (H2) as a by-prod-
uct of BNF greatly affects the composition of the soil
microbial population, further favouring the development
of plant growth-promoting bacteria [2].
Some grain legumes, including chickpea, pigeon
pea and white lupin can mobilize fixed forms of soil P
through the secretion of organic acids such as citrate
and malate and other P mobilizing compounds from
their roots [36]. Among grain legumes, white lupin most
strongly solubilize P, a function that can be facilitated by
its proteoid roots that may englobe small portions of soil
[2]. Glasshouse experiments using a highly P-fixing soil
showed better wheat growth following white lupin than
soybean [37], suggesting that the cereal was able to access
P made available by the previous white lupin break crop.
‘Break crop’ effects also include increased soil water con-
tent, since the break-crop stubble can affect retention
of soil water and infiltration and retention of rain water
[47]. A species-specific response has also been docu-
mented. Soil profiles after pea field can be wetter than
after a wheat crop [2]. In Saskatchewan, Canada, Miller
et al. [68] reported that post-harvest soil water status
up to 122cm-depth was 31 and 49mm greater for all
legumes (field pea, lentil and chick pea) with respect of
wheat under loam and clay soils, respectively. is was
primarily due to increased plant water use efficiency.
Lentil in rotation with cereals has been shown to increase
total grain production by increasing residual soil water in
dry areas of Saskatchewan [25].
In general, grain legumes are not susceptible to the
same pests and diseases as the main cereal crops (non-
host), resulting suitable as break crops in wheat-based
rotations [121]. Grain legumes as break crops can also
contribute to weed control [97] by contrasting their spe-
cialization and helping stabilizing the agricultural crop
weed community composition [7].
Despite the described beneficial effects, there are still
concerns on the introduction of grain legumes into crop-
ping sequences. Cropping systems that include legume
crops in farm rotations must be supported by best crop-
management practices (e.g. N fertilization rates and tim-
ing, soil management, weeding, irrigation), which often
do not match standard techniques normally applied by
farmers. For example, some possible risks in terms of
nitrate leaching associated to grain legumes cultivation
can be counteracted by including cover crops in the sys-
tem [33, 81]. Additional reasons may explain why grain
legumes are not very common in high-input cropping
systems. ese include (1) their low and unstable yields
[16, 86]; (2) inadequate policy support [14]; (3) lack of
proper quantification (and recognition) of long-term
benefits of legumes within cropping systems [82]. How-
ever, other efforts could be addressed, for example, to
breeding programs for improved crop cultivars, to better
sustain livelihood and increase the economic return to
farmers. Indeed, during last years significant progresses
in breeding for quality traits for food [110] and feed uses
[79], as well as for resistances to biotic [91] and abiotic
stresses [4] are being achieved, but several others, many
of which are controlled quantitatively by multiple genes,
have been more difficult to achieve.
Grain legumes inintercropping
Intercropping systems consist in simultaneous growth of
two or more crop species on the same area and at the
same time [13]. Intercropping is widely used in develop-
ing countries or in low-input and low-yield farming sys-
tems [73]. Despite several recognized beneficial aspects
of intercropping such as better pest control [60], com-
petitive yields with reduced inputs [70, 107], pollution
mitigation [63], more stable aggregate food or forage
yields per unit area [100], there are a number of con-
strains that make intercropping not common in modern
agriculture, such as example the request of a single and
standardized product and the suitability for mechaniza-
tion or use of other inputs as a prerogative in intensive
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Page 8 of 13
Stagnari et al. Chem. Biol. Technol. Agric. (2017) 4:2
farming system [13]. It is therefore necessary to opti-
mize intercropping systems to enhance resource-use
efficiency and crop yield simultaneously [55], while also
promoting multiple ecosystem services (see also [13]).
Most recent research has focalized on the potential of
intercropping in sustainable productions and in par-
ticular on grain legumes that can fix N2 through bio-
logical mechanisms (BNF). Indeed, legumes are pivotal
in many intercropping systems, and of the top 10 most
frequently used intercrop species listed by Hauggaard-
Nielsen and Jensen [32], seven are legumes One of the
basic spatial arrangements used in intercropping is
strip intercropping, in which two or more crops grow
together in strips wide enough to permit separate crop
production using inputs but close enough for the crops
to interact. e current challenge is how to determine an
optimal intercropping width to maximise the resources
use efficiency and, consequently, the crop productivity.
In a maize-bean strip intercropping, Mahallati etal. [65]
suggested that strip width of 2 and 3 rows was superior
compared with monoculture and other strip intercrop-
ping combinations in terms of radiation absorption,
radiation use efficiency and biological yields of both
species, also allowing to an improve of total land pro-
ductivity and land equivalent ratio (1.39 and 1.37). Gao
etal. [26] showed a total yield increase of 65 and 71% in
a system of 1 and 2 rows of maize (planted at a higher
density in intercropping) alternated with 3 rows of soy-
bean compared with both crops grown as monoculture.
However, Liu etal. [59] showed a reduction in the pho-
tosynthetically active radiation and R:FR ratio at the
top of soybean canopy intercropped with maize - under
two intercropping patterns: 1 row of maize with 1 row
of soybean; 2 rows of maize with 2 rows of soybean -
leading to increased internode lengths, plant height and
specific leaf area (SLA), but reduced branching of soy-
bean plants. In order to gain sufficient light in the most
shaded border rows of the neighbouring, shorter crops,
efforts could be addressed to (i) the selection of highly
productive maize cultivars with reduced canopy height
and LAI; (ii) the increase of the strip width under a
higher fraction of direct PAR; (iii) the selection of crops
and cultivars suitable under the shade levels that likely
occur in strip-intercropping systems with maize [71].
e increase in N availability in intercrops hosting leg-
umes occurs because the competition for soil N from
legumes is weaker than from other plants. Moreover,
non-legumes obtain additional N from that released by
legumes into the soil [56, 117] or via mycorrhizal fungi
[113]. Legumes can contribute up to 15% of the N in an
intercropped cereal [57], thus increasing biomass pro-
duction and carry-over effects [75], reducing synthetic
mineral N-fertilizer use and mitigating N2O fluxes [9,
96]. However, the adoption of grain legume intercrop-
ping systems should benefit from the identification of
suitable legumes that are less susceptible to N fertilizer-
induced inhibition of BNF—that is, legumes that sustain
higher %BNF in the presence of increasing soil mineral
N. To this purpose, Rose etal. [90] indicated that faba
bean is more suitable as intercrop than chickpea when
supplementary N fertilizer additions are required, with
about 40%BNF and 29%BNF maintained in faba bean
and chickpea, respectively, supplying both crops with
150kgNha−1.
BNF represents the most common plant growth stim-
ulating factor that can also improve crop competition
with respect to weeds in both organic and sustainable
farming systems [10]. Grain legumes are weak suppres-
sors of weeds, but mixing species in the same crop-
ping system could represent a valid way to improve the
ability of the crop itself to suppress weeds [41, 94]. In
a wheat-chickpea intercropping system (20cm spacing
without weeding treatment) it was observed a 69.7%
reduction in weed biomass and 70% in weed population
as compared to un-weeded monocrop wheat at 20cm
spacing [6]. Similar results on weed smothering have
been obtained by Midya et al. [67] in rice-blackgram
(20 cm) intercropping system although the deferred
seeding of blackgram in rice field (30 cm) with one
weeding may be recommended for both better yield and
weed suppression.
Direct mutual benefits in cereal-legumes intercropping
involve below-ground processes in which cereals while
benefiting of legumes-fixed N, increase Fe and Zn bio-
availability to the companion legumes [118].
Physiology, agronomy and ecology can simultaneously
contribute to the improvement of intercropping systems,
allowing to enhance crop productivity and resource-use
efficiency, so making intercropping a viable approach for
sustainable intensification, particularly in regions with
impoverished soils and economies where measured ben-
efits have been greatest [93]. But to realize these goals,
major efforts in research programs still remain. For exam-
ple: (1) breeding for intercrops; (2) better understanding
of the interactions between plants and other organisms in
crop systems, focusing on the roles of above- and below-
ground interactions of plants with other organisms; (3)
improving agricultural engineering and management, i.e.
developing new machinery that can till, weed and harvest
at small spatial scales and in complex configurations to
encourage the uptake of intercropping without greater
demands for labour [58]; (4) adoption of a wider ‘systems
thinking’ through the enactment of schemes, including
payment for ecosystem services [105].
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Page 9 of 13
Stagnari et al. Chem. Biol. Technol. Agric. (2017) 4:2
Grain legumes andconservation agriculture
Legumes have some characteristics particularly suitable
for sustainable cropping systems and conservation agri-
culture, and making them functional either as growing
crop or as crop residue. Conservation agriculture is based
on minimal soil disturbance and permanent soil cover
combined with rotations [35]. As previously described,
major advantages of legumes include the amount of
nitrogen fixed into the soil and the high quality of the
organic matter released to the soil in term of C/N ratio.
Some legume species have also deep root systems, which
facilitate nutrients solubilization by root exudates and
their uptake/recycling as well as water infiltration in
deeper soil layers.
Many countries already rely on conservation agricul-
ture. Brazil has implemented conservation agriculture
systems using soybean as legume crop. Grain legumes
like lentil, chickpea, pea and faba bean play a major role
in conservation agriculture in North America, Australia,
and Turkey. In Australia, some advantages of minimum
tillage for grain legumes have been quantified for water-
limited environments. Some studies indicate that the
majority of grain-legumes producers use direct seeding
after a legume pre-crop [1]. is change from conven-
tional tillage (CT) to reduced or no tillage (NT) systems
(with at least 30% of the soil surface covered) would lead
to significant positive impacts on SOC [18]. In contrast,
other results indicate that such positive effects are lim-
ited to the first 20cm depth, while little or no difference
between CT and NT in total SOC can be seen lower
down the soil profile [5, 111]. Such findings suggest that
C stock changes in the soil are mainly dependent to the
net N-balance in the system. With high N harvest index
legumes, SOC stocks are not preserved due to the high
amount of N taken off from the field into the grain [42].
Conversely, the effect of legumes on soil carbon seques-
tration is more detectable for forage, green-manures
and cover-crops which return to the soil large amounts
of organic C and N [52]. Boddey etal. [12] indicate that
vetch under no tillage may increase SOC stocks under
NT (0–100 cm) at a rate between 0.48 and 1.53Mg C
ha−1 per year [42].
e implementation of practices of conservation till-
age could significantly reduce the GWP, especially when
a grain legumes is added to the rotation. In Mediter-
ranean agro-ecosystems, Guardia et al. [29] compared
three tillage treatments (i.e. no tillage: NT, minimum
tillage: MT, conventional tillage: CT) and two crops (i.e.
vetch, barley) and recorded the emission of N2O, CH4
and CO2 during one year. Authors found a significant
‘tillage×crop’ interaction on cumulative N2O emissions
with vetch releasing higher N2O amount than barley only
in CT and MT, whereas similar fluxes were observed
under NT. is was attributable to the soil water-filled
pore space, dissolved organic carbon content and denitri-
fication losses, in spite of the presumable predominance
of nitrification. In any case, the most sustainable crop
and tillage treatments in terms of GWP were represented
by the non-fertilized vetch and NT, due to higher carbon
sequestration, lower fuel consumption and the absence
of mineral N fertilizers [29]. In subtropical Ultisol, under
legume cover crops, NT soil exhibited increased N2O
emissions with respect to CT soil (531 vs. 217kg CO2
eqha−1 year−1); however, emissions of this gas from NT
soil were fully offset by CO2 retention in soil organic mat-
ter (−2063 to −3940kg CO2 ha−1 year−1) [8]. Moreover,
NT soil under legume cover crops behaved as a net sink
for GHG (GWP ranged from −971 to −2818kg CO2 eq
ha−1 year−1) [8].
e expansion of ecological-based approaches like con-
servation agriculture opens opportunities to food leg-
umes to be profitably included in sustainable cropping
systems. ere are still major challenges for conserva-
tion agriculture that need to be overcome, including the
development of effective methods for weed control (see
also [92]) that can avoid the use of herbicides or tillage.
Overall conservation agriculture is an environmentally
sustainable production system that may boost the incor-
poration of grain legumes within large and small-scale
farming.
Conclusion
e roles and importance of grain legumes in a context
of sustainability in agriculture could be enhanced by the
emerging research opportunities for the major topics dis-
cussed above.
A major task in the future will be the selection of leg-
ume species and cultivars which could be effectively
introduced across different cropping systems. An impor-
tant point concerns balancing yield, which gives eco-
nomic return, with the environmental and agronomic
benefits.
Some priority areas seem emerge. Nitrogen fixation
activity of grain legumes should be evaluated in relation
with soil, climatic, plant characteristics and management
conditions to find the suitable approach to achieve the
best improvements. With this respect, the ability of the
host plant to store fixed nitrogen appears to be a major
component of increasing nitrogen fixation input. A par-
ticular focus should be paid also to the study of abiotic
stress limitations and in particular water deficit, salinity
and thermal shocks require extensive investigation.
Legumes that can recover unavailable forms of soil
phosphorus could be major assets in future cropping
systems. Consequently, those legumes which are able to
accumulate phosphorus from forms normally unavailable
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Page 10 of 13
Stagnari et al. Chem. Biol. Technol. Agric. (2017) 4:2
need to be further studied, since phosphorus represents
an expensive and limiting resource in several cropping
systems.
Because of the growing request for plant products, i.e.
protein and oils, and to the increased economic and envi-
ronmental pressures on agro-eco systems, it emerges that
grain legumes would play a major role in future cropping
systems.
Abbreviations
GHG: greenhouse gases; CO2: carbon dioxide; N2O: nitrous oxide; LCA: life
cycle assessment; GWP: global warming potential; BNF: biological nitrogen
fixation; NT: no tillage; CT: conventional tillage.
Authors’ contributions
FS participated in the topic literature view and selection, and in drafting
of the manuscript. AM drafted the manuscript and revised it critically. AG
participated in the topic literature view and selection, and in the drafting of
the manuscript. MP drafted the manuscript and revised it critically. All authors
read and approved the final manuscript.
Author details
1 Faculty of Biosciences and Technologies for Agriculture Food and Environ-
ment, University of Teramo, Coste Sant’Agostino, Teramo, TE, Italy. 2 Depart-
ment of Agricultural Science, University of Naples Federico II, Via Università
100, Portici, Italy.
Authors information
FS: Associate Professor of Agronomy and Crop Sciences at University of
Teramo (ITALY). AM: Associate Professor of Agronomy and Crop Sciences at
University Federico II°, Naples (ITALY). AG: Researcher in Agronomy and Crop
Sciences at University of Teramo (ITALY). MP: Full Professor of Agronomy and
Crop Sciences at University of Teramo (ITALY).
Availability of data and materials
Data will not be shared, because they care adapted from other works of
several different authors.
Competing interests
The authors declare that they have no competing interests.
Consent for publication
Each author give his personal consent for publication.
Funding
No funds were received for this work.
Received: 27 September 2016 Accepted: 15 December 2016
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