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  <front>
    <journal-meta />
    <article-meta>
      <title-group>
        <article-title>Legume-Livestock System as a Solution for Sustainable Agriculture: A Review</article-title>
      </title-group>
      <contrib-group>
        <contrib contrib-type="author">
          <string-name>Efstratios Michalis</string-name>
          <email>efstratiosmichalis@gmail.com</email>
          <xref ref-type="aff" rid="aff0">0</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Dimitrios Skordos</string-name>
          <xref ref-type="aff" rid="aff1">1</xref>
        </contrib>
        <contrib contrib-type="author">
          <string-name>Athanasios Ragkos</string-name>
          <email>ragkos@agreri.gr</email>
          <xref ref-type="aff" rid="aff2">2</xref>
        </contrib>
        <aff id="aff0">
          <label>0</label>
          <institution>Agricultural Economics Research Institute, Hellenic Agriculture Organization 'Demeter'</institution>
          ,
          <addr-line>Ilisia, Athens, 11528</addr-line>
          ,
          <country country="GR">Greece</country>
        </aff>
        <aff id="aff1">
          <label>1</label>
          <institution>Agricultural Economics Research Institute, Hellenic Agriculture Organization 'Demeter'</institution>
          ,
          <addr-line>Ilisia, Athens, 11528</addr-line>
          ,
          <country country="GR">Greece</country>
        </aff>
        <aff id="aff2">
          <label>2</label>
          <institution>Agricultural Economics Research Institute, Hellenic Agriculture Organization 'Demeter'</institution>
          ,
          <addr-line>Ilisia, Athens, 11528</addr-line>
          ,
          <country country="GR">Greece</country>
        </aff>
      </contrib-group>
      <fpage>19</fpage>
      <lpage>25</lpage>
      <abstract>
        <p>Legumes constitute one of the most important groups of crop production. They are particularly attractive for livestock production because of their unique ability to fix the atmospheric nitrogen biologically. This review presents the high potential of legume-based systems, by indicating their socioeconomic and environmental benefits for sustainable agriculture and livestock production. Lower chemical nitrogen inputs, efficiency in crop rotation combined with higher yields, increased soil productivity, applicability in mixed farming systems as well as improvement of livestock production are considered as highly significant advantages associated with the cultivation of legumes. Despite these advantages and expectations, their cultivation meets some constraints which limit their potential. Further research and increasing knowledge are required, in order to overcome challenges at the production and market level.</p>
      </abstract>
      <kwd-group>
        <kwd>legumes</kwd>
        <kwd>livestock production</kwd>
        <kwd>sustainability</kwd>
        <kwd>livestock-crop systems</kwd>
        <kwd>circular economy</kwd>
      </kwd-group>
    </article-meta>
  </front>
  <body>
    <sec id="sec-1">
      <title>1 Introduction</title>
      <p>
        Legumes represent the second most important family of crops in economic terms
after Poaceae (grass family), accounting for approximately 27% of the world’s crop
production (Mlyneková, et., al., 2014). The family of legumes (Fabaceae or
Leguminosae) includes several important plants, such as soybean, vetch, pea,
chickpea, lentil, lupine, bean, alfalfa, clover and peanut. They are grown for human
consumption or for animal nutrition, as coarse feed (forage) or seeds for concentrates.
They are also cultivated as green fertilizer plants, as they are included in crop rotation
systems and their residuals are integrated in order to increase soil productivity. The
introduction of legumes in livestock production especially, has been an issue of high
importance during the last two decades, as many researches in Europe have focused
on the potential of legumes to contribute to sustainable and low-cost livestock
production
        <xref ref-type="bibr" rid="ref8">(Rochon, et., al., 2004)</xref>
        .
Τhe pods of legumes are rich in carbohydrates and are known for their high
nutritional value. Indeed, legumes contribute by about one-third to human direct
protein intake worldwide (Mlyneková, et., al., 2014). The benefits from their
consumption are accepted by different societies around the world and have been
associated with longevity in the food cultures of many peoples such as the Japanese,
the Swedes and in the Mediterranean
        <xref ref-type="bibr" rid="ref1">(Darmadi-Blackberry, et., al., 2004)</xref>
        . They
constitute the main protein source in the diet of the population of developing countries,
since proteins of animal origin are scarce and costly in these areas, and they are
sometimes referred to as the “meat” of poor people
        <xref ref-type="bibr" rid="ref6">(Nedumaran, et., al., 2015)</xref>
        .
Legumes are also steadily gaining higher significance in developed countries as well,
as they are included in healthier diets and lifestyles.
      </p>
      <p>
        In Greece, the adoption rate of legumes in farm production remains low. The most
commonly cultivated legumes are chickpeas, lentils, peas and beans. The limited
cultivated areas, in combination with the unavailability of seeds and varieties adapted
to the specific conditions of each region imply deficient production, unable to cover
domestic consumption and livestock needs. This leads to high imports of legumes for
human consumption and soybean for livestock use. In 2017, Greece imported 649008
tons of soybean and soy flour
        <xref ref-type="bibr" rid="ref5">(ELSTAT, 2017)</xref>
        . Producers achieve low yields
combined with high production costs, thus not valorizing the high potential of legumes,
which is mainly associated with the beneficial climate and soil conditions of Greece.
      </p>
      <p>The purpose of this study is to examine the importance of legumes at a
socioeconomic level by investigating their benefits for production systems. In particular,
the review builds around the main issues concerning the production and use of legumes
especially in livestock production as well as the possibilities to create sustainable
legume-livestock systems.
2</p>
    </sec>
    <sec id="sec-2">
      <title>Decrease in Nitrogen Inputs</title>
      <p>The great importance of legumes, in relation to other types of crops, is based on
their ability to fix the atmospheric nitrogen, so that their nitrogen needs can be partially
or completely covered. This happens because of the symbiosis of legumes with
Rhizobium bacteria. Because of this attribute, legumes can be used as a source of
nitrogen in both natural and agricultural ecosystems (Mlyneková, et., al., 2014).</p>
      <p>
        The unique ability of legumes to fix atmospheric nitrogen, implies their ability to
grow satisfactorily in soils with low nitrogen availability. By fixing nitrogen, legumes
could maintain and improve soil fertility, which results in the reduction of expenses
for chemical fertilizers
        <xref ref-type="bibr" rid="ref2">(Kebede, et., al., 2016)</xref>
        . This is really important, considering
that prices of chemical fertilizers are rapidly increasing in recent years and their use
will be limited in the long term
        <xref ref-type="bibr" rid="ref2">(Kebede, et., al., 2016)</xref>
        . Cropping systems with
legumes can reduce nitrogen fertilizer use by 38%, compared to systems without
legumes
        <xref ref-type="bibr" rid="ref7">(Reckling, et., al., 2016)</xref>
        . Substitution of industrial nitrogen fertilizer by
improved use of nitrogen fixed by legumes could be an important contribution to
resource-efficient and environmental-friendly agricultural systems
        <xref ref-type="bibr" rid="ref3">(Luscher, et., al.,
2014)</xref>
        .
      </p>
      <p>The enrichment of soil with nitrogen can be beneficial in cases of crop rotation,
since nitrogen can be used by the next crop installed after legumes. The importance of
using legumes in different types of crop rotation systems has been known since ancient
times in Ancient Greece, Egypt and China.</p>
      <p>
        The inclusion of legumes in a well-planned crop rotation reduces insect, diseases
and pest, improves organic matter levels and soil productivity and increases crop yield
        <xref ref-type="bibr" rid="ref2">(Kebede, et., al., 2016)</xref>
        . The fixed nitrogen leads to higher protein concentration in
soil, which can also be recycled as a form of fertilizer
        <xref ref-type="bibr" rid="ref2">(Kebede, et., al., 2016)</xref>
        . As a
result, subsequent crops do not require the use of chemical fertilizers, which implies
economic and environmental benefits.
      </p>
      <p>
        Except for their advantages in terms of sustainable production, legumes entail yield
benefits in crop rotations. Under standard fertilization levels, cereals yield is on
average 17% higher in legume-based rotation systems than in monocropping
cultivations
        <xref ref-type="bibr" rid="ref10">(Stagnari, et., al., 2017)</xref>
        . Studies have also proven that wheat reports
higher yields grown in rotation after legumes
        <xref ref-type="bibr" rid="ref10">(Stagnari, et., al., 2017)</xref>
        . It should also
be mentioned that yield advantages of legumes depend on the climate conditions of a
specific area, on the amount of fixed nitrogen, as well as on the species
        <xref ref-type="bibr" rid="ref10">(Stagnari, et.,
al., 2017)</xref>
        .
      </p>
    </sec>
    <sec id="sec-3">
      <title>4 Benefits in Livestock Production</title>
      <p>
        The most important advantage of legumes in livestock production is related to the
use of soybean in animal nutrition. Soybean is the only legume whose acreage is
continuously increasing in Europe, reaching 3.45 million ha in 2012, more than all the
other legumes together
        <xref ref-type="bibr" rid="ref9">(Rubiales &amp; Mikic, 2015)</xref>
        . However, the highest percentage of
international soybean production comes from genetic modified plants. As a result, the
European Union and national governments promote the cultivation of other legumes
with subsidies
        <xref ref-type="bibr" rid="ref9">(Rubiales &amp; Mikic, 2015)</xref>
        as an alternative to soybean. In addition,
soybean is only imported in Greece (Table 1) since it is not cultivated in a domestic
level, which implies higher and uncertain production costs for livestock farms. As a
result, the use of legumes to substitute soybean is considered important for countries
like Greece.
      </p>
      <p>Legumes were suggested as a sustainable solution for livestock production many
years ago. It is expected that, by increasing the availability of legumes, livestock farms
will benefit from a cheap and good quality protein source. In Greece, the use of
legumes in livestock production is really important, considering that animal nutrition
with legumes produced on-farm will be able to reduce production costs, as well as the
dependence of farms on imported feedstuff.</p>
      <p>
        There is also evidence that the inclusion of legumes in animal nutrition affects the
quality of produced milk in a positive way. Legume silages and legume-dominated
silages can increase milk production compared to pure grass silages
        <xref ref-type="bibr" rid="ref3">(Luscher, et., al.,
2014)</xref>
        . Rations including legume silages led to high levels of performance of dairy
cows, especially when legumes were of a high nutritive value. Similar results were
reported for beef production
        <xref ref-type="bibr" rid="ref3">(Luscher, et., al., 2014)</xref>
        .
      </p>
    </sec>
    <sec id="sec-4">
      <title>5 Legumes in Mixed Farming Systems and Circular Economy</title>
      <p>
        The use of legumes in mixed farming systems is another significant factor
associated with the advantages of legumes at the socio-economic level, as they can be
used as forage in animal nutrition. Legumes species also represent excellent sources
of green manure in sustainable agriculture and organic farming
        <xref ref-type="bibr" rid="ref2">(Kebede, et., al., 2016)</xref>
        .
The contribution of legumes in mixed farming systems is recognized, since production
costs can be reduced by using lower amount of coarse feed. This also implies that these
systems pertain to circular economy principles, since they can operate as economic
systems aimed at eliminating waste, via the circular use of their resources, forage and
manure.
      </p>
      <p>
        Indeed, mixed farming systems involve complementary interactions between crops
and livestock, which means that legumes can be a basic component because of their
unique characteristics. The use of manure for cropping as well as the use of crop
residuals for livestock constitutes important interactions between livestock-crop
systems
        <xref ref-type="bibr" rid="ref2">(Kebede, et., al., 2016)</xref>
        . The uncertainty of agricultural activities can also be
reduced through mixed farming systems because of internalizing part of the input
requirements of farms due to the combination of livestock and crop enterprises
        <xref ref-type="bibr" rid="ref2">(Kebede, et., al., 2016)</xref>
        .
      </p>
      <p>
        In general, the integration of the forage legumes instead of grass could contribute a
more preferable option for livestock-crop systems. The possibility of nitrogen fixation,
the continuity of feed supply, the increased crop productivity, the high coarse feed
quality and the use of manure as fertilizer can secure a sustainable production
        <xref ref-type="bibr" rid="ref2">(Kebede,
et., al., 2016)</xref>
        .
      </p>
    </sec>
    <sec id="sec-5">
      <title>6 Challenges and Limitations</title>
      <p>
        Legumes suffer from some limitations, which implies the need for further research
in order to fully develop the opportunities they offer
        <xref ref-type="bibr" rid="ref3">(Luscher, et., al., 2014)</xref>
        . Besides
the growing trends observed between 197
        <xref ref-type="bibr" rid="ref4">4 and 2014</xref>
        , the cultivated areas of species
such as pea, bean and lupine have declined worldwide
        <xref ref-type="bibr" rid="ref10">(Stagnari, et., al., 2017)</xref>
        . The
average yield increase for most legumes was about 50%, which is still below the
increases achieved by major cereal crops, which ranged between 130 to 160%
        <xref ref-type="bibr" rid="ref9">(Rubiales &amp; Mikic, 2015)</xref>
        . Poor spring growth, unavailability of seeds, limited
farmers’ knowledge on the appropriate use of the fixed nitrogen and management of
legumes in a whole cropping system, as well as animal health issues are the main
reasons of concern about the viability of legume-based systems.
      </p>
      <p>
        There are also limitations regarding their adoption by mixed farming systems.
Nutrient management in livestock-crop systems remains a challenge, especially
regarding nitrogen losses in managing manure
        <xref ref-type="bibr" rid="ref7">(Reckling, et., al., 2016)</xref>
        . The adoption
of forage legumes is also restricted in some farms in many European countries
        <xref ref-type="bibr" rid="ref7">(Reckling, et., al., 2016)</xref>
        .
      </p>
      <p>
        Market constraints are also of high significance. Although the global market is very
well developed for soybean, supply chains and markets in general are inadequately
prepared for the majority of legumes crops
        <xref ref-type="bibr" rid="ref10">(Stagnari, et., al., 2017)</xref>
        . There is also
evidence that immediate profits are not delivered to producers from the introduction
of legumes into a farming system because of the high diversification of legumes
production trends around the world
        <xref ref-type="bibr" rid="ref10">(Stagnari, et., al., 2017)</xref>
        . This is the main reason
why there is a high preference for cereals from farmers in Europe and they will need
to be more convinced by future research that the cultivation of legumes has profitable
potential. Low prices and few marketing channels affect legumes’ commercialization
in a negative way. Prices are currently lower than the actual feed value, which means
that legumes produced in European countries have difficulties in the competition with
other protein crops of the world market
        <xref ref-type="bibr" rid="ref7">(Reckling, et., al., 2016)</xref>
        . Undoubtedly, there
are still a lot of challenges and constraints that need to be overcome for legumes to
increase their reliability in production systems and their competitiveness in global
markets.
      </p>
    </sec>
    <sec id="sec-6">
      <title>7 Conclusions</title>
      <p>
        The advantages of legumes are numerous and should become even more significant
in the following years. The opportunities emerging from legume-based systems are
important in socio-economic terms and environmental perspective. Due to their unique
characteristics, they can secure more rational use of chemical fertilizers, increase in
soil productivity, efficiency in crop rotations and benefits in livestock production.
Their introduction in mixed farming systems has a high potential as well. However,
legumes are still not competitive and widespread. In order to overcome possible
constraints and limitations, their positive effects need to be communicated to advisors
and farmers, and regional supply chains need to be developed in food markets
        <xref ref-type="bibr" rid="ref7">(Reckling, et., al., 2016)</xref>
        . Further research is required to increase attractiveness and
confidence for producers. There is also a need for research on how to integrate them
in mixed farming systems. Agronomic knowledge is required and has to be more
widely available. Finally, agricultural policy measures have to be introduced and
implemented specifically for legume-based systems, so that their economic and
ecological benefits can be valorized.
      </p>
      <p>Acknowledgement. This research has been co-financed by the European Union and
Greek national funds through the Operational Program Competitiveness,
Entrepreneurship and Innovation, under the call RESEARCH – CREATE –
INNOVATE (project ‘Legumes4Protein’, Code:T1EDK-04448)».</p>
    </sec>
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