abiotic and biotic constraints, biomass production
potential etc., could be expected; they warrant further
The main 5 features of this plant family in general are
exploration.
summarized as follows:
5. A wide range of phytochemicals (secondary meta-
1. Legumes in the Papilionoideae subfamily and in what
bolites) occur in many species of the Leguminosae.
used to be the Mimosoideae subfamily [now the
These are often referred to as ‘antinutritional factors’
‘mimosoid
clade’
in
the
newly
defined
when legume feeding to livestock is considered
Caesalpinioideae subfamily (LPWG 2017)] and a few
taxa in the Caesalpinioideae subfamily can fix, in
These key features imply that legumes can have a
symbiosis with rhizobia ( Bradyrhizobium, Rhizobium),
significant ecological advantage over other plant families.
atmospheric nitrogen (N). Therefore they have the
However, it is also via this ecological advantage that a
potential to: (1) be N self-sufficient; and (2) increase N
legume can become a weed that threatens biodiversity
availability in the soil for associated or subsequent
and/or agricultural productivity and can also affect
crops, forage grasses and soil biota. Depending on
productivity via soil acidification (see below).
legume species, effectiveness of rhizobium strains,
nutrient supply (mainly phosphorus, potassium and the
trace element molybdenum), climatic conditions and
Tropical forage legumes and natural resources
assessment method applied, published data for
symbiotic N fixation (SNF) by tropical forage legumes
Concern 1. Ecosystem destruction and degradation
cover a wide range, e.g. 15−158 kg N/ha/yr using 15N
methodologies (Thomas 1995); a recent example is the
This concern encompasses both the destruction of natural
range of 123‒280 kg symbiotically fixed N/ha/yr in 6
ecosystems such as forests and the degradation of areas
Arachis glabrata cultivars, reported by Dubeux et al.
that have already undergone land use changes, such as
(2017a). Total input of SNF to mixed grass-legume
unproductive, mismanaged pastures. ‘Prevention is better
pasture systems can range from 98 to 135 kg N/ha/yr
than cure’ – so the initial approach to this problem should
(Boddey et al. 2015). This attribute is particularly
be taking measures to avoid ecosystem destruction and
important in production systems that depend on external
land degradation in the first place. Solving this issue does
N inputs (Douxchamps et al. 2014).
not require development of technology but rather appli-
2. Most forage legumes have high nutritive value for
cation of existing appropriate land use policies and
ruminants, mainly in terms of concentration of crude
strategies.
protein (CP) (percentage N x 6.25) but also of energy
Among them is the SI policy goal of concentrating
(Lüscher et al. 2014). This feature can be particularly
production on existing agricultural land (Garnett et al.
significant in mixtures with, or as complement to,
2013; The Montpellier Panel 2013), thereby lowering the grasses with CP levels often below livestock
colonization pressure on natural ecosystems that should
maintenance requirements or when low-CP and low-
be considered as ecological and biodiversity reserves.
digestibility crop residues are fed.
Intensification, however, is usually closely linked to N
Tropical Grasslands-Forrajes Tropicales (ISSN: 2346-3775)
4 R. Schultze-Kraft, I.M. Rao, M. Peters, R.J. Clements, C. Bai and G. Liu fertilization and its detrimental consequences for the
ovalifolium (‘ D. ovalifolium’) and Arachis pintoi can
environment (nitrate leaching and emission of N2O, a
control erosion, suppress weed growth and provide
potent GHG; see below).
forage. Dubeux et al. (2017b) reviewed the role of tree Forage legumes can contribute to SI by providing N to
legumes and their benefits in warm-climate silvopastoral
the soil-plant system and high quality forage to livestock.
systems and concluded that they were a key component
By this, the productivity of land and livestock can be
for the SI of livestock systems in that climatic zone.
substantially increased in production systems with grass-
Research has shown that, once mismanaged land has
legume pastures and/or legume-only protein banks. In
become unproductive, both herbaceous (Ramesh et al.
Table 1 a number of examples in the tropics are presented.
2005) and woody legumes (Chaer et al. 2011) can be used There is also significant potential to increase overall
successfully for rehabilitation of degraded land, including
land productivity via mixed-production systems such as
degraded cattle ranching land (Murgueitio et al. 2011).
agropastoral systems (Ayarza et al. 2007; Boddey et al.
2015), including intercropping forage legumes (Hassen et
Concern 2. Soil degradation and loss
al. 2017), and (agro) silvopastoral systems (Nair et al.
2008; Dubeux et al. 2015). Multi-purpose legumes serve Soil degradation and loss are intimately linked to the
multiple roles, e.g. Leucaena leucocephala provides
previous concern, ecosystem destruction and degradation.
wood and forage, while Desmodium heterocarpon subsp.
The loss of top soil, where most soil organic carbon
Table 1. Effects of tropical forage legumes on liveweight gain of cattle (extracted from Rao et al. 2015).
Grass
Country/region
Climate/
Legume species
Liveweight gain
Reference
ecosystem
Grass alone
With legume
Native
Australia, Central
Dry subtropics
Stylosanthes
83 kg/an/yr
121 kg/an/yr
( Heteropogon
Queensland
humilis
contortus)
Native
Australia,
Dry tropics
Centrosema
-183 g/an/d
489 g/an/d
Northern Territory
pascuorum 1
Urochloa
Australia,
Dry tropics
Leucaena
381 g/an/d2
723 g/an/d2
mosambicensis Northern
leucocephala cv.
Queensland
Cunningham
L. diversifolia
532 g/an/d2
Brachiaria
Venezuela,
Humid tropics
Desmodium
336 g/an/d
385 g/an/d
humidicola 3
Táchira
ovalifolium 4
Brachiaria
Colombia, Llanos
Subhumid
Pueraria
124 kg/an/yr
174 kg/an/yr
decumbens 5
(savanna)
phaseoloides
Andropogon
Colombia, Llanos
Subhumid
Stylosanthes
120 kg/an/yr
180 kg/an/yr
gayanus
(savanna)
capitata
240 kg/ha/yr
280 kg/ha/yr
Brachiaria
Colombia, Llanos
Subhumid
Centrosema
191 g/an/d6
456 g/an/d6
dictyoneura3
(savanna)
acutifolium cv.
Vichada
Stylosanthes
446 g/an/d6
capitata
Brachiaria
Brazil, Mato
Subhumid
Calopogonium
327 kg/ha/yr
385 kg/ha/yr
decumbens 5
Grosso do Sul
(savanna)
mucunoides
Pennisetum
Brazil, Santa
Humid
Arachis pintoi
716 g/an/d
790 g/an/d
purpureum cv.
Catarina
subtropical
Kurumi
Brachiaria
Costa Rica,
Humid tropics
Arachis pintoi
139 kg/an/yr8
166 kg/an/yr8
brizantha 7
Guápiles
597 kg/ha/yr8
736 kg/ha/yr8
Brachiaria
Mexico, Veracruz
Wet-dry tropics
Cratylia argentea
580 g/an/d
839 g/an/d
brizantha 7
1Supplementation as ley during the main dry season; 2192 grazing days; 3Now classified as Urochloa humidicola; 4Now classified as Desmodium heterocarpon subsp. ovalifolium; 5Now classified as Urochloa decumbens; 6Means of 3 grazing cycles totalling 385 days, newly established pastures; 7Now classified as Urochloa brizantha; 8Mean of 2 stocking rates (low and high).
Tropical Grasslands-Forrajes Tropicales (ISSN: 2346-3775)
Tropical forage legumes and environment 5
(SOC) and plant nutrients are concentrated (Lal 2010),
et al. 2005); or species with physiological mech-
leads not only to loss of a stratum that is crucial for plant
anisms for avoiding and/or tolerating water stress
production but also to oxidation of SOC and subsequent
(annual life cycle, narrow leaflets, leaf move-
liberation of the GHG, CO2. Since this carbon stems from
ments, tolerance of very low leaf water potentials),
recent (= not fossil) photosynthesis, it does not alter the
such as Centrosema pascuorum (Ludlow et al. 1983;
longer-term CO2 balance in the atmosphere. However, it
is lost from a key carbon sink: soil organic matter (SOM).
Reducing sedimentation of water bodies. Sedimentation
Among the multiple possibilities (most of which are
is a major issue with devastating consequences in times
based on legume N contribution, soil-covering growth
of excessive rainfall and is, obviously, intimately linked
habit and deep root system) to contribute to the mitigation
to soil erosion by water. Consequently, the potential role
of this environmental problem, are:
of legumes consists primarily in prevention of soil
Soil conservation by: cover legumes such as
erosion (see above). Additional potential lies in water-
Alysicarpus vaginali s, Arachis pintoi and Desmodium
shed protection through productive, N self-sufficient
‘ovalifolium’ which prevent erosion; contour-hedges
multipurpose trees.
with shrub species such as D. cinereum and Flemingia
Enhancement of water infiltration via the potential
macrophylla; and leguminous trees such as Erythrina
amelioration effect on soil structure of legumes (see
spp. and Leucaena spp.
above).
Rehabilitation of degraded soils by pioneering
Using cover legumes to control weed growth in oil
legumes such as Stylosanthes spp., Macrotyloma
palm and rubber plantations as an attractive alter-
axillare and Flemingia spp., which are deep-rooted
native to the use of herbicides.
and adapted to infertile soils, with soil improvement
Replacing N fertilizer, at least partly, by a legume.
resulting from cycling of minerals from deeper soil
This could reduce nitrate leaching and water eutroph-
layers and enhanced concentration of SOM through
ication as both groundwater contamination by nitrate
litter production (Amézquita et al. 2004; Boddey et al.
leaching and N-eutrophication of water bodies as a
2015). In the case of tannin-rich species, such as
consequence of surface runoff are recognized negative
F. macrophylla, litter has a marked impact as it
consequences of N fertilization in tropical pastures
decomposes slowly (Budelman 1988) and provides a
longer-lasting soil cover and slow nutrient release.
Exploring and exploiting the potential of legumes to
Concern 4. Biodiversity degradation and loss
ameliorate compacted soil, as shown by e.g. Rochester
et al. (2001) for Lablab purpureus (among other, more
Any land use change, such as the establishment of forage
temperate grain legumes) and Lesturguez et al. (2004)
species, has profound implications for biological diversity
for Stylosanthes hamata.
(Alkemade et al. 2013) in terms of plant and animal species
Exploring and exploiting the potential adaptation of
and ecotypes, including entomofauna and the whole soil
species to soil salinity. There seems to be some
biota in the area concerned. This is particularly true if a
potential in a few genera such as Acaciella,
monospecific grass sward is established, as is common in
Desmanthus, Neptunia and Sesbania (Cook et al.
the tropics. While this is an area of considerable knowledge
gaps, we claim that the inclusion of an N-fixing and,
subsequently, SOM-increasing legume in a mixture with
Concern 3. Water degradation and loss
a grass will mitigate the overall negative effects of such a
land-use change on biodiversity, namely entomofauna
On a global scale, water and its decreasing availability,
and soil biota (Ayarza et al. 2007). In their review which
accessibility and quality, are major concerns (Rogers et
focused on temperate conditions, Phelan et al. (2015)
al. 2006). As far as tropical pastures and forages are
reported on positive effects of legumes on the diversity
concerned, we see the role of legumes primarily in the
and abundance of pollinating insects and earthworms.
following areas:
In this context, the possible mitigating effects on
Use of drought-adapted species, e.g. deep-rooted herbs
biodiversity loss of using mixtures of legume species
and subshrubs such as Centrosema brasilianum and
should be explored. Mixtures of herbaceous cover
Stylosanthes guianensis; shrubs and trees such as
legumes are commonly used for weed control in
Cratylia argentea and Leucaena leucocephala (Cook
Southeast Asian tree plantations, e.g. Calopogonium
Tropical Grasslands-Forrajes Tropicales (ISSN: 2346-3775)
6 R. Schultze-Kraft, I.M. Rao, M. Peters, R.J. Clements, C. Bai and G. Liu mucunoides, C. caeruleum, Centrosema pubescens
It has been suggested that increased presence of a grass
(now classified as C. molle), Desmodium ovalifolium
reduces the problem (Scott et al. 2000).
(now classified as Desmodium heterocarpon subsp.
ovalifolium) and Pueraria phaseoloides (Jalani et al.
Tropical forage legumes and climate change
1998). Such mixtures might also improve functional
biodiversity.
Increase in GHG emissions is claimed to be the main
A related area is the role that forage legumes can play
causal agent of climate change (Adger and Brown 1994).
in combating agricultural pests through exudation of
In low-income countries, that is, in the developing world,
chemical compounds. A significant example is the
agriculture and land use changes are estimated to
increasing use of Desmodium intortum and D. uncinatum
contribute 20 and 50%, respectively, to overall GHG
as intercrops to control maize stemborer and Striga spp.
emissions (The World Bank 2010). Climate change is
in the so-called push-pull systems in East Africa (Khan et
expected to: (1) raise temperatures across the planet; and
(2) disturb rainfall patterns, but regional differences will
occur, resulting in increases of both drought-stricken and
Negative aspects of tropical forage legumes
waterlogged areas, and salinization of agricultural soils
(IPCC 2014; Zabel et al. 2014; Brown et al. 2015).
Two negative aspects of tropical forage legumes must be
General strategies to cope with climate change are:
recognized:
adaptation to the modified climatic conditions; and mitigating
Weed potential. The danger that an exotic legume could
GHG emissions that lead to climate change. Both are
become a serious invasive weed that threatens local
examined in relation to tropical forage legumes as follows:
biodiversity and/or affects crop production must be
considered. According to available literature, this risk
Adaptation potential
seems to be a particular concern in Australia, even to the
point that Low (1997) suggested that introduction of
We suggest that research make use of the large organismal
exotic forage germplasm should cease with the focus
(= taxonomic) and genetic diversity of tropical forage
changing to developing cultivars from native species.
legumes that is available in the world’s major germplasm
Among the factors contributing to the weed potential are
collections, e.g. particularly those held by the Australian
(Driscoll et al. 2014): region- or production system-
Pastures Genebank, CIAT (Centro Internacional de
specific lack of grazing or browsing animals;
Agricultura Tropical), Embrapa (Empresa Brasileira de
unpalatability or low palatability to livestock, due to
Pesquisa Agropecuária) and ILRI (International Live-
presence of secondary metabolites; prolific seeding; and
stock Research Institute). Collections can be screened for
presence of thorns and spines. Tropical legume species
adaptation to constraints such as high temperatures and
currently listed among the 32 land plant species of “100
tolerance of drought, waterlogging or soil salinity (Baron
of the world’s worst invasive alien species” (Lowe et al.
and Bélanger 2007). As a result of phenotypic evaluation
2004) include: Acacia mearnsii, Leucaena leucocephala, within the naturally available diversity, promising
Mimosa pigra, Prosopis glandulosa and Pueraria
germplasm can be developed further via selection or
montana var. lobata. It is well recognized that attributes
breeding (Araújo et al. 2015).
which make a legume a useful pasture species are the
In this context, existing legume germplasm collections
same as those which allow it to become potentially a
need to be complemented by further gathering of wild
serious weed.
germplasm in the field. Collecting missions should focus
Even if a legume might not represent a risk to
on areas which experience drought or waterlogging or soil
biodiversity on a larger scale, at the pasture level soil N
salinity problems, i.e. areas where naturally occurring
accumulation following eventual legume dominance
plants can be expected to have the desired adaptations for
could lead to changes in species composition: nitro-
survival and productivity.
philous weeds can become an agroecological problem
Mitigation potential
Soil acidification. Continuous use of legume-only or
legume-dominated swards can result in soil acidification
While a recent overview (Peters et al. 2013) concluded
as Noble et al. (1997) and Liu et al. (1999) reported for that tropical pastures and forages in general have the
Stylosanthes species in Australia and China, respectively.
potential to play a significant role in mitigation of climate
Tropical Grasslands-Forrajes Tropicales (ISSN: 2346-3775)
Tropical forage legumes and environment 7
change, the following discussion refers specifically to the
SOM under legume-only vegetation is less stable than
contribution of forage legumes.
under a grass-legume mixture (Sant-Anna et al. 2017).
Carbon dioxide (CO2). The work of Fisher et al. (1994) in Methane (CH4). Methane has 25 times greater global
the Colombian Llanos showed that sown, deep-rooted
warming potential per unit mass (100-yr time horizon)
tropical grasses can accumulate more SOC than native
than CO2. In agriculture, it is generated mainly by enteric
savanna, in fact, almost as much as under forest. When a
fermentation, manure management and rice cultivation.
legume was mixed with the grass, the amount of C stored
By nature ruminants produce enteric CH4 (Broucek 2014)
in the soil (0−80 cm) increased by 20% to a total of 268 t
and research is underway to determine how this might be
C/ha. Tarré et al. (2001) reported that, in the humid tropics
modified. Options are either to increase the amount of
of Bahia, Brazil, soil C accumulation (0−100 cm soil depth)
meat or milk produced per unit of CH4 emitted or to
in a Brachiaria humidicola (now accepted as Urochloa
decrease the amount of CH4 emitted per unit of feed intake
humidicola) -Desmodium ovalifolium (now accepted as
through: (1) providing high quality forage, mainly in
Desmodium heterocarpon subsp. ovalifolium) pasture over
terms of CP concentration and digestibility; and (2)
a 9-yr period was almost twice that of a B. humidicola
improving livestock breeds that are able to respond to
improved forage quality with increased productivity
pasture (1.17 vs. 0.66 t C/ha/yr). Contributions by non-
tropical permanent pastures and perennial legumes to
In a recent meta-analysis, Lee et al. (2017) showed that
increased C accumulation in the soil are cited in the review
rising temperatures lead to decreased nutritive value of
of Jensen et al. (2012). According to these authors, the grasses and increased CH
organic N provided by the legumes fosters C accumulation.
4 emissions by ruminant
livestock, which worsens the global warming scenario.
As Smith et al. (2008) and Chaer et al. (2011) showed, trees On the other hand, forage legumes have high nutritive
in agroforestry systems, particularly leguminous trees,
value and can contribute to lower emissions of CH4 per
have the potential to increase C accumulation in the soil
unit of livestock product or unit of feed ingested. A study
considerably, as well as accumulating C in their own
by Molina et al. (2016) of methane emissions of Lucerna
biomass, especially on degraded land.
heifers fed a Leucaena leucocephala-stargrass mixture or
On the other hand, respiration by legume roots during
grass only demonstrated the benefits of the legume in the
the energy-consuming SNF process releases substantial
diet in reducing methane emissions per unit gain. The
amounts of CO2 to the atmosphere, even more CO2 per unit
optimal situation is to have improved livestock feeding,
N than is emitted during the production of industrial N
based on high quality forage including legumes, combin-
fertilizer (Jensen et al. 2012). As these authors point out,
ed with improved livestock breeds that can more
however, in contrast to CO2 from fertilizer production, CO2
efficiently use such improved feed.
produced during SNF stems from photosynthesis, so the
In addition to this general quality-based role of forage
atmospheric CO2-concentration balance is not altered.
legumes regarding enteric CH4, another meta-analysis
The particular role of SOM merits further emphasis.
(Jayanegara et al. 2012) showed that polyphenols such as
This is the most important carbon sink and can be larger
condensed tannins, i.e. secondary metabolites that occur
than the above-ground C in a tropical rainforest (Lal
in many tropical forage legumes, decrease CH4 emissions.
2010). If soil erodes, this eventually leads to oxidation of
According to an analysis based on 22 in vivo studies,
C to CO2, which is released to the atmosphere (Olson et
ruminants fed warm-climate legumes produced less CH4
al. 2016). Therefore, perennial plants, e.g. grasses and
per kg OM intake than ruminants fed cold-climate
legumes, which provide soil cover and prevent erosion,
legumes, C3 grasses and C4 grasses (Archimède et al.
play a particularly significant role in mitigating CO2
2011). Low-molecular weight tannins, such as those in
emissions in tropical production systems. To guarantee
L. leucocephala (Molina et al. 2016), can also play a role.
this environmental benefit, vegetation/pasture manage-
It is important to ensure that tannins in the diet do not
ment must be such that there is always adequate soil
reduce protein digestibility, compromising animal intake
cover. Creeping, stoloniferous species such as
and thus its performance, which in turn will affect CH4
Desmodium ‘ovalifolium’ and Arachis pintoi that provide
emissions per unit of livestock product. Working with
a dense soil cover – while supplying N-rich litter – appear
subterranean clover ( Trifolium subterraneum) Kaur et al.
to be of particular interest. It must, however, be
(2017) showed that a plant breeding approach to reduce
mentioned that, because of the low C:N ratio of legumes,
methanogenesis has potential.
Tropical Grasslands-Forrajes Tropicales (ISSN: 2346-3775)
8 R. Schultze-Kraft, I.M. Rao, M. Peters, R.J. Clements, C. Bai and G. Liu Nitrous oxide (N2O). Nitrous oxide has 300 times greater
Legume technology adoption and payment for ecosystem
global warming potential per unit mass (100-yr time
services
horizon) than CO2. Its production by soil microorganisms
during nitrification and denitrification processes is very
In their review paper, which examined the role of forage
much related to the use of N fertilizers in agriculture
legumes in general (though they focused primarily on
(Subbarao et al. 2013). In their meta-analysis, Jensen et
temperate zones), Phelan et al. (2015) reported a low and
al. (2012) concluded that there is a tendency for lower even declining use of forage legumes. We must recognize
N
that in the tropics adoption of legume-based technologies
2O production from soil under legumes than from
systems based on industrial N fertilizer, depending on the
has, in general, been disappointing – in spite of many success
amount of N fertilizer applied. This seems to be an area
stories with tropical forage legumes worldwide (see the 33
of considerable knowledge gaps in relation to tropical
contributions in Tropical Grasslands Vol. 39, No. 4, 2005;
forage legumes.
goo.gl/Qf5VJu). The reasons were analyzed by Shelton et al.
(2005) and include a number of issues that should be taken
In view of the recent detection of biological nitrification
into account when planning R&D programs promoting the
inhibition (BNI) in some tropical forage grasses,
use of tropical forage legumes. A particularly important
particularly Brachiaria (now Urochloa) humidicola
issue is the organization of efficient seed production
(Subbarao et al. 2009; 2017), the challenge is to determine
systems. The lack of seed availability is often cited as a
whether such a mechanism might also exist in tropical
key reason for adoption failure and the resulting vicious
forage legumes. It might then be possible to exploit the
circle (lack of robust demand – lack of interest of the
synergy between SNF and BNI to the benefit of both
private seed production sector – lack of seed production
agriculture and the environment. Due to BNI, symbiotically
and availability – lack of adoption) needs to be broken.
fixed N might be available for longer periods and less prone
Successful results have been achieved with contracting
to loss by nitrate leaching and N2O production.
farmers for forage legume seed production and farmer to
farmer seed sales, e.g. in Thailand, India and Bolivia. For