Key attributes of legumes

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

(Kumar and D´Mello 1995).

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

Shaw and

( Heteropogon

Queensland

humilis

Mannetje

contortus)

(1970)

Native

Australia,

Dry tropics

Centrosema

-183 g/an/d

489 g/an/d

McCown et al.

Northern Territory

pascuorum 1

(1986)

Urochloa

Australia,

Dry tropics

Leucaena

381 g/an/d2

723 g/an/d2

Jones et al.

mosambicensis Northern

leucocephala cv.

(1998)

Queensland

Cunningham

L. diversifolia

532 g/an/d2

Brachiaria

Venezuela,

Humid tropics

Desmodium

336 g/an/d

385 g/an/d

Chacón et al.

humidicola 3

Táchira

ovalifolium 4

(2005)

Brachiaria

Colombia, Llanos

Subhumid

Pueraria

124 kg/an/yr

174 kg/an/yr

Lascano and

decumbens 5

(savanna)

phaseoloides

Estrada (1989)

Andropogon

Colombia, Llanos

Subhumid

Stylosanthes

120 kg/an/yr

180 kg/an/yr

CIAT (1990)

gayanus

(savanna)

capitata

240 kg/ha/yr

280 kg/ha/yr

Brachiaria

Colombia, Llanos

Subhumid

Centrosema

191 g/an/d6

456 g/an/d6

Thomas and

dictyoneura3

(savanna)

acutifolium cv.

Lascano (1995)

Vichada

Stylosanthes

446 g/an/d6

capitata

Brachiaria

Brazil, Mato

Subhumid

Calopogonium

327 kg/ha/yr

385 kg/ha/yr

CNPGC (1988)

decumbens 5

Grosso do Sul

(savanna)

mucunoides

Pennisetum

Brazil, Santa

Humid

Arachis pintoi

716 g/an/d

790 g/an/d

Crestani et al.

purpureum cv.

Catarina

subtropical

(2013)

Kurumi

Brachiaria

Costa Rica,

Humid tropics

Arachis pintoi

139 kg/an/yr8

166 kg/an/yr8

Hernández et al.

brizantha 7

Guápiles

597 kg/ha/yr8

736 kg/ha/yr8

(1995)

Brachiaria

Mexico, Veracruz

Wet-dry tropics

Cratylia argentea

580 g/an/d

839 g/an/d

González-Arcia

brizantha 7

et al. (2012)

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

Clements 1990).

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

(Vendramini et al. 2007).

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

2005).

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

al. 2010; icipe 2015).

(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

(McIvor et al. 1996).

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-

(Gerber et al. 2013).

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