Sub‐families, number of genera and species, distribution and examples of tree and shrub legumes (adapted from LPWG ).
Climate variability and changes are utmost important primary drivers of biological processes. They are intimately associated with a wide array of abiotic stresses, highlighting the vulnerability of ecosystems and endangering biodiversity. Nitrogen‐fixing trees and shrubs (NFTSs) constitute a unique group of plants for their wide range of applications at the environmental, social and economic levels. In this chapter, we review and analyse the potential of this group of legumes in agroforestry towards sustainable agriculture in Africa. In the first part, the intertwined pillar of sustainable agriculture is brought forward under the context of growing population and climate changes. The second part addresses general aspects of legumes, including botany and the symbiosis with rhizobia. The third part includes the application of NFTS as N‐fertilizers in agroforestry, highlighting the importance of an accurate choice of the crop(s)/NFTS combination(s) and cropping type (intercropping, multistrata or fallows). The implementation of agroforestry systems with NFTS should be supported by fundamental research strategies such as stable isotopes and systems biology and preceded by experimental assays, in order to identify the factors promoting N‐losses and to design appropriate management strategies that synchronize legume‐N availability with the crop demand.
- climate changes
- sustainable agriculture
- shrub legumes
Global agriculture is facing a series of challenges mainly related to growing population, climate changes and loss of biodiversity. Firstly, it is estimated that crop production must increase more than 60% by the year 2050 to fulfil the needs of the world’s population . Secondly, drought and soil salinization are expected to result in losses of up to 50% of arable lands by the middle of this century [1, 2]. Thirdly, the spreading of agriculture to arid and semi‐arid regions under intensive irrigation management will promote secondary soil salinization . Thus, the future of agriculture must rely on the sustainable intensification of crop production to feed the increasingly growing population, as well as on the use of tolerant cultivars that are able to cope with extreme environmental conditions, i.e. low fertility and saline soils, increasing water shortage periods as well as raising air temperatures and CO2 [4, 5].
These challenges will be particularly critical in the developing countries, which have the highest rates of population growth and where most of the farmland is managed by smallholders . It is estimated that in these countries one of five persons still live on less than $1.25 a day . In this context, intensive agriculture based on agro‐chemicals and mechanization is not sustainable and the systems must rely on appropriate cropping and post‐harvest practices, preferably based on local ecosystem‐based resources. Such practices include, for example, the implementation of integrated agroforestry systems, crop‐livestock integration and crop‐aquaculture production, that concomitantly have the potential to promote the conservation and the rational use of biodiversity and other ecosystem services.
According to the Food and Agriculture Organization of the United Nations (FAO), sustainable agriculture lies at the core of the 2030 Agenda . Indeed, 6 of the 17 sustainable development goals (SDGs) concentrate on this issue. These are as follows: (i) SDG 2—
Since 2014, FAO has supported over 80 initiatives in Africa to promote sustainable agricultural production practices . To achieve that, three intertwined pillars are considered essential: (i)
Legume fixing trees and shrubs play a crucial role in biodiversity dynamics. From the ecological point of view, their introduction in cropping systems may contribute to reduce the use of chemical fertilizers and to ecosystems stability.
2. Description and functioning
The Fabaceae or Leguminosae family is the third largest group of flowering plants and the second most important in agriculture . According to recent molecular and morphological studies, Fabaceae is a single monophyletic family [9, 10], comprising more than 18,000 species distributed over ca. 800 genera and six sub‐families (Table 1) : (i) Cercidoideae and (ii) Detarioideae, both comprising mainly tropical species; (iii) Duparquetioideae, a sub‐family from western and central Africa, with only one species identified; (iv) Dialioideae, widespread throughout the tropics; (v) the pantropical Caesalpinioideae, with more than 4000 species (including the former sub‐family Mimosoideae) and (vi) the cosmopolitan and largest legume sub‐family, Faboideae (Papilionoideae), with ca. 14,000 species, mainly herbs and small shrubs.
|Subfamily||Genera (number)||Species (number)||Distribution|
|Cercidoideae||12||ca. 335||Mainly tropical, e.g. |
|Detarioideae||84||ca. 760||Mainly tropical, e.g. |
|Duparquetioideae||1||1||West and Central Africa, |
|Dialioideae||17||ca. 85||Widespread throughout the tropics, e.g. |
|Caesalpinioideae*||148||ca. 4400||Pantropical, e.g. |
|Faboideae (Papilionoideae)||503||ca. 14,000||Cosmopolitan, e.g. |
Varying in habit from annual herbs to large trees, legumes are conspicuous and well represented throughout temperate and tropical regions [9, 12, 13]. The family is particularly diverse in tropical forests and temperate shrub lands with a seasonally dry or arid climate. Such preference for semi‐arid to arid habitats seems to be related to a nitrogen‐demanding metabolism . The vast majority of legume species (ca. 90%) is able to establish symbiosis with nitrogen‐fixing diazotrophic bacteria of the genera
Nitrogen is among the key elements for plant growth and production, being decisive to the adequate plant response to environmental stresses . It is a major component of chlorophyll (photosynthesis), purines and pyrimidines (nucleic acids), amino acids (proteins) and ATP (energy). Although it is one of the most abundant elements in the Earth, its predominant form, i.e. N2 (g), cannot be directly assimilated by the plants, which need reduced forms of this element (NH4+, NO2− and NO3−) [18, 19]. This conversion can be achieved chemically through the Harber‐Bosch process, or biologically through bacterial nitrogen fixation . While chemical nitrogen fixation is cost intensive and 40–50% of the nitrogen applied as fertilizer is lost via denitrification, runoff or leaching, only 10–20% of the biologically fixed nitrogen is lost that way . Besides that, the use of chemical fertilizers has a series of ecological impacts, such as air, soil and water pollution . Thus, there is a strong interest in symbiotic N2 fixation between legumes and rhizobia towards the improvement of agricultural systems, i.e. better productivity with the least ecological impact [23, 24].
In Africa, tree and shrub legumes provide a wealth of goods and services (e.g. wood, food, medicines, energy and housing) to millions of rural and urban dwellers (Table 2 and Figure 1) [25, 26]. The interest on this group of legumes has increased tremendously in the last decades, particularly regarding soil erosion control [27, 28] and farming systems (e.g. windbreaks, shade trees, nitrogen fertilizers, forage, fruits and vegetables) [29, 30, 31, 32].
|Poles, household, agriculture crafts, firewood, charcoal (stem and branches); tannin, ropes (bark); food (pods and seeds); forage (foliage and pods); honey (flowers); gum Arabic (Gum), medicine (various); erosion control; nitrogen fixation; fertilizer; fencing; intercropping [90, 91]||Drier tropical Africa, from Senegal and Mauritania (west) to Eritrea and Ethiopia (north‐east) and South Africa (south); Oman, Pakistan and India ||28.7–46.7 |
less than 20 
|Small articles, firewood (stem and branches); ropes, twine, cloth and fishing nets, tanning, beehives (bark); food for edible larvae (leaves); medicinal (various) [25, 95, 96, 97]||Angola, Botswana, Malawi, Mozambique, Tanzania, Zaire, Zambia, Zimbabwe ||Not available|
|Construction, furniture, household items, firewood, charcoal (stem and branches); tannin, beehives, ropes, sacks (bark); forage (foliage and pods); honey (flowers); medicinal (various); nitrogen fixation, shading [91, 98, 99]||Angola, Kenya, Malawi, Mozambique, Tanzania, Zaire, Zambia, Zimbabwe ||Not available|
|Light construction, baskets, fuel (stems and branches); forage (vegetative parts); honey (flowers); food (seeds and pods); medicinal (various); erosion control; shading, sheltering, nitrogen fixation; fertilizer; intercropping [91, 100]||Unknown origin, probably Indian and African [13, 101]; India ||260 |
|Farm implements, furniture, posts, firewood, charcoal (stem and branches); forage (foliage and pods); honey and food (flowers); medicine and rodenticide (various); erosion control; shading; nitrogen fixation; fertilizer; fencing ||Central America, Caribbean, South America, Asia (Java and Peninsular Malaysia) ||210 |
|Timber, firewood (stems and branches); forage (leaves); food (seeds); similar to gum Arabic (Gum); shading; nitrogen fixation; fertilizer; fencing; intercropping ||Mexico and Guatemala [13, 91]||Not available|
|Building, furniture and handicrafts (stem); fish poison (bark); body anointment (root bark); tannin, dyestuff (Sap); forage (foliage); honey (flowers); medicine (various); erosion control; nitrogen fixation ||Angola, Mozambique, Namibia, South Africa, Swaziland, Tanzania, Zaire, Zambia ||Not available|
|Firewood, charcoal (Stem and branches); tannin, ropes (Bark); forage (leaves and young branches); food (flowers), ropes, fishnets (fiber); gum (seeds and bark); medicine (various); shading; fencing; fertilizer; nitrogen fixation; intercropping ||Africa, Asia, Australia ||84 |
|Firewood (stem and branches); forage and insecticide (leaves); erosion control, shading; land reclamation; nitrogen fixation; fertilizer; fencing; intercropping ||India, SE Asia ||Not available|
|Fish poison, insecticide and molluscicide (leaves); medicine (various); shading; fencing; nitrogen fixation; fertilizer ||Tropical Africa, SE Asia [13, 91]||150 |
3. Importance and role in agroforestry tropical systems
Most tree and shrub legumes are resilient to extreme environments, e.g. erosion, low fertility, salinity, drought, fire and other adverse conditions [33, 34, 35, 36]. Such abilities seem to be innate and enhanced by the symbiosis with N2‐fixing rhizobia [30, 37]. According to Diabate et al.  and Sprent , the use of nitrogen‐fixing tree and shrubs (NFTSs) constitute a promising strategy to recover soil fertility, representing a sustainable agricultural approach to smallholder farmers. This is particularly important in sub‐Saharan Africa where 80% of the farmland is managed by smallholders whose livelihoods depend strongly on the agricultural sector . Most of these households live below the poverty line and therefore cannot afford the use of fertilizers. For example, smallholders from Niger, Namibia and Mozambique use less than 1 kg.N.ha−1.yr−1, i.e., 100 times less than the average fertilizer needs for most crops [1, 34].
The rates of N2 fixation by NFTS depend on the species, climate and soil type, ranging from 0.1 to 700 kg.N.ha−1.yr−1 (Table 2) [33, 39, 40]. Despite the fact that many genera from the subfamilies Mimosoideae and Caesalpinioideae do not always establish root‐nodule symbiosis, under proper environmental conditions, many species nodulate and fix atmospheric N at rates closer to those obtained with the traditional legumes belonging to the Papilionoideae . Additionally there is also evidence that NTFS are also able to increase P availability in the soil, mostly due to mycorrhizal associations .
The use of fertilizer tree legumes (
Another interesting NFTS‐based agroforestry system is the tree cropping system, like those used for coffee production (Figure 2). Such system is very popular in Latin America [48, 49, 50, 51] and less exploited in Africa. In Mexico, the rates of N2 fixation obtained by
4. Towards scientific knowledge
Legume research has been mainly focused on annual grain crops [34, 52, 53, 54]. Instead, a limited amount of knowledge has been produced in perennials. In this section, we will discuss the potential of the two promising strategies to analyse nitrogen mineralization and metabolism in tree legumes, i.e. stable isotopes and, briefly, systems biology.
4.1. Stable isotopes
The use of stable isotopes at natural abundance levels has brought a new dimension to our understanding of plant physiology and ecology. Analyses of the relative natural abundances of stable isotopes of carbon (13C/12C), oxygen (18O/16O), nitrogen (15N/14N) and deuterium (D/H) have been used across a wide range of scales, from cell to community and ecosystem level, contributing much to our understanding of the interactions between biosphere, pedosphere and atmosphere.
In general terms, processes such as diffusion and enzymatic incorporation favour the lighter isotope and lead to depletion of the heavier isotope as compared to source material. Natural abundance of 15N can provide valuable information about N sources used by plants and fluxes of N in the ecosystems [e.g. 55, 56, 57]. There has been some debate on the interrelationship between nitrogen natural abundance (15N/14N) in soils and plants, and the use of a tracer or indicator of fractionation during N‐uptake, assimilation and transport [58, 59]. Indeed, a variety of fractionations may occur during processes related to nitrogen transformation in soils [60, 61] and plants , which may complicate source‐sink relationships. For example, nitrification discriminates against 15N more than N mineralization, which makes NH4+ isotopically heavier than the organic N from which it is derived . Additionally, the δ15N of a particular compound may change and, together with the complexity of the N geochemical cycle, the use of δ15N should be carefully evaluated when applied to natural ecosystems.
However, there are substantial evidence that the natural abundance ratios for 15N/14N in soil and plants are useful integrators of the types and turnover rates of N cycling [62, 63, 64]. These ratios can indicate whether a range of plants have access to the same N source . For instance, differences in leaf δ15N can indicate differences in rooting depth or root characteristics, such as mycorrhizal or N‐fixing root associations [59, 65]. Also, nitrification and plant uptake properties (such as timing and type of uptake) can be determined by the leaf δ15N signatures [66, 67]. Robinson  developed a mixing model to account for contrasting N sources which provided useful insights on the quantification of biological N fixation in tree legumes [68, 69]. Since N2‐fixing species typically have δ15N signatures close to the atmospheric value (0%), which strongly differ from the δ15N signature of non‐fixing species, δ15N can be used as a sensitive tracer of N flow within an ecosystem. This approach was successfully used in the oligotrophic Portuguese primary dunes utilizing foliar δ15N of the non‐leguminous native shrub
4.2. Systems biology
Systems biology is an emerging approach applied to biological scientific research that focuses on the complex interactions within biological systems, frequently associated with the environmental conditions. The best known example is the
In our laboratory, we have recently initiated an integrated approach, combining eco‐physiology and system’s biology to understand the responses of two tree legumes (
5. Concluding remarks
Agriculture has a primordial role to fight poverty and hunger and increase crop resilience to climate changes. The introduction of tree and shrub nitrogen‐fixing trees into cropping systems is the most straightforward approach to reduce the use of chemical fertilizers, improving the soil ecosystem and the livelihoods of smallholder farmers in southern Africa. Additionally, agroforestry may improve ecosystem services such as, soil organic matter, biodiversity and N‐retention. However, it is not devoid of environmental consequences, specifically N‐leaching. Therefore, the implementation of agroforestry systems with NFTS should be preceded by experimental assays, in order to identify the factors promoting N‐losses and design appropriate management strategies that synchronize legume‐N availability with the crop demand.
The authors like to acknowledge Fundação para a Ciência e a Tecnologia through the research units UID/AGR/04129/2013 (LEAF), UID/GEO/04035/2013 (GeoBioTec), CE3C, Fundo para a Investigação Aplicada e Multissectorial. The authors thank Luís Catarino (CE3C), and Mark Stalmans (E.O. Wilson Biodiversity, Lab. Gorongoza National Park) for kindly providing the photographs.