Scholarly article on topic 'Agronomic biofortification of crops to fight hidden hunger in sub-Saharan Africa'

Agronomic biofortification of crops to fight hidden hunger in sub-Saharan Africa Academic research paper on "Agriculture, forestry, and fisheries"

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Abstract of research paper on Agriculture, forestry, and fisheries, author of scientific article — A.W. de Valença, A. Bake, I.D. Brouwer, K.E. Giller

Abstract Micronutrient deficiencies or ‘hidden hunger’ resulting from unbalanced diets based on starchy staple crops are prevalent among the population of sub-Saharan Africa. This review discusses the effectiveness of agronomic biofortification - the application of mineral micronutrient fertilizers to soils or plant leaves to increase micronutrient contents in edible parts of crops – and it's potential to fight hidden hunger. There is evidence that agronomic biofortification can increase yields and the nutritional quality of staple crops, but there is a lack of direct evidence that this leads to improved human health. Micronutrient fertilization is most effective in combination with NPK, organic fertilizers and improved crop varieties, highlighting the importance of integrated soil fertility management. Agronomic biofortification provides an immediate and effective route to enhancing micronutrient concentrations in edible crop products, although genetic biofortification may be more cost effective in the long run.

Academic research paper on topic "Agronomic biofortification of crops to fight hidden hunger in sub-Saharan Africa"

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Global Food Security

journal homepage: www.elsevier.com/locate/gfs

Agronomic biofortification of crops to fight hidden hunger in sub-Saharan ■. Africa

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A.W. de Valengaa, A. Bakeb, I.D. Brouwerb, K.E. Giller3'*

a Plant Production Systems, Wageningen University, PO Box 430, Wageningen, The Netherlands b Human Nutrition and Health, Wageningen University, PO Box 8129, Wageningen, The Netherlands

ARTICLE INFO

Keywords:

Micronutrient deficiency Foliar fertilization Sub-Saharan Africa Soil fertility Plant nutrition Human nutrition

ABSTRACT

Micronutrient deficiencies or 'hidden hunger' resulting from unbalanced diets based on starchy staple crops are prevalent among the population of sub-Saharan Africa. This review discusses the effectiveness of agronomic biofortification - the application of mineral micronutrient fertilizers to soils or plant leaves to increase micronutrient contents in edible parts of crops - and it's potential to fight hidden hunger. There is evidence that agronomic biofortification can increase yields and the nutritional quality of staple crops, but there is a lack of direct evidence that this leads to improved human health. Micronutrient fertilization is most effective in combination with NPK, organic fertilizers and improved crop varieties, highlighting the importance of integrated soil fertility management. Agronomic biofortification provides an immediate and effective route to enhancing micronutrient concentrations in edible crop products, although genetic biofortification may be more cost effective in the long run.

1. Introduction

Hidden hunger or micronutrient deficiency retards the growth and

development of both crops and humans. Soil micronutrient deficiencies limit crop productivity and nutritional quality of foods, which together

affect nutrition and human health (Sanchez and Swaminathan, 2005). Many soils in sub-Saharan Africa are affected by multiple nutrient deficiencies including the macronutrients N, P, K, secondary nutrients

S, Ca and Mg, as well as the micronutrients Zn, Fe, Cu, Mn, Mo and B (Vanlauwe et al., 2015). Soil micronutrient deficiencies are thought to be severe in sub-Saharan Africa, where 75% of the total arable land has serious soil fertility problems (Toenniessen et al., 2008). Insufficient micronutrient availability in soils in these regions not only causes low crop productivity, but also poor nutritional quality of the crops and consequently contributes to malnutrition in the human population (Nube and Voortman, 2011; Hurst et al., 2013; Kumssa et al., 2015). Diets in sub-Saharan Africa (especially among resource poor households) are often low in diversity and dominated by staple crops such as maize, rice, cassava, sorghum, millet, banana and sweet potato. Such diets are poor in micronutrients (minerals and vitamins) and consequently micronutrient deficiencies are widespread (FAO, 2015). The chronic lack of micronutrients can cause severe but often invisible

health problems, especially among women and young children (Black et al., 2013): hence 'hidden hunger'.

Worldwide over 2 billion people suffer from iron (Fe), zinc (Zn) and/or other (multiple) micronutrient deficiencies (WHO, 2016; Black, 2003). The problem is most severe in low- and middle income countries, especially in Africa where the estimated risk for micronu-trient deficiencies is high for Ca (54% of the continental population), Zn (40%), Se (28%), I (19%) and Fe (5%) (Joy et al., 2014). In sub-Saharan Africa, micronutrient deficiencies are responsible of 1.5-12% of the total Disability Adjusted Life Years (DALYs)1 (Muthayya et al., 2013). Alarming numbers concern iron deficiency anaemia, which affects more than half of the female population in countries such as DR Congo, Ghana, Mali, Senegal, Togo (IFPRI, 2015). Many people suffer from multiple micronutrient deficiencies (Muthayya et al., 2013); for example in Malawi > 50% of the households are estimated to be at risk of Ca, Zn and/or Se deficiencies (Joy et al., 2015a). Selenium is not essential for plant growth, but contributes to the human diet through uptake by crops from the soil. Even mild to moderate deficiencies of micronutrients can lead to severe human health problems, generally related to sub-optimal metabolic functioning, decreased immunity and consequently increased susceptibility to infections, growth failure, cognitive impairment and, finally, reduced productivity (Tulchinsky,

* Corresponding author.

1 DALYs are the sum of Years of Life Lost (YLL) and Years Lived with Disabilities (YLD) for people living with a disease or consequential health condition. One DALY can be thought of as one lost year of 'healthy' life. The sum of these DALYs across the population, or the burden of disease, can be thought as a measurement of the gap between current health status and an ideal health situation where the entire population lives to an advanced age, free of disease and disability (www.who.int/healthinfo/global burden disease/metrics daly/).

http://dx.doi.org/10.1016/j.gfs.2016.12.001

Received 10 June 2016; Received in revised form 6 December 2016; Accepted 8 December 2016 2211-9124/ © 2016 The Authors. Published by Elsevier B.V.

This is an open access article under the CC BY-NC-ND license (http://creativecommons.Org/licenses/BY-NC-ND/4.0/).

Fig. 1. Agronomic biofortification is the application of micronutrient-containing mineral fertilizer (blue circles) to the soil and/or plant leaves (foliar), to increase micronutrient contents of the edible part of food crops. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

2010).

Hidden hunger can be alleviated by direct (nutrition-specific) and indirect (nutrition-sensitive) interventions (Ruel et al., 2013). Direct interventions focus on consumption behaviour and include dietary diversification, micronutrient supplementation, modification of food choices and fortification. Nutrition-sensitive interventions address the underlying determinants of malnutrition and include biofortification. Biofortification is the process of increasing the content and/or bioa-vailability of essential nutrients in crops during plant growth through genetic and agronomic pathways (Bouis et al., 2011). Genetic biofortification involves either genetic engineering or classical breeding (Saltzman et al., 2013). Agronomic biofortification is achieved through micronutrient fertilizer application to the soil and/or foliar application directly to the leaves of the crop (Fig. 1). Biofortification is mainly focused on starchy staple crops (rice, wheat, maize, sorghum, millet, sweet potato and legumes), because they dominate diets worldwide -especially among groups vulnerable to micronutrient deficiencies - and provide a feasible means of reaching malnourished populations with limited access to diverse diets, supplements, and commercially fortified foods (Saltzman et al., 2013).

We review evidence on the effectiveness of agronomic biofortification and its potential to alleviate hidden hunger in sub-Saharan Africa. First we discuss some technical aspects of agronomic biofortification concerning micronutrient bioavailability pathways and micronutrient fertilization approaches. We then address the questions: (1) what is the impact of agronomic biofortification on a) yields and nutritional quality of crops, b) nutrition and human health status, c) the environment, and 2) how effective is agronomic biofortification compared with other interventions? We focus on agronomic biofortification with Zn, Se and Fe, as these micronutrients are considered to be the most appropriate for the technique and are highly important for human health (Cakmak,

Fig. 2. Schematic overview of micronutrient (MN) pathway from soil to humans and the factors that influence MN bioavailability to the next level. Based on Mayer et al. (2011).

2014; Welch and Graham, 1999). We conclude with an analysis of the potentials and constraints for implementation of agronomic biofortification in sub-Saharan Africa).

2. Micronutrient bioavailability

Micronutrients follow a path from the soil through the crop and food into the human body. Several critical factors determine the success of agronomic biofortification to alleviate micronutrient deficiencies among humans. These factors depend on nutrient bioavail-ability at different stages: the presence and bioavailability of soil nutrients for plant uptake (soil to crop), nutrient allocation within the plant and re-translocation into the harvested food (crop to food), bioavailability of nutrients in prepared food for humans and the physiological state of the human body which determines the ability to absorb and utilize the nutrients (food to human) ( Fig. 2).

2.1. Soil to crop

Bioavailability of micronutrients from soil to crop is influenced by many soil factors (i.e. pH, organic matter content, soil aeration and moisture and interactions with other elements) and by the crop variety that, for example, defines the structure and functioning of rooting systems (Alloway, 2009). Some plants can modify the rhizosphere by the excretion of H+ ions or organic acids that enhance micronutrient availability and uptake (Zhang et al., 2010; Marschner, 2012). Interactions between elements influence the bioavailability for root uptake. Soil phosphorus, for example, can either stimulate root growth and Zn uptake while at the same application of P fertilizer can precipitate already small concentrations of Zn and trigger Zn deficiency (Zingore et al., 2008). Addition of P also appears to induce Zn deficiency through dilution effects and interference with Zn translocation from the roots (Singh et al., 1988). Soil management with lime or organic manures can alter soil properties such as pH and stimulate micronutrient bioavailability and crop uptake. Symbioses with arbuscular mycorrhizal fungi (a fungal network acting as an extension of the root system and increasing the volume of soil explored for nutrient uptake) can increase uptake of nutrients that are sparingly soluble in soil, such as P and Zn (Smith and Read, 1997).

2.2. Crop to food

Bioavailability from crop to food is influenced by the crop (variety) - which defines whether micronutrients are (re-)localized into edible parts of the crop - and by food processing. In rice, Zn and Fe are localized in protein bodies in the outer layer of the grains, which is often removed during processing (dehusking, milling) leaving less Zn and Fe in the consumed rice (Haas et al., 2005; Zimmermann and Hurrell, 2007). Rice parboiling is an effective method to increase nutrient contents especially when micronutrients are added to the soak water during the parboiling, as the process drives nutrients from the bran and germ layer to the endosperm (Prakash et al., 2016; Hotz et al., 2015). Other crops like wheat allocate Zn in the consumed part of the grain (endosperm) that remains even after removal of the seed coat and aleurone layer during the process of bread making (Ajiboye et al.,

2015). Also Se, Fe, Mn and Cu are hardly lost during wheat grain milling and bread production (Lyons et al., 2005) - making wheat more suitable for agronomic biofortification. Food processing generally results in nutrient loss, but it also often reduces the amounts of antinutrients and thus may increase the bioavailability of micronu-trients. For example soaking of cereals in water can reduce the presence of the antinutrient phytate, enhancing the bioavailability of Fe, Zn and Ca (Hotz and Gibson, 2007). Contrary to 'usual cooking practices' like cooking and canning causing negligible losses of Se, grilling, frying, dry heating and boiling do cause loss of Se. In addition to tailored food processing techniques, the main technique to ensure that targeted micronutrients end up in the food being consumed, is breeding for crop varieties that allocate micronutrients in the edible part of the crop (genetic biofortification).

2.3. Food to human

Bioavailability of micronutrients in the food for the human body is influenced by many factors that can be either food or host related (Gibson, 2007). Dietary intake is an essential factor, as micronutrient bioavailability depends on the chemical form and amount consumed, the nature of the dietary matrix, as well as interaction between nutrients and/or food components that enhance or inhibit absorption in the gastrointestinal tract (Sandstrdm, 2001). Enhancers like ascorbic acid (available in fruits and vegetables) can increase Fe bioavailability, while polyphenols and especially phytate or phytic acid (with high concentrations in staple grains like wheat) are major inhibitors that form complexes with Fe and Zn and limit uptake in the human body (Clemens, 2014). An individual's health and nutrient status as well as age, sex, ethnicity, genotype, and physiological state also impacts micronutrient bioavailability from foods for uptake into the human body (Gibson, 2007). Absorption of micronutrients is often tightly regulated by the micronutrient status of the individual; for example Fe and Zn absorption is increased when individuals have Fe or Zn deficiency (Hallberg, 2001). Infections and parasites impair micronu-trient absorption and increase the risk for malnutrition, while malnutrition itself also makes a person more susceptible for infections and parasites (Katona and Katona-Apte, 2008). These interactions may cause a vicious downward cycle for individuals with a poor health status.

In summary, micronutrient bioavailability at various stages from soil availability and plant uptake to human digestion determines the potential of agronomic biofortification. Even though metabolisms and interactions vary largely among nutrients, soils, crop (varieties) and human beings, generally we can say that there are many steps at which potential losses of micronutrients occur. All of these steps must be considered when assessing the effectiveness of agronomic biofortification and its potential to alleviate hidden hunger, as explored below.

3. Fertilization approaches and agronomic biofortification

The soils of sub-Saharan Africa are highly diverse, ranging from some of the oldest soils in the world to relatively young volcanic soils in the Great Rift Valley that splits East and Southern Africa and alluvial soils along rivers. Many African soils suffer from multiple micronu-trient deficiencies, due both to their inherent soil properties and to continuous cropping without nutrient replenishment. Current fertilization programmes in African countries, primarily focus on NPK fertilizers, but many soils are non-responsive to NPK due to (multiple) micronutrient deficiencies. Soil amendment with small amounts of (multiple) micronutrients has been suggested as a sustainable strategy to increase yields and nutritional quality of crops (Vanlauwe et al., 2015; Voortman and Bindraban, 2015; Manzeke et al., 2012). In the succeeding paragraphs we discuss the impact of different fertilization approaches on agronomic biofortification, as well as the interactions of micronutrients with NPK fertilizers and the importance of Integrated

Soil Fertility Management (ISFM).

3.1. Impact of different fertilization techniques

Effectiveness of mineral fertilizer application on crop performance is influenced by the fertilizer type and application method. The fertilizer formulation largely determines the micronutrient bioavailability, as the form of the nutrients and interactions between them can have positive as well as neutral or even negative effects on yields and nutrient use efficiencies (Rietra et al., 2015). Foliar fertilization with micronutrients often stimulates more nutrient uptake and efficient allocation in the edible plant parts than soil fertilization, especially with cereals and leafy vegetables (Lawson et al., 2015). The combination of soil and foliar application is often the most effective method (Phattarakul et al., 2012; Cakmak, 2010). Foliar pathways are generally more effective in ensuring uptake into the plant because immobilization in the soil is avoided. The downside of foliar application is that fertilizers can easily be washed off by rain and are more costly and difficult to apply (Garcia-Banuelos et al., 2014). Seed priming and seed coating with fertilizers are other strategies for precise micronutrient application, that can stimulate plant development and increase yields, but increased nutritional values of grains are rarely found (Duffner et al., 2014).

3.2. Impact in combination with NPK fertilization

Interactions of micronutrients with macronutrients can influence the effectiveness of agronomic biofortification. Good N and P status of plants has a positive effect on root development, shoot transport and re-localization of nutrients from vegetative tissue to the seeds (Prasad et al., 2014). This results in increased micronutrient uptake and concentrations in the edible parts of the crop, as shown in wheat experiments, where high N application increased Zn and Fe concentrations in the grain endosperm (the edible part of the grain) (Kutman et al., 2011; Shi et al., 2010). Wheat fertilization with Zn-enriched N and P fertilizer has also been effective to increase wheat grain yields (Cakmak, 2004). Rao et al. (2012) observed that nutrient uptake (N, P, Zn, B, S) and productivity of sorghum and finger millet were increased significantly by fertilization with blends of mineral NPK plus Zn, B and S. On the other hand, P fertilization can also decrease micronutrient concentrations due to a dilution effect when plants grow prolifically (Singh et al., 1988). As indicated above, addition of P fertilization can also reveal incipient Zn deficiency by precipitation of insoluble Zn phosphate (Zingore et al., 2008). Proper N and P management is important for the (increased) effectiveness of micronutrient fertilization and indicates the importance of a more integrated soil fertility management approach, as explained further below.

3.3. Impact of integrated soil fertility management

Good soil conditions that enhance micronutrient availability for crop uptake are essential for the success of agronomic biofortification. Not only N and P increase the effectiveness of micronutrient fertilization, but also other soil chemical, physical and biological characteristics are essential to optimize nutrient use efficiency. A commonly suggested strategy to optimize soil conditions is Integrated Soil Fertility Management which is defined as "a set of soil fertility management practices that necessarily include the use of mineral fertilizer, organic inputs and improved germplasm" (Vanlauwe et al., 2010). The combination of mineral fertilizers and organic inputs is beneficial, because they have complementary functions and enhance mutual effectiveness. Organic resources (plant residues and animal manure) help to sustain soil organic matter with multiple benefits in terms of enhanced soil structure, cation exchange capacity and water holding capacity (van Noordwijk et al., 1997). Furthermore, where organic inputs provide more slow but constant nutrient release, mineral

fertilizers offer flexibility in the proper timing, placing and application rate to synchronize nutrient availability with crop demand (Giller, 2002). Fertilization with organic matter alone has the potential to increase soil micronutrient content and availability (Thilakarathna and Raizada, 2015; Traore, 2006). Animal manures, for example, are a good source of many micronutrients (Zingore et al., 2008; Manzeke et al., 2012). Manzeke et al. (2014) found that Integrated Soil Fertility Management approaches where Zn-enriched fertilizer was applied together with cattle manure and forest leaf litter gave larger increases in maize grain yield and Zn concentration in the grain. Long-term application of organic matter to the soil not only increases total Zn content of the soil but also the proportion of labile Zn, which is the readily available form for plant uptake (Santos et al., 2010; Manzeke et al., 2014). However, organic inputs alone are often insufficient to maintain nutrient balances in resource poor farming systems, because of the limited availability of nutrient-rich organic matter (e.g., manures and compost) and overall lack of nutrients in the system. The combined application of organic inputs and mineral micronutrient fertilizers has the potential to alleviate overall micronutrient shortage. Besides, agronomic efficiency of mineral fertilizers is often increased when applied in combination with organic matter (Vanlauwe et al., 2015). Green manures (cover crops that serve as mulch or soil amendment) are also effective to enhance nutrient bioavailability, as was shown in a study on basmati rice in India, where the combined fertilization with green manure and mineral Zn improved yields and grain Zn nutritional quality (Pooniya and Shivay, 2013). The combination of mineral and organic fertilizers with improved germplasm enhances optimal nutrient use efficiency, when the variety is selected for characteristics of improved nutrient uptake and localization in the consumed parts of the crop.

4. Impact of agronomic biofortification with Se, Zn and Fe on yields and nutritional quality of crops

Agronomic biofortification has so far been most effective with Zn and Se (Cakmak, 2014). Several studies have shown that application of Se-enriched fertilizers can increase grain Se concentrations (in maize and wheat), although yield increases were not observed. One of the most celebrated cases is from Finland, where the nationwide addition of Se to NPK fertilizers (15 mg Se/kg) increased cereal crop Se contents by 15-fold on average. This intervention increased the Se intake of the population to well above nutrition recommendations (Alfthan et al., 2015). Another experiment on wheat in Australia with the application of Se (4-120 g Se/ha) increased grain Se concentrations progressively up to 133-fold when applied to the soil and up to 20-fold when applied as foliar spray. Other authors observed linear relationships between Se fertilization and maize grain Se concentrations (Chilimba et al., 2012) as well as bioavailable Se in wheat flour and bread (Hart et al., 2011).

Most current research and development programmes focus on Zn, as this is a widespread crop yield-limiting factor and one of the most prevalent deficiencies in humans. Evidence is accumulating that Zn fertilization can increase both yields and nutritional quality of crops. Most research has been done in Turkey, where Zn fertilization of various cereals (maize, sorghum, barley, wheat) and dicotyledonous (soybean, safflower, pea, common bean, canola, common vetch) crops showed increased yields and grain Zn concentrations (Cakmak et al., 2010). Yilmaz et al. (1997) observed a threefold increase in wheat yields and wheat grain Zn concentrations, after both soil and foliar Zn application. Field studies in India showed that the use of Zn-enriched urea on rice could increase yields and grain Zn concentrations threefold (Cakmak, 2009). A review of experiments from ten African countries on the impact of Zn-enriched fertilizers showed that soil Zn application increased the Zn concentration in maize, rice and wheat grains by respectively 23%, 7% and 19% and by 30%, 25% and 63% through foliar application (Joy et al., 2015b). Teff yields in Ethiopia increased with Zn fertilization (Haileselassie et al., 2011). Besides the

increased yields and grain Zn concentrations upon Zn-enriched fertilizer application to cereals, another agronomic benefit is that seedlings from seeds with high Zn concentration have better growth performance and resilience against environmental stress, so positive impacts on productivity may be seen in the next cropping generation. Furthermore, Zn fertilization reduces P uptake and the accumulation of phytate in grains, which may increase the Zn bioavailability for humans (Hussain et al., 2013).

Iron is the third most studied element, but soil application of Fe-enriched fertilizers is more difficult than with Zn and Se, because Fe is precipitated in insoluble forms in the soil which cannot be absorbed by plants. For example, a greenhouse experiment that compared Zn and Fe application on wheat showed enhanced grain Zn concentrations, while Fe concentrations were not effectively improved (Cakmak et al., 2010). The most effective agronomic practices for the Fe enrichment of crops are through litter fertilization or foliar application of mineral Fe. Foliar application has already showed to increase Fe concentrations in wheat grain and rice grain (Shahzad et al., 2014). However, some studies also showed no response of plants upon foliar Fe application, especially under treatment with inorganic and chelated Fe fertilizers (Garcia-Banuelos et al., 2014).

5. Impact of agronomic biofortification on nutrition and human health status

The only known case that clearly showed a direct effect of agronomic biofortification on human micronutrient status comes from Finland, where nationwide agronomic Se biofortification was practiced since 1985 (Alfthan et al., 2015). This programme resulted in significantly increased cereal grain Se concentrations, which in turn led to increased human and animal Se intake and significantly decreased Se deficiencies among the population. The average dietary intake doubled from 0.04 mg Se/day/10 MJ in 1985 to 0.08 mg Se/ day/10 MJ in 2014, which is above nutrition recommendations leading to an average human plasma Se concentration of 1.4 ^mol/L and reflecting an optimal Se status (Alfthan et al., 2015). This long-term intervention showed that Se (sodium selenate) supplementation of fertilizers was a safe and effective method to increase Se intake of humans as well as animals. Interestingly, foods of animal origin accounted for over 70% of the human daily Se intake, indicating that interventions in sub-Saharan Africa would require dietary changes next to agronomic Se biofortification in order to achieve similar results as in Finland.

We are unaware of other studies that similarly quantified the direct impact of agronomic biofortification on dietary intake of micronutri-ents on human health. Even though it is shown that agronomic biofortification has the potential to increase micronutrient contents in crops, literature connecting these enhanced concentrations to micronutrient bioavailability, dietary intake and human health are scarce (Joy et al., 2014). Such studies do exist on genetically bioforti-fied crops, such as in the case of the increased Fe status of Filipino women who consumed Fe-biofortified rice (Haas et al., 2005), of Rwandan iron-repleted university women consuming iron biofortified beans (Haas et al., 2016) and of Indian schoolchildren consuming iron biofortified pearl millet (Finkelstein et al., 2015).

Modelled estimations have been made on the potential of agronomic biofortification using agronomic and dietary data. For example, Chilimba et al. (2012) calculated that application of about 5 g Se per ha to all maize crops in Malawi could increase the average dietary intake with 0.04 mg Se/day, considering a maize-based diet. Joy et al. (2015b) modelled the potential of Zn-enriched fertilizers to alleviate human dietary Zn deficiency, focussing on ten African countries where Zn supply is low and agronomic biofortification has potential through fertilizer subsidy programmes (Burkina Faso, Ethiopia, Ghana, Kenya, Malawi, Mali, Nigeria, Senegal, Tanzania and Zambia). Based on data from other studies on Zn concentrations in maize, rice and wheat

grains after Zn fertilization, the potential to reduce DALYs lost due to Zn deficiency was calculated. Malawi showed most potential: Zn-enrichment of currently used granular fertilizers could increase the amount of absorbable Zn in the diet by 5%, which would reduce DALYs lost due to Zn deficiency by 15%.

Finley (2006) suggested that further credibility of agronomic biofortification requires much more research on micronutrient bioa-vailability, including metabolic pathways that affect absorption and health benefits of different chemical forms of micronutrients. We can conclude that there is a considerable knowledge gap on the relationship between micronutrient fertilization of crops and the nutrition and health status of people who consume these crops. Systematic research on this is necessary to clarify the potential and required conditions to improve human health with agronomic biofortification.

6. Impact of agronomic biofortification on the environment

Application of micronutrient-enriched fertilizers is considered to have minimal negative environmental impact. Most micronutrients are not susceptible to leaching because they are strongly bound in the soil. The downside is that these elements accumulate over time and cause toxicity if large amounts are applied repeatedly. Selenium is the only micronutrient that can be lost by volatilization from the soil in gaseous form (Malagoli et al., 2015). To optimize nutrient use efficiency and minimize risks for toxicity, fertilization practices should include precise application strategies. The 4 R strategy aims to optimize precise application by fertilization of the "Right source and Right amount at the Right place and Right time" (Bruulsema et al., 2012). Studies such as that of Wang et al. (2013) investigating optimal fertilizer application rates are essential to increase production efficiency while minimizing environmental pollution and toxicity. When micronutrient demand and supply are well-matched, there should be no negative environmental effects. In fact, crop health improves when micronutrient deficiencies in the crop are alleviated. The improved general crop health enhances growth and nutrient uptake efficiency, as well as resilience against pests and diseases, what may reduce the need for pesticides and herbicides (Dimpka and Bindraban, 2015).

Mineral resources are mined for manufacture of micronutrient fertilizers, causing concern of natural resources and environmental pollution. Further concerns have been raised about the limited global availability of micronutrient rocks that may be exhausted in future (Dimpka and Bindraban, 2015). Although it is difficult to predict future supply and demand, these concerns emphasize the importance to increase nutrient use efficiency and nutrient recycling of micronutri-ents.

7. Agronomic biofortification compared with other interventions

The question remains whether agronomic biofortification is an effective, feasible and sustainable approach to alleviate micronutrient deficiencies; especially in comparison with other intervention strategies such as genetic biofortification, food fortification, supplementation and dietary diversification. Studies that compare the relative benefits of different interventions on nutrition are hardly available, and economic analyses available did not consider agronomic biofortification. Among the other interventions, genetic biofortification is more cost effective than food fortification, supplementation or dietary diversification in the long run, because it requires only one period of (breeding) investments (Stein et al., 2006; Ma et al., 2008).

Agronomic biofortification is often considered as a short-term solution to increase micronutrient availability and mainly to complement genetic biofortification (breeding), which is seen as a more sustainable approach (Garcia-Banuelos et al., 2014; Velu et al., 2014). Cakmak et al. (2010) argued that breeding is the only agricultural intervention to improve nutritional contents of staple

crops in low-income countries, because fertilizers are not accessible and affordable for resource poor farmers. The CGIAR biofortification programme HarvestPlus, (http://www.harvestplus.org), suggests that dietary diversification is the most sustainable solution, yet diverse foods are often not affordable for those at greatest risk. Bouis and Welch (2010) argue that supplementation and diet diversification programmes work best in centralized urban areas, whereas agronomic biofortification is the best approach to reach rural populations. Even though currently food fortification and supplementation are the most commonly used strategies to alleviate micronutrient deficiencies among humans, biofortification (agronomic and/or genetic) is considered to have more potential in the long-term because it seems more cost-effective, and practical (Garcia-Banuelos et al., 2014).

8. Potentials and constraints for implementation in sub-Saharan Africa

Multiple factors play a role in the potential of agronomic biofortification to be implemented in sub-Saharan agricultural systems and to eradicate micronutrient deficiencies among the undernourished population. Mineral micronutrient fertilizer use is currently limited in African countries due to general issues of cost and supply, the lack of information on micronutrient problems, a reliable fertilizer recommendation system, and the poor availability of micronutrient fertilizers. Weak infrastructure causes high prices, while investments are not always profitable for rural farmers when market accessibility or storage capacity are limited (Sanchez and Swaminathan, 2005). Nevertheless there is intense current interest in expansion of fertilizer use in sub-Saharan Africa among fertilizer companies and new fertilizer blending plants are under construction in several countries (IFDC, 2015).

Especially in regions with limited access to micronutrient fertilizers, integrated soil fertility management practices are the most realistic approach to alleviate micronutrient deficiencies (Cakmak and Hoffland, 2012). There are many low-cost, locally available and environmentally sustainable technologies that smallholder farmers can use to create fertile soil conditions using an integrated approach (Kerr et al., 2012). An example is micro-dosing: a strategy of fertilizer application in small quantities and close to the seed or plant. The precise targeting for the roots minimizes nutrient losses as well as fertilizer costs (Thilakarathna and Raizada, 2015). However, nutrient management can be a challenge for farmers (especially smallholders) who face obstacles such as limited availability of organic and mineral resources, high investment costs, extra labour requirements and environmental stress from drought, extreme rainfall, pests and crop diseases (Giller, 2002).

To overcome challenges concerning logistics to successfully implement agronomic biofortification, a whole supply chain approach is required (Slingerland, 2007). Development of the bio-physical, economic, social and political environment is necessary to facilitate proper technologies, allocation of resources and food processing systems. A key issue is the commercialization of smallholder agriculture to create markets for the extra production, because otherwise investments in (extra) mineral fertilizer are not economically feasible (Giller, 2002). In this regard, Kempen et al. (2015) engaged in initial analyses of spatial patterns of limiting soil micronutrients along with crop responses to micronutrient to identify where and what combination of nutrients are required (see also http://africasoils.net). Such information can guide agri-business and policymakers to target their interventions. Mapping of micronutrient deficiencies in order to provide field-specific fertilization recommendations, remains a challenge. Furthermore, knowledge and tools should be accessible and affordable for farmers in rural African regions. Soil test kits have been developed to assess soil fertility, but such tests are not sensitive or accurate enough to detect micronutrient deficiencies. The scientific world generally has more trust in models that can derive nutrient management recommendations on the basis of soil, climate and land-use

characteristics. Along with recommendations for mineral fertilizers, ISFM recommendations could be provided to ensure highest effectiveness and nutrient use efficiency. The African Soil Health Consortium (ASHC) works towards this goal (http://africasoilhealth. cabi.org).

Next, new fertilizer products and management practices need to be matched with local socio-cultural environments in order to enhance adoption (Slingerland et al., 2006). It is important to raise awareness about proper food processing and consumption that stimulates micro-nutrient uptake into the human body.

9. Conclusions

The effectiveness of agronomic biofortification largely depends on the bioavailability of micronutrients throughout the entire pathway from soil to plant, food and into the human body. Enhanced micro-nutrient uptake by crops is observed when the micronutrient-enriched fertilizer is applied to the soil in combination with NPK and organic fertilizers - highlighting the importance of integrated soil fertility management. The application of micronutrient-enriched fertilizers should have no serious negative environmental effect when used at appropriate rates and generally has agronomic benefits as it improves soil fertility and crop health. Agronomic biofortification can be effective in increasing yields and nutritional quality for certain crop-micronu-trient combinations; especially Zn and Se on wheat and maize, whereas Fe has shown little potential to date. Studies that link micronutrient fertilizer application to improved human health are scarce, especially for sub-Saharan Africa, which hampers definite conclusions about the efficacy and effectiveness of agronomic biofortification to alleviate micronutrient deficiencies among humans. We recommend to set up experiments and pilot-scale fertilization programmes in sub-Saharan Africa, to further explore this knowledge gap of the direct link between micronutrient-enriched fertilizer application to crops and the dietary micronutrient intake and uptake in the human bodies of consumers. Concerning the wide-scale implementation in sub-Saharan Africa, it is clear that multiple technical and socio-economic development steps are required to make micronutrient-enriched fertilizers more accessible and affordable for farmers.

Acknowledgements

This paper is based on a report prepared for the workshop 'Micronutrients management for improving harvest, farmers' income, human nutrition and the environment', facilitated and funded by the Food and Business Knowledge Platform in April 2016, in The Netherlands. We thank Nicole Metz, Prem Bindraban and the reviewers for their valuable comments.

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