“Ground-Truthing” Efficacy of Biological Control for Aflatoxin Mitigation in Farmers’ Fields in Nigeria: From Field Trials to Commercial Usage, a 10-Year Study

Abstract

In sub-Saharan Africa (SSA), diverse fungi belonging to Aspergillus section Flavi frequently contaminate staple crops with aflatoxins. Aflatoxins negatively impact health, income, trade, food security, and development sectors. Aspergillus flavus is the most common causal agent of contamination. However, certain A. flavus genotypes do not produce aflatoxins (i.e., are atoxigenic). An aflatoxin biocontrol technology employing atoxigenic genotypes to limit crop contamination was developed in the United States. The technology was adapted and improved for use in maize and groundnut in SSA under the trademark Aflasafe. Nigeria was the first African nation for which an aflatoxin biocontrol product was developed. The current study includes tests to assess biocontrol performance across Nigeria over the past decade. The presented data on efficacy spans years in which a relatively small number of maize and groundnut fields (8–51 per year) were treated through use on circa 36,000 ha in commercially-produced maize in 2018. During the testing phase (2009–2012), fields treated during one year were not treated in the other years while during commercial usage (2013–2019), many fields were treated in multiple years. This is the first report of a large-scale, long-term efficacy study of any biocontrol product developed to date for a field crop. Most (>95%) of 213,406 tons of maize grains harvested from treated fields contained <20 ppb total aflatoxins, and a significant proportion (>90%) contained <4 ppb total aflatoxins. Grains from treated plots had preponderantly >80% less aflatoxin content than untreated crops. The frequency of the biocontrol active ingredient atoxigenic genotypes in grains from treated fields was significantly higher than in grains from control fields. A higher proportion of grains from treated fields met various aflatoxin standards compared to grains from untreated fields. Results indicate that efficacy of the biocontrol product in limiting aflatoxin contamination is stable regardless of environment and cropping system. In summary, the biocontrol technology allows farmers across Nigeria to produce safer crops for consumption and increases potential for access to premium markets that require aflatoxin-compliant crops.

Present Status and Perspective on the Future Use of Aflatoxin Biocontrol Products

“…The extensive research demonstrating the efficacy, safety, and benefits of the technology have allowed registration of several aflatoxin biocontrol products with regulatory authorities. Following registration, large-scale use is possible after developing infrastructure to produce the biocontrol product on a large-scale, developing sound commercialization strategies, transferring the technology to appropriate industries, and implementing innovative marketing and distribution channels [48,60,87]. It is worth mentioning that this management strategy is especially useful in food-insecure regions with rapidly growing populations in Africa, which also suffer major losses in agriculture due to pests and diseases [121], and where farmers' access to other control methods is much more restricted.…”

“…Recently, efficacy trials have been conducted in sorghum in Ghana and sunflower in Tanzania and substantial reductions in aflatoxin have been achieved (unpublished results). Results of both field experiments and commercial treatments in cotton, maize, and groundnut fields show reduction in aflatoxin contamination ranging from 70% to 100% compared to adjacent non-treated fields [48,52,87,88,101,102]. In the commodities in which aflatoxin contamination is more frequent (i.e., the proportion of grains/seeds/fruits that can be contaminated by aflatoxin is higher), the impact of biocontrol isolates…”

“…The true value of a biocontrol product composed of single or multiple isolates as active ingredient is revealed when the product is applied in crops managed by the farmers themselves, in multiple fields (usually 300 to 500) in multiple agro-ecological zones, and during multiple years [51,87,88]. Evaluating a product under controlled conditions, in a limited number of locations can result in incorrect interpretation regarding the benefits of biocontrol and its efficacy across environments [89].…”

“…Conversely, when the percentage of potential points of infection is meager, which occurs in the case of tree nut crops (i.e., from 1/5000 to 1/20,000 in pistachio kernels), the aflatoxin contamination on untreated fields is highly variable (measured as the variation coefficient) and, subsequently, the impact of the biocontrol agents in reducing aflatoxin contamination is frequently low but highly variable. Figure 3 shows the relationship between reduction of aflatoxin contamination as a result of application of atoxigenic A. flavus isolates in different commodities and the variation coefficient of aflatoxin contamination in untreated fields of these crops [29,47,51,52,87,88,92,101,102].…”

Functional Biology and Molecular Mechanisms of Host-Pathogen Interactions for Aflatoxin Contamination in Groundnut (Arachis hypogaea L.) and Maize (Zea mays L.)

“…A promising strategy is the field application of atoxigenic A. flavus strains to reduce aflatoxin content in crops. In the United States and several African countries, driven primarily by USDA-ARS and IITA, respectively, the application of carefully selected atoxigenic A. flavus strains as biocontrol agents has consistently reduced aflatoxin contamination in commercially produced crops and allowed farmers to enter domestic and international premium markets (Cotty et al, 2007;Dorner, 2009;Mehl et al, 2012;Doster et al, 2014;Bandyopadhyay et al, 2019;Ortega-Beltran and Bandyopadhyay, 2019;Schreurs et al, 2019;Senghor et al, 2019). When applied at the right stage, treated crops accumulate over 80% less and sometimes even 100% less aflatoxin than non-treated adjacent crops.…”