Agricultural practices and their potential role in AUTHORS: mycotoxin contamination of maize and groundnut Sylvia Phokane1,2 Bradley C. Flett1,3 Edson Ncube1 subsistence farming John P. Rheeder4 Lindy J. Rose2 AFFILIATIONS: Mycotoxigenic fungi are common pathogens of maize and groundnuts; they produce mycotoxins which 1Grain Crops Institute, Agricultural reduce the yield and quality of these grain crops. Numerous agricultural practices including crop rotation and Research Council, Potchefstroom, storage methods have been shown to impact mycotoxin accumulation. Therefore, the farming and storage South Africa 2Department of Plant Pathology, practices in maize and groundnut subsistence farming systems in Pongola, Vryheid, Jozini, Manguzi and Stellenbosch University, Stellenbosch, Mbazwana Districts of northern KwaZulu-Natal (South Africa) were surveyed to determine their potential role South Africa 3Unit for Environmental Sciences and in promoting or mitigating mycotoxin contamination. A questionnaire about agricultural farming practices Management, North-West University, and storage facilities was presented to 65 subsistence maize and/or groundnut farmers. At least 90% of Potchefstroom, South Africa 4 the farmers surveyed were not aware of mycotoxins and their consequences to animal and human health. Institute of Biomedical and Microbial Biotechnology, Cape Peninsula The majority of the farmers did not practise crop rotation. However, they practised intercropping and sorted University of Technology, Cape Town, damaged and mouldy grain (maize and groundnuts) before storage. The damaged or mouldy grain was South Africa largely used as animal feed, thereby exposing animals to an increased risk of mycotoxicoses. Metal tanks CORRESPONDENCE TO: and inqolobane (a type of wooden structure) were identified as the most common storage structures. Edson Ncube Harvested homegrown maize was mostly used for the farmers’ own consumption but also sometimes sold to the local community. The implementation of mycotoxin awareness campaigns is necessary, particularly in EMAIL: NcubeE@arc.agric.za these districts. The storage facilities used by the subsistence farmers allowed increased moisture and insect invasion. The need for the surveillance of mycotoxins in subsistence-farmed food crops is vital. DATES: Received: 04 Apr. 2019 Significance: Revised: 13 June 2019 • The main finding of this study is the extent of post-harvest losses and mycotoxin contamination of Accepted: 15 July 2019 maize produced by smallholder farmers in South Africa. Published: 26 Sep. 2019 • We further identify methods to manage the risk of mycotoxin exposure to smallholder farmers and their HOW TO CITE: communities as well as reduce post-harvest losses. Phokane S, Flett BC, Ncube E, Rheeder JP, Rose LJ. Agricultural practices and their potential role in Introduction mycotoxin contamination of maize Maize (Zea mays L.) and groundnuts (Arachis hypogaea L.) are produced by subsistence farmers, particularly in and groundnut subsistence farming. the northern KwaZulu-Natal Province of South Africa.1,2S Afr J Sci. 2019;115(9/10), Maize is an important staple food and groundnuts serve Art. #6221, 6 pages. https://doi. as a protein and fat supplement for subsistence farmers.3,4 Both maize and groundnut may be contaminated with org/10.17159/sajs.2019/6221 mycotoxins, produced by fungi, prior to and after harvesting.5-7 Mycotoxin contamination follows infection by mycotoxigenic fungi, of which the most common are Fusarium and Aspergillus species1,2,8 that can contaminate ARTICLE INCLUDES: maize and groundnut with fumonisins and aflatoxins, respectively. Ingestion of mycotoxin-contaminated food and ☒ Peer review feed can cause mycotoxicoses in humans and animals.9,10 Fumonisins have been associated with a high incidence ☐ Supplementary material of oesophageal cancer in rural areas in South Africa due to the preference for mouldy kernels to produce traditional umqombothi beer.11 Mycotoxicoses may also develop in cattle that consume contaminated feed.12,13 During 2011, an DATA AVAILABILITY: ☐ estimated 100 dogs died in South Africa’s Gauteng Province due to the ingestion of aflatoxin-contaminated feed. 14 Open data set ☒ All data included Agricultural practices such as crop rotation, irrigation, early planting and use of transgenic hybrids are employed ☐ On request from author(s) by commercial farmers to reduce mycotoxin contamination of crops.15 Moreover, some subsistence farmers in ☐ Not available Tanzania and Zimbabwe recently applied these agricultural practices and a reduction in mycotoxin contamination ☐ Not applicable was reported.16,17 Hand sorting of maize before storage was also reported as a good measure to reduce fungal infection and subsequent mycotoxin contamination at storage.18,19 Unlike in a commercial setting, many subsistence EDITOR: farmers do not apply these agronomic practices, concentrating only on sorting their grain after harvest into visually Teresa Coutinho healthy and mouldy grain.20,21 In areas in the Eastern Cape and Limpopo Provinces, mouldy grain is not discarded but used for traditional beer, thereby posing a risk of mycotoxin contamination.3,22 KEYWORDS: mycotoxigenic fungi, storage, Limited information exists on storage of these crops by subsistence farmers and the associated mycotoxin risks. mycotoxins, survey, South Africa Storage of improperly dried grain, accompanied by high temperatures, causes rapid proliferation of mycotoxigenic fungi which results in reduced quality, nutrition and dry matter and higher mycotoxin levels.23-25 Contamination at FUNDING: National Research Foundation storage by fungi can occur when the moisture content is above 13% and temperatures are between 10 °C and 40 °C. 26 (South Africa); The Maize Trust Therefore, the use of ventilated storage systems to reduce mycotoxin contamination is recommended, together with (South Africa); Agricultural Research appropriate post-harvest control technologies to minimise mycotoxin contamination in the food chain.27-29 For example, Council (South Africa) storage in moisture-free, dry wooden pallets, ventilated drying on polythene sheets and hand sorting led to a decrease in aflatoxin contamination of kernels at storage.30 Storage facilities are some of the control points that have to be re- evaluated in the value chain; good storage facilities will lead to good marketable agricultural products. Subsistence farmers incur economic losses due to pre-harvest and post-harvest contamination of grain crops caused by fungal species and insect pests. The present work continues earlier studies1,2 that identified hotspots for fumonisin and aflatoxin contamination. Good farming practices and proper pre-harvest handling of maize and groundnuts, © 2019. The Author(s). Published together with good storage practices, have been demonstrated to minimise the risk of fungal contamination. Hence, under a Creative Commons we aimed to identify pre- and post-harvest practices that could potentially contribute to mycotoxin contamination of Attribution Licence. maize and groundnuts produced in KwaZulu-Natal. Research Article https://doi.org/10.17159/sajs.2019/6221 1 Volume 115| Number 9/10 September/October 2019 Mycotoxin contamination of maize and groundnuts Page 2 of 6 Materials and methods Only 6% and 9% of farmers in Pongola and Vryheid, respectively, had an idea of what mycotoxins could be, but did not know the cause of Geographical areas surveyed these mycotoxins and their implications on animal and human health Agricultural extension officers from the South African Department of (Figure 1). Mycotoxin awareness and maize districts were therefore Agriculture and Rural Development assisted with the selection of five independent (p=0.1766). districts in northern KwaZulu-Natal and identification of households within districts where maize and groundnuts were planted. Global Positioning Residue removal System (GPS) was used to detect and mark different localities within Of the farmers in Jozini, 43% removed residues from the soil before the districts. Subsistence farmers growing maize or groundnuts were planting their groundnuts, 54% of the farmers in Manguzi did so, while all interviewed in all five districts: Jozini (n=7), Manguzi (n=17), Mbazwana of the farmers in Pongola but none of the farmers in Mbazwana removed (n=13), Pongola (n=17) and Vryheid (n=11). All farmers in all five crop residues before planting groundnuts (Figure 2). Residue removal and districts planted maize and all farmers in Jozini, Manguzi and Mbazwana groundnut districts were therefore independent (p=1.769) planted groundnuts as well. No farmer in Vryheid planted groundnuts and there was only one identified groundnut farmer in Pongola. Questionnaires The agricultural farming practices, storage facilities and grain consumption for each farmer were determined through a survey. Questionnaires were drafted in English and translated into isiZulu, the predominant local language. These questionnaires were approved by the South African Medical Research Council. Both closed- and open-ended questions were asked randomly to ensure adequacy of the questionnaire. The questions were on the awareness of mycotoxins, crop rotation, intercropping, residue removal, sorting of damaged and mouldy grain, end result of the sorted grain, types of storage facilities, consumption and trading of homegrown maize and groundnut. An awareness of mycotoxins, nematodes and fungal Figure 2: Residue removal before planting groundnuts by subsistence pathogens was determined as well as whether participants were aware farmers in four districts of northern KwaZulu-Natal (chi-square: of negative health implications caused by fungal pathogens. Additional d.f.=3; p=1.769). explanations of questions were provided when needed and included non- scientific descriptions such as mould growth for fungal infection and Crop rotation and intercropping mycotoxin contamination. All the farmers were also informed that fungal The majority of groundnut farmers did not practise crop rotation: 71%, infection may be associated with mycotoxin contamination. 92% and 100% in Jozini, Manguzi and Mbazwana, respectively, did not Interviews rotate their groundnuts with any other crop (Figure 3). Only farmers in Pongola (100%) practised crop rotation (Figure 3) and therefore crop Before the interviews, the farmers were informed about the significance rotation and groundnut-farming districts were dependent on each other of the survey. The first author interviewed each farmer according to the (p=0.0122). Farmers in all districts did not rotate maize with other crops questions stated on the questionnaire. Gathering of information was done (data not shown), but a variety of crops including beans, groundnuts and in collaboration with local extension officers. An opportunity was granted pumpkins were intercropped with maize. Maize was widely intercropped for questions after the interviews and appropriate management strategies with groundnut in the Manguzi and Mbazwana Districts by 53% and 92% were discussed with the farmers and local extension officers. of farmers, respectively. Some farmers in all surveyed maize districts only Statistical analyses planted maize (data not shown). Intercropping and the districts in which maize farmers were surveyed were, therefore, dependent on each other The data obtained from the questionnaires were analysed using a chi- (p<0.001) (data not shown). Only farmers in the Pongola District did square test for independence. One-way analysis of variance (ANOVA) not intercrop groundnuts with other crops, whereas farmers in the other was used to test only the numerical entries. The significance level for districts intercropped with crops such as spinach (Spinacia oleracea L.) and both tests was set at a 95% confidence level with p<0.05 indicating a cowpeas (Vigna unguiculata L.) (data not shown). Therefore, intercropping significant difference. The tested null hypothesis (Ho) for the chi-square was dependent on the groundnut-farming districts surveyed (p=0.0071) test was that the factor evaluated is independent of the different districts (data not shown). surveyed. Conversely, the alternative hypothesis (Ha) was that the factor is dependent on the different districts surveyed. The null hypothesis was accepted if p>0.05 and rejected if p<0.05.31 No Yes Results Mycotoxin awareness None of the farmers in Jozini, Manguzi and Mbazwana were aware of mycotoxins (Figure 1). Jozini Manguzi Mbazwana Pongola Districts Figure 3: Rotation of groundnuts with other crops by subsistence farmers in four districts of northern KwaZulu-Natal (chi-square: d.f.=4; p=0.0122). Grain sorting before storage All the maize farmers in all districts surveyed sorted their maize into apparently healthy, mouldy and damaged maize before storage (results Figure 1: Mycotoxin awareness of subsistence farmers in five districts of not shown). All the groundnut farmers in Jozini and Manguzi and 10% in northern KwaZulu-Natal (chi-square: d.f.=4; p=0.17766). Mbazwana also sorted their groundnuts into apparently healthy, mouldy Research Article Volume 115| Number 9/10 https://doi.org/10.17159/sajs.2019/6221 2 September/October 2019 Percentage farmers Mycotoxin contamination of maize and groundnuts Page 3 of 6 and damaged groundnuts before storage (Figure 4). Sorting and groundnut farmers in Jozini, Pongola and Vryheid (Figure 7). The storage facilities districts surveyed are therefore independent variables (p=0.610). and maize districts surveyed were dependent variables (p=0.0014). 120 No Yes 100 80 60 40 a b c 20 Figure 6: Common storage facilities for maize utilised by subsistence 0 farmers in districts of northern KwaZulu-Natal: (a) inqolobane, Jozini Manguzi Mbazwana Pongola (b) metal drum and (c) groundnut bags. Districts Figure 4: Sorting of damaged and mouldy groundnuts by subsistence 100 House Inqolobane Metal tank farmers in four districts of northern KwaZulu-Natal (chi-square: d.f.=3; p=0.610). 80 60 End result of mouldy and damaged grain 40 All the farmers in Jozini fed the mouldy and damaged maize kernels to 20 chickens (Gallus gallus domesticus) only. Some farmers in the other four districts used the mouldy and damaged maize as chicken feed, but 0 also discarded the grain. Additionally, 59% of farmers in Pongola and Jozini Manguzi Mbazwana Pongola Vryheid 55% of farmers in Vryheid fed the mouldy and damaged grain to other Districts domestic animals such as pigs (Sus domesticus), cattle (Bos taurus) and goats (Capra aegagrus hircus). Furthermore, 18%, 8% and 9% of Figure 7: Storage facilities utilised by subsistence farmers in five districts the farmers in Manguzi, Mbazwana and Vryheid, respectively, consumed of northern KwaZulu-Natal (chi-square: d.f.=8; p=0.0014). the mouldy and damaged maize (Figure 5). The end-users of mouldy and damaged maize kernels and the maize districts surveyed were, therefore, Consumption and trading of grain dependent (p=0.0009). For groundnuts, all the farmers in Pongola and Farmers from all districts either only consumed or both consumed some farmers in other districts fed the mouldy and damaged groundnuts and sold their homegrown maize (Figure 8). Consumption with trading to chickens only. Less than 30% of farmers in Manguzi and Mbazwana of homegrown maize and maize-farming districts were independent discarded the mouldy and damaged groundnuts. In contrast with maize (p=0.1766). Half the farmers in Mbazwana only consumed their farmers, more groundnut farmers in Manguzi (50%) consumed the homegrown groundnuts and the other half both sold and consumed their mouldy and damaged groundnuts. Also, 60% of groundnut farmers in homegrown groundnuts. Over 60% of farmers in Jozini and Manguzi only Jozini consumed mouldy and damaged groundnuts (data not shown). consumed their homegrown groundnuts (data not shown). Consumption The end-users of mouldy and damaged groundnuts and groundnut with trading of homegrown groundnuts and groundnut-farming districts districts surveyed were also dependent variables (p=0.0396) (data were also independent (p=0.635) (data not shown). All the farmers not shown). in Jozini and Manguzi only sold their homegrown maize to the local community; farmers in Mbazwana, Pongola and Vryheid also sold their homegrown maize to the nearest markets (data not shown). Maize trading areas and maize districts were dependent on each other (p=0.0046) (data not shown). Figure 5: End result of damaged and mouldy maize produced by subsistence farmers in five districts of northern KwaZulu-Natal (chi-square: d.f.=12; p=0.0009). Storage facilities Figure 8: Consumption and trading of harvested homegrown maize by A type of storage facility widely used in all the northern KwaZulu-Natal subsistence farmers in five districts of northern KwaZulu-Natal districts surveyed was an inqolobane, which is the isiZulu name for (chi-square: d.f.=4; p=0.1766). a widely ventilated wooden storage facility (Figure 6a). Metal drums were used by maize farmers only; some metal drums were ventilated and others unventilated (Figure 6b). Groundnuts were planted in small Discussion quantities in comparison to maize, hence groundnuts were easily and Numerous crop production and post-harvest practices have been found most commonly placed in bags which were stored in the farmers’ homes to influence mycotoxin accumulation in grain crops. In this study, the (Figure 6c). In fact, in all the groundnut-farming districts (Jozini, Manguzi majority of groundnut farmers and all the maize farmers surveyed did not and Mbazwana), farmers stored groundnuts in their homes only (data practise crop rotation. Furthermore, nearly half of the groundnut farmers not shown). Metal tanks were used to store maize by some subsistence did not remove plant residues before planting. Crop rotation can help Research Article Volume 115| Number 9/10 https://doi.org/10.17159/sajs.2019/6221 3 September/October 2019 Percentage farmers Percentage farmers Mycotoxin contamination of maize and groundnuts Page 4 of 6 reduce available inoculum for subsequent infection when non-host crops Most farmers use wooden granaries for storage; these structures are are employed.32 In a recent study, conservation agriculture – commonly widely used, possibly because of the ease of construction and for drying described as practices that maintain permanent soil cover (no removal of maize ears. However, this structure allows invasion by insect pests and plant residues) and minimum soil disturbance – did not increase the risk rodents as it is not covered on top. Insects damage maize ears during of maize ear rots and mycotoxin production.33 The storage facilities used feeding, thereby facilitating fungal invasion and infection.43 Therefore, by both maize and groundnut farmers favour fungal entry which increases maize cannot be stored for prolonged periods under such conditions. the risk for mycotoxin contamination. Improving maize and groundnut Farmers could be advised to use metal silos44,45 and hermetic storage subsistence farming and grain storage is crucial in mitigating the risk of containers46; these storage structures are airtight and, therefore, prevent mycotoxin contamination within the particular communities surveyed. any pathogen or pest from invading the stored maize42. Subsistence Good-quality maize-based and groundnut-based products are not only farmers prefer the traditional storage systems as they are cheaper to necessary for consumption but also for trade. Hence, it was important to construct and maintain, although their use can cause high post-harvest conduct a survey on the current farming practices in order to determine losses.45 The specific storage practices employed were dictated by the which potentially contribute to increased risk of mycotoxin contamination. quantity of maize produced. For instance, in high maize production areas This information will help to determine possible intervention strategies that such as Vryheid and Pongola, maize was predominantly stored in tanks. could cause a reduction in the risk of mycotoxin contamination. Subsistence farmers consume high quantities of homegrown maize, The lack of mycotoxin awareness in these districts indicates that humans as much as 300 g per person per day,47 and also sell the homegrown and livestock may be consuming mycotoxin-contaminated maize and maize and groundnuts to the local community. Hence their exposure groundnuts daily which places them at a high health risk. Incidentally, to mycotoxins is potentially higher than that of consumers in cities some agricultural practices used by subsistence farmers, such as sorting and towns. Furthermore, subsistence farmers have to contend with of damaged and mouldy grain from storage, may have assisted in limiting supermarkets present in local communities and small towns, which sell mycotoxin exposure. Crop residues also harbour mycotoxigenic fungi,34 their good-quality products, especially maize meal and bread, at reduced hence it is vital to remove crop residues before planting so that they do costs.48 Also, pressure is placed on subsistence farmers to produce safe not serve as an inoculum source. Destruction or removal of infected crop and healthy food due to new regulations for deoxynivalenol and fumonisin residues from the field has been found to reduce fungal inoculum.35 B1 and B2 limits in maize. The South African government implemented new regulations, setting maximum levels of 2000 µg/kg for deoxynivalenol The practice of rotating maize and groundnuts with other crops may be and 4000 µg/kg for fumonisin B and B .49 Subsistence farmers were associated with the variation in soil types of the districts surveyed as 1 2not aware of these regulations. The monitoring of these regulations in an this directly determines the crops that can be successfully cultivated. informal environment is unclear and possibly impractical; however, the For example, the Manguzi and Mbazwana Districts had sandy soil types supply chain will need to be regulated for quality and safety10 considering which mostly favour the cultivation of groundnuts over maize. Light- the potential for trade between subsistence farmers. Therefore, there is a textured soils which include deep, well-drained sandy and loamy sand need to determine the extent of mycotoxin contamination of these crops. soils at a pH between 5.3 and 7.3 favour significant groundnut yields.36 Additionally, limited information is available on control methods to reduce The majority of farmers do not employ crop rotation, possibly because of the risk of mycotoxin contamination of food crops. a lack of knowledge of the advantages. Pest and disease cycles are broken by crop rotation, thereby reducing fungal infestation and subsequent Conclusion mycotoxin contamination in the field.37 Farmers prefer to grow the same crop throughout, especially when it can be sustainably produced under Mycotoxin contamination of maize and groundnuts produced through prevailing conditions. However, rotating crops potentially increases crop subsistence farming systems can be reduced by following good agricultural yield and the root system health is maintained by the reduced inoculum farming and storage practices such as crop rotation and sorting before potential of soil-borne pathogens.38 Intercropping has also been shown to storage, respectively, thus, improving the health and economic status of reduce contamination of maize with mycotoxins.39 subsistence farmers and the communities involved. The implementation of good farming practices can be effortless; however, access to adequate The manner in which farmers sorted groundnuts was determined by storage facilities may not be feasible. Therefore, support in this regard is the quantity of groundnuts harvested and/or whether this would be kept of utmost importance in subsistence farming. Furthermore, it is vital, to for household consumption or sold for additional income. Mycotoxin minimise mycotoxin contamination, that knowledge of good agricultural contamination was reduced in the former Transkei region by sorting practices be transferred to subsistence farmers as well as agricultural damaged/mouldy grain from apparently healthy grain.40 This study extension officers. This knowledge transfer can form part of mycotoxin reported that fumonisin concentration decreased by 71% after removing awareness campaigns to inform farmers of the threats and effects of highly infected maize kernels. Also, washing and sorting of maize kernels mycotoxins on humans and animals. Additional surveillance is required was found to reduce fumonisin contamination by 84%.8 In the Rombo to continuously monitor and advise on mycotoxin contamination and District of Tanzania the sorting of maize also led to a reduction in fumonisin potential exposure in subsistence farming. contamination.18 Therefore, it is good practice that the majority of the farmers in the northern KwaZulu-Natal sort their maize and groundnut to Acknowledgements decrease contamination at storage. Mouldy and damaged maize was used We acknowledge the financial support received from The Maize Trust, to feed domestic livestock while most farmers across all districts fed the National Research Foundation of South Africa (Thuthuka grant no. 84162) mouldy and damaged maize to chickens. Mycotoxin-contaminated feed and the Agricultural Research Council of South Africa. We thank the generally affects the growth of chickens.41 Department of Agriculture and Environmental Affairs in the KwaZulu-Natal Farmer preference dictated the use of specific storage facilities in the Province for their collaboration and support provided; Ms Gugu Khali and different districts. The choice of a storage facility may be due to problems Ms Yvonne Maila for assisting with sample collection in all the districts; experienced at storage relating to the different districts; for example, the use and Ms Nicolene Thiebaut for statistical analysis of the results. of tanks and drums to prevent mice damage specifically. Storage facilities used by farmers in the surveyed districts in northern KwaZulu-Natal are the Authors’ contributions same as those used by other farmers in sub-Saharan African countries30 S.P.: Research design; fieldwork and sample collection; laboratory analysis and some of these storage facilities do not promote proper drying of of samples; data analysis; and writing article drafts. B.C.F.: Research maize and thus enhance interaction with insects, thereby promoting fungal design; research supervision; reviewing article drafts. E.N.: Obtaining infection and mycotoxin production30. The application of a pesticide to funding; research design; research supervision; reviewing article drafts. control stored-maize insect pests was proved to be an ineffective method J.P.R.: Obtaining funding; research design; reviewing article drafts. L.J.R.: compared to other post-harvest methods.42 Research design; research supervision; reviewing article drafts. 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