Assessing and Mitigating Mycotoxin Contamination in Cereal Crops under Sustainable Management Systems

Cereal crops are fundamental to global food security but are susceptible to contamination by mycotoxins, secondary metabolites produced by pathogenic fungi, posing significant risks to human and animal health and causing substantial economic losses. Concurrently, agriculture is shifting towards more sustainable practices to reduce environmental impact and enhance resilience. However, the adoption of practices like conservation tillage, organic farming, and altered crop rotations can have complex and sometimes counterintuitive effects on the dynamics of toxigenic fungi and mycotoxin accumulation. This review synthesizes current knowledge on the occurrence of major mycotoxins (aflatoxins, ochratoxin A, fumonisins, deoxynivalenol, zearalenone) in key cereal crops (maize, wheat, barley, rice) and examines how prevalent sustainable agricultural management strategies influence mycotoxin risk. We discuss the impacts of conservation tillage, cover cropping, crop rotation, organic farming principles, and biological control approaches on fungal infection and toxin production. Furthermore, we explore current assessment methodologies and highlight integrated mitigation strategies compatible with sustainable frameworks, including host plant resistance, biological control agents, and optimized pre- and post-harvest handling. Challenges remain in predicting and managing mycotoxin risks within diverse agroecosystems, particularly under changing climate scenarios. An integrated, context-specific approach considering agronomic practices, environmental factors, and food safety is crucial for ensuring both the sustainability of cereal production and the safety of the resulting food and feed.

1. Introduction

Cereal grains, including maize (corn), wheat, rice, and barley, form the cornerstone of the global food system, providing staple calories and nutrients for a vast majority of the world’s population and essential feed for livestock (Awika, 2011). Ensuring the safety and quality of these crops is paramount. A significant threat to cereal safety arises from contamination by mycotoxins – toxic secondary metabolites produced by various filamentous fungi, primarily belonging to the genera Aspergillus, Penicillium, and Fusarium (Bennett & Klich, 2003). Mycotoxin contamination can occur pre-harvest in the field, during harvest, or post-harvest during storage and transportation. Consumption of contaminated food and feed can lead to acute or chronic health problems in humans and animals (mycotoxicoses), ranging from immune suppression and liver damage to carcinogenic effects (Marin et al., 2013; Wild & Gong, 2010). Consequently, regulatory limits for major mycotoxins in food and feed have been established in many countries, leading to significant economic losses due to rejected lots, reduced market value, and testing costs (Wu, 2006).

Simultaneously, there is a growing imperative to transition towards more sustainable agricultural systems. These systems aim to maintain productivity while minimizing negative environmental impacts, conserving resources (soil, water), enhancing biodiversity, and ensuring long-term economic viability (Pretty, 2008). Practices commonly associated with sustainable agriculture include conservation tillage (reduced or no-till), cover cropping, complex crop rotations, organic farming methods, and the promotion of integrated pest management (IPM) strategies often emphasizing biological control (Reganold & Wachter, 2016).

However, the relationship between sustainable agricultural practices and mycotoxin risk is complex and not always synergistic. Changes in agronomic management, such as altered tillage regimes or the avoidance of synthetic fungicides, can modify the agroecosystem in ways that may favour or inhibit the growth of toxigenic fungi and subsequent toxin production (Edwards et al., 2009; Schöneberg et al., 2016). Understanding these interactions is critical for developing management strategies that achieve both sustainability goals and food safety objectives. This review aims to:
(i) Briefly outline the major mycotoxins and associated fungi affecting key cereal crops.
(ii) Critically evaluate the influence of common sustainable agricultural practices on mycotoxin contamination risk.
(iii) Discuss current assessment and integrated mitigation strategies suitable for sustainable cereal production systems.
(iv) Identify knowledge gaps and future research directions.

2. Major Mycotoxins and Producing Fungi in Cereals

Several mycotoxins are of global concern in cereals. The most prominent include:

Aflatoxins (AFs): Primarily produced by Aspergillus flavus and A. parasiticus. They are potent hepatocarcinogens (particularly AFB1) and immunosuppressants. Maize and rice are particularly susceptible, especially under warm and humid conditions or drought stress (Payne & Brown, 1998).
Ochratoxin A (OTA): Produced mainly by Aspergillus section Circumdati and Nigri species, and Penicillium verrucosum. OTA is nephrotoxic, teratogenic, and potentially carcinogenic. It contaminates various cereals like wheat, barley, and maize, often associated with improper storage but field contamination can also occur (Heenan et al., 2021).
Fumonisins (FUMs): Produced predominantly by Fusarium verticillioides and F. proliferatum. They are associated with oesophageal cancer in humans and specific diseases in animals (e.g., leukoencephalomalacia in horses). Maize is the primary commodity affected (Marasas et al., 2004).
Trichothecenes (e.g., Deoxynivalenol – DON, Nivalenol – NIV): Produced by various Fusarium species, notably F. graminearum and F. culmorum. DON (also known as vomitoxin) causes feed refusal, vomiting, and immune system disruption. These toxins commonly contaminate wheat, barley, oats, and maize, often associated with Fusarium Head Blight (FHB) or Gibberella Ear Rot (GER) (Foroud & Eudes, 2009).
Zearalenone (ZEA): Also produced mainly by F. graminearum and F. culmorum. ZEA is an estrogenic mycotoxin, causing reproductive problems in livestock, particularly swine. It often co-occurs with DON in contaminated grains (Binder et al., 2007).

The prevalence and concentration of these mycotoxins are influenced by complex interactions between the host plant’s susceptibility, the presence of toxigenic fungal strains, environmental conditions (temperature, humidity, rainfall, insect damage), and agricultural practices (Magan et al., 2003).

3. Influence of Sustainable Agricultural Practices on Mycotoxin Risk

Sustainable practices alter the agroecosystem, impacting fungal inoculum levels, plant stress, microclimate, and microbial interactions, thereby influencing mycotoxin contamination.

3.1 Conservation Tillage (Reduced/No-Till)
Conservation tillage practices, which leave significant crop residues on the soil surface, are promoted for soil health benefits (erosion control, organic matter accumulation). However, crop residues can serve as a primary inoculum source for certain pathogenic fungi, particularly Fusarium species responsible for FHB/GER and DON/ZEA production (Edwards et al., 2009; Dill-Macky & Jones, 2000). Numerous studies have linked no-till or reduced tillage systems, especially in maize-wheat rotations, with increased FHB severity and DON accumulation in wheat compared to conventional ploughing which buries residues (Leplat et al., 2013). Conversely, for aflatoxins produced by soil-borne Aspergillus flavus, the impact of tillage is less consistent and may depend more on drought stress and insect damage (Abbas et al., 2006).

3.2 Crop Rotation
Diversified crop rotations are a cornerstone of sustainable agriculture, helping to break pest and disease cycles. Rotating cereals with non-host crops (e.g., legumes, oilseeds) can reduce the build-up of specific fungal inoculum in the soil and residues (Krupinsky et al., 2002). For example, avoiding planting wheat directly after maize can significantly reduce FHB risk, as maize residue is a major source of F. graminearum inoculum (Dill-Macky & Jones, 2000). The effectiveness depends on the specific fungi, their host range, and survival mechanisms. Monoculture or short rotations involving susceptible crops generally increase mycotoxin risk (Champeil et al., 2004).

3.3 Cover Cropping
Cover crops, grown primarily for soil protection and improvement between cash crops, can influence mycotoxin risk indirectly. They can improve soil structure and water infiltration, potentially reducing plant stress. Some cover crops may harbour beneficial microbes antagonistic to toxigenic fungi (Schöneberg et al., 2018). However, some cover crop species could potentially act as alternative hosts for certain Fusarium species, complicating their effect (Wegulo et al., 2015). The net impact likely depends on the cover crop species, termination method, and interaction with subsequent cash crops and environmental conditions. More research is needed to fully elucidate these interactions.

3.4 Organic Farming
Organic farming systems prohibit the use of synthetic fungicides, relying instead on cultural practices, resistant varieties, and biological methods for disease control. The impact on mycotoxin contamination is variable and debated (Hoogenboom et al., 2009; Bernhoft et al., 2010). Some studies report lower mycotoxin levels in organic cereals, potentially due to enhanced soil health and plant resilience, while others find higher levels, possibly attributed to the absence of effective fungicides during high-pressure disease periods or different storage practices (Malmauret et al., 2002; Cirillo et al., 2003). The outcome is highly dependent on the specific crop, region, climatic conditions, and overall management quality within the organic system.

3.5 Integrated Pest Management (IPM) and Biological Control
IPM frameworks, central to sustainability, emphasize monitoring and multiple control tactics. Reducing insect damage (e.g., corn borer damage in maize) is crucial, as insect wounds provide entry points for fungi like Fusarium and Aspergillus, often leading to higher mycotoxin levels (Blandino et al., 2012). Biological control, using non-pathogenic microorganisms to compete with or antagonize toxigenic fungi, is a promising sustainable strategy. Application of atoxigenic (non-toxin-producing) strains of Aspergillus flavus has proven effective in reducing aflatoxin contamination in maize and other crops (Pitt & Hocking, 2009; Dorner, 2004). Similar approaches are being explored for controlling Fusarium species (Palazzini et al., 2016).

3.6 Nutrient Management
Balanced plant nutrition contributes to overall plant health and resilience against pathogens. Deficiencies or excesses of certain nutrients (e.g., nitrogen, potassium, zinc) can increase plant susceptibility to fungal infection and potentially influence mycotoxin production (Técnor et al., 2006). Sustainable nutrient management, focusing on soil health and optimized nutrient supply (e.g., through organic amendments, precision application), may indirectly contribute to lower mycotoxin risk by reducing plant stress, though direct effects require further investigation.

4. Assessment and Monitoring Strategies

Effective management requires accurate assessment of mycotoxin risk.

Field Monitoring: Regular scouting for signs of fungal disease (e.g., FHB in wheat, ear rot in maize) is essential.
Risk Assessment Models: Predictive models incorporating weather data (temperature, humidity, rainfall during critical growth stages like flowering), previous crop, tillage system, and variety susceptibility are increasingly used to forecast high-risk periods for FHB/DON or aflatoxin contamination, guiding management decisions (e.g., fungicide application timing where permitted) (De Wolf et al., 2003; Moschini & Fortugno, 1996).
Sampling and Analysis: Representative sampling of grain lots is critical but challenging due to the heterogeneous distribution of mycotoxins. Approved sampling protocols must be followed. Various analytical methods are available for detection and quantification, ranging from rapid screening tests (e.g., ELISA, lateral flow devices) suitable for on-site checks to highly sensitive laboratory methods (e.g., HPLC, LC-MS/MS) for confirmation and regulatory compliance (Shephard et al., 2013).

5. Mitigation Strategies within Sustainable Frameworks

An integrated approach combining multiple strategies is most effective for managing mycotoxins sustainably:

Pre-Harvest Strategies:
- Host Plant Resistance: Selecting and breeding cereal varieties with genetic resistance or tolerance to fungal infection and/or mycotoxin accumulation is a cornerstone of sustainable management (Mesterházy, 2020).
- Agronomic Practices: Optimizing planting dates, crop density, irrigation (avoiding drought stress for aflatoxins, managing moisture for Fusarium), and implementing appropriate crop rotations and residue management tailored to the specific pathosystem and region.
- Biological Control: Application of registered atoxigenic strains of A. flavus (e.g., Afla-Guard®, AF36) is a key tool for aflatoxin management (Dorner, 2004). Research continues on biocontrol agents for Fusarium toxins (Palazzini et al., 2016).
- Chemical Control (within IPM): Where permitted and necessary based on risk assessment, targeted fungicide applications during critical periods (e.g., flowering for FHB) can be part of an IPM strategy, though their use is restricted in organic systems (Wegulo et al., 2011). Careful consideration of fungicide efficacy against specific fungi and potential impacts on non-target organisms is needed.
Post-Harvest Strategies:
- Timely Harvest: Harvesting at optimal maturity and moisture content.
- Drying: Rapidly drying grain to safe moisture levels (<14-15% for cereals) is critical to prevent fungal growth and toxin production during storage (Magan & Aldred, 2007).
- Cleaning and Sorting: Removing damaged kernels, dust, and foreign material can reduce overall mycotoxin load, as toxins are often concentrated in damaged fractions. Optical sorting technologies show promise (Pearson et al., 2004).
- Storage Conditions: Maintaining cool, dry, and aerated storage conditions is essential. Using hermetic storage technologies can also be effective, especially for smallholders (Mutungi et al., 2019).

6. Challenges and Future Directions

Despite progress, managing mycotoxins within sustainable systems faces challenges:

Complexity of Interactions: The effects of specific practices (like tillage) can vary significantly depending on the climate, soil type, specific fungal species, crop rotation, and interacting factors. General recommendations are often difficult.
Climate Change: Changing temperature and precipitation patterns, along with increased frequency of extreme weather events (droughts, floods), are likely to alter the geographical distribution and prevalence of toxigenic fungi and mycotoxin profiles, requiring adaptive management strategies (Paterson & Lima, 2010; Magan et al., 2011).
Knowledge Gaps: Further research is needed on the specific impacts of cover crops, complex rotations, and soil health improvements on diverse mycotoxin risks. The long-term effects of organic management need continued evaluation across different environments.
Socio-Economic Factors: Adoption of best practices, particularly by smallholder farmers in developing countries, is often constrained by cost, access to technology (resistant seeds, biocontrol agents, proper storage), knowledge, and market incentives.
Integrated Tools: Developing more accurate, localized risk prediction models and cost-effective, rapid detection methods remain priorities. Continued breeding efforts for robust host resistance are essential.

Conclusion

Mycotoxin contamination remains a significant challenge for global cereal production, impacting food safety, animal health, and trade. While sustainable agricultural practices offer numerous environmental and agronomic benefits, their implementation requires careful consideration of potential impacts on mycotoxin risks. Practices like conservation tillage can increase risk for residue-borne fungi like Fusarium, while crop rotation and biological control offer clear mitigation potential. The effect of organic farming is context-dependent. An integrated management approach, combining host resistance, informed agronomic practices (including appropriate tillage and rotation choices tailored to the specific risk), biological control where available, timely harvest, and proper post-harvest handling, is crucial. Achieving sustainable cereal production necessitates a holistic view that explicitly incorporates food safety considerations, supported by ongoing research, effective monitoring, risk assessment tools, and policies that enable farmers to adopt best practices. Addressing mycotoxin contamination is not merely a technical challenge but an integral part of building resilient and safe food systems for the future.

References

Abbas, Hamed & Wilkinson, J. & Zablotowicz, R. & Accinelli, Cesare & Abel, Craig & Bruns, HA & Weaver, MA. (2009). Ecology of Aspergillus flavus, regulation of aflatoxin production, and management strategies to reduce aflatoxin contamination of corn. Toxin Rev.. 28. 142-153. 10.1080/15569540903081590.
Awika, Joseph. (2011). Major Cereal Grains Production and Use around the World. Advances in Cereal Science: Implications to Food Processing and Health Promotion. 1089. 1-13. 10.1021/bk-2011-1089.ch001.
Brodal, Guro & Hofgaard, Ingerd & Eriksen, Gunnar & Bernhoft, Aksel & Sundheim, Leif. (2016). Mycotoxins in organically versus conventionally produced cereal grains and some other crops in temperate regions. World Mycotoxin Journal. 9. 1-16. 10.3920/WMJ2016.2040.
Binder, E.M. & Tan, L.M. & Chin, L.J. & Handl, Josy & Richard, J.. (2007). Worldwide occurrence of mycotoxins in commodities, feeds and feed ingredients. Animal Feed Science and Technology. 137. 265-282. 10.1016/j.anifeedsci.2007.06.005.
Blandino, Massimo & Scarpino, Valentina & Testa, Giulio & Vanara, Francesca & Reyneri, Amedeo. (2022). The Effect of Foliar Fungicide and Insecticide Application on the Contamination of Fumonisins, Moniliformin and Deoxynivalenol in Maize Used for Food Purposes. Toxins. 14. 10.3390/toxins14070422.
Champeil, Agnès & Doré, Thierry & Fourbet, J.F. (2004). Fusarium head blight: Epidemiological origin of the effects of cultural practices on head blight attacks and the production of mycotoxins by Fusarium in wheat grains. Plant Science. 166. 1389-1415. 10.1016/j.plantsci.2004.02.004.

If you want to learn more about Mitigating Mycotoxin Contamination in Cereal Crops under Sustainable Management Systems, check out Agri AI : Smart Farming Advisor and feel free to ask any questions!