Climate change and mycotoxin risk: Analysing an evolving problem

Authors: Dr. Radka Borutova and Nicholas Adams, Alltech Mycotoxin Management

Click below to listen to the Mycotoxin Matters podcast episode with Dr. Radka Borutova hosted by Nick Adams. You can also hear the full audio or listen to the episode on Apple Podcasts or Spotify. 

Introduction

The mycotoxins of greatest concern to food and feed safety are produced by several fungal genera of filamentous fungi, among which Aspergillus, Fusarium and Penicillium are the primary strains. These families of fungi produce many of the most important species of mycotoxins globally, including aflatoxins, fumonisins, ochratoxins, trichothecenes and zearalenone (Marasas, et al., 2008). These fungi colonize a large variety of crop species and can adapt to a wide range of environmental conditions. An understanding of the environmental factors that affect the ability of fungi to grow, survive and interact with plants is important in order to better understand the variation in the population structures of mycotoxigenic fungi, their interactions with crop plants and their ability to produce mycotoxins. Because climate conditions can profoundly affect growth, distribution and mycotoxin production in fungi, changes in climatic conditions has the potential to increase the risks that mycotoxigenic fungi pose to food and feed safety (Medina et al., 2017). The appearance of new mycotoxin-commodity combinations is of further concern and provides evidence for the emergence of new fungal genotypes with higher levels of aggressiveness and altered mycotoxin production (Moretti et al., 2019).

Climate change

Climate change (CC) (IPCC, 2007) will affect mycotoxins in food and feed. Human activity is causing the weather phenomenon; hence, we are living in the Anthropocene epoch, whereby the environment is being changed (Crutzen and Stoermer, 2000). Concentrations of methane, carbon dioxide and nitrous oxide in the atmosphere are increasing, resulting in environmental warming, greater precipitation and/or drought.

1. Predictions concerning temperature on pre-harvest crops

IPCC (2007) states that a warmer planet is “virtually certain” and that warm spells or heat waves are “very likely”. The impact this will have on agriculture and food safety will vary for different geographical regions, but a profound impact on agriculture (e.g., alterations in arable land and crop yields, variations in the seasons, changes in soil quality) will occur. Increases in the loss of soil minerals, variations in their bioavailability and alterations of soil microorganism ecosystems are all mentioned (IPCC, 2007). The report states that temperature will rise by approximately 4°C in 100 years. This may affect mycotoxin concentrations, as fungi with higher temperature optima for growth and mycotoxin production will dominate in regions that currently experience cooler climates or may become less prevalent as the temperatures become too high in regions where the temperature is already hot. Temperature is more predictable in terms of its effect on mycotoxin problems than moisture.

More crops/greater yields will be seen in regions that are currently cool, while fewer crops/yields will be produced in currently warm regions (IPCC, 2007). If crops increase, it will be important to consider increasing the amount of mycotoxin analyses proportionately. Where more crops/greater yields will occur due to CC in currently cool regions, an increase in the total mass of mycotoxins will also tend to occur, simply because there are more crops in which mycotoxins can proliferate. The overall quality of the crops may be worse than before in terms of mycotoxins per unit weight of crop because, for example, aflatoxins may increase as the temperature increases towards the optima for the producing fungi. Finally, the regions that are currently cool will experience worsening storage conditions as the temperatures increase to those compatible with increased fungal growth. Fewer crops/yields will occur as a result of CC in some currently warm regions. This will lead to a decrease in the total mass of mycotoxins simply because there are fewer crops in which those mycotoxins can thrive. However, it is possible that the crops produced will be of lower quality due to the stressful effects of CC and may contain more mycotoxins per unit weight of crops. Finally, the new hot and dry conditions in some regions will lead to good storage conditions — a potential advantage of CC. This is because these hot and dry conditions will assist in maintaining the crop in conditions that are unsuitable for fungal growth and mycotoxin production.

Furthermore, some regions may become suitable for growing novel crops while others become unsuitable for existing ones. More insects and pests will manifest at higher temperatures (IPCC, 2007), by which mycotoxigenic fungi are spread (Tirado et al., 2010), and more insects may increase the population of insect-feeding birds, perhaps resulting in more bird damage to crops.

2. Predictions concerning precipitation on pre-harvest crops

The IPCC (2007) report states that heavy precipitation is “very likely” in some regions while drought is “likely” in others. The effects that precipitation will have on mycotoxins in crops will be more unpredictable compared to the impact of temperature, whose effects are more defined. It is very likely that annual precipitation in the European and African Mediterranean regions will decrease greatly, as will winter rain in southwestern Australia. At high latitudes, precipitation will increase, whilst decreases are likely in most subtropical lands — especially at the margins of the subtropics — due to the intensification of the global hydrological cycle. Extremes of daily precipitation will very likely increase in Northern Europe, Southern and Eastern Asia, Australia and New Zealand, and in many other regions.

Summer drying in mid-continental areas increases the prospect and risk of drought. It is predicted that half of the plant species in those regions will be at risk (IPCC, 2007; Miraglia et al., 2009). Fewer crops are predicted, which may reduce the total amounts of mycotoxins in those crops. Consequently, there will be a proportionate reduction in the need to analyze these crops, as they will be fewer in quantity. Increased crop stress from heavy precipitation will occur with lower crop yields. These crops will have a lowered resistance to fungal invasion, and consequently, increases in mycotoxins may occur. Damage to crops, soil erosion and an inability to cultivate land are all predicted in the IPCC (2007) report, and these effects will lead to greater fungal ingress and mycotoxin production. Soil erosion allows nutrients to leach away from the plant and decrease the plant’s resistance to fungal infection, which may result in more mycotoxins. Conversely, storage conditions may improve under drought conditions, perhaps resulting in fewer mycotoxins thanks to the improved drying of crops. Drought stress will be important, particularly in developing countries. For example, marginal land where stress-tolerant sorghum was grown has been replaced with maize, especially in Africa (IPCC, 2007; Miraglia et al., 2009), and it is perhaps obvious that, increasingly, methods for analyzing mycotoxins in maize over sorghum will be required.

3. Post-harvest stored grain ecosystems

The second phase of contamination with mycotoxins may occur from crop maturation until consumption (Tirado et al., 2010). The crop could be exposed to warm, moist conditions on the feedlot floor, in the field, and during transportation (Tirado et al., 2010) and storage. However, problems begin during heavy rains before harvest and late dry-down, with implications regarding CC. The key environmental factors of temperature, water availability and gas composition influence mycotoxin production. Spoilage will not happen if grain is stored at ≤0.70 aw (water activity), and CC that leads to warmer temperatures can help achieve this. In addition, farms that can afford to keep silos within safe ranges may “only” experience increased costs from more energy expenditure (Paterson and Lima, 2010). Storage will be difficult in cases where CC results in high moisture levels, leading to problems with drying crops.

Magan et al. (2003) developed an Index of Dominance (ID) to interpret dominance in grains, which varied with aw and temperature. Presumably, an assessment of the role of mycotoxins was outside the remit of the study. The most competitive species of bacteria in wheat grain in the U.K. were Aspergillus fumigatus, Aspergillus nidulans, Penicillium brevicompactum, Penicillium hordei and Penicillium roqueforti, none of which are the predominant mycotoxigenic species (with the possible exception of P. roqueforti). Furthermore, an ochratoxin A-producing strain of A. ochraceus dominated A. candidus and A. flavus at 18°C in situ. However, at 30°C, it was not dominant against A. flavus (Magan et al., 2003), indicating that in temperate climates, if the temperature increases to 30°C, A. flavus may become problematic. F. verticillioides and Fusarium proliferatum form niches with other storage fungi, such as Penicillium spp., A. flavus and A. ochraceus, at 25° and 30°C. A. ochraceus and Alternaria alternata demonstrated changed interactions within an altered environment.

The niche overlap is in a state of flux and is influenced significantly by water availability, temperature and nutrient status. The importance of such fluxes is crucial to understanding and controlling mycotoxigenic fungi in the stored-grain ecosystem, as will occur during CC, although more information on how mycotoxins affect competition is required (Paterson and Lima, 2010). Fusarium species incubated with Aspergillus niger resulted in an increase in fumonisin, especially at 0.98 aw, although under drier conditions, an increase did not occur in maize (Marín et al., 1998), which is relevant to regions that will become dryer from CC. However, A. niger can also produce fumonisin (Frisvad et al., 2007; Noonim, et al., 2009), and so the increase may relate to both fungi producing these compounds, which was not considered. Deoxynivalenol was stimulated from F. culmorum with Microdochium nivale on wheat grain with 0.995 aw and was reduced under drier conditions (0.955 aw), with Alternaria tenuissima, Cladosporium herbarum and Penicillium verrucosum.

4. Carbon dioxide change and mycotoxin production

Slightly elevated CO2 concentrations and interactions with temperature and water availability may stimulate growth in some mycotoxigenic species, especially under water stress (Magan et al., 2011), although the information relating to this is scant. The concentration would increase from 0.03% to 0.08% in the atmosphere if the predicted CO2 increase from CC is maintained for the next 100 years (IPCC, 2007). Magan et al. (2011) reported the effect of high concentrations on growth, which may not be relevant to the low levels from CC. However, the increase in CO2 is predicted to increase the metabolism of crops providing higher yields. Increased stomata closure will be associated, inevitably, with lower latent heat loss, thereby increasing leaf temperatures and affecting which fungi infect the plant and how (DaMatta et al., 2010; Paterson and Lima, 2010).

Based on the present available data, atmospheric concentrations of CO2 are expected to double or triple (from 350–400 to 800–1,200 ppb) in the next 25 to 50 years. As such, different regions in Europe mentioned previously will be impacted by the increases in temperature of 2–5° C coupled with elevated CO2 (80–1,200 ppm) and drought episodes. This will have a profound impact on pests and diseases and, ultimately, yields (Gregory et al., 2009; Bebber et al., 2013, 2014; Bebber and Gurr, 2015). Similar impacts have been predicted in other areas of the world, especially parts of Asia and Central and South America, which are important producers of wheat, maize and soya beans for food and feed uses on a global basis (IPCC, 2013).

5. Parasites lost

The “parasites lost” phenomenon may occur as crops are moved to new growing regions. Such crops often thrive, with increases in body mass and spread, thanks to the loss of their associated pests, resulting in a potential advantage in terms of fungi and mycotoxins. The introduced plant may experience the “enemy release” phenomenon that has been hypothesized, resulting in reduced natural enemy attacks. For example, 473 plant species naturalized to the United States from Europe had, on average, 84% fewer fungi infecting each plant species. The results indicated that the impact of invasive plants may be a function of release from and, in a few cases, the accumulation of natural enemies, including pathogens (Mitchell and Power, 2003).

6. The climate-change mycotoxin cycle

This novel concept considers how CC could activate the “furnace of evolutionary change”. Paterson (2008) and Paterson and Lima (2009) discuss how mutagens produced during the culturing of fungi may exert changes in the structure of DNA (e.g., mutations), affecting diagnostic methods and phylogenetic schemes. The possibility of increased mutations in fungi from CC is mentioned by Paterson and Lima (2010), and the emergence of disease includes the evolution of new microbes (Olival and Daszak, 2005). Many mycotoxins are mutagenic and are well-known as a source of mutation in the environment. CC may result in increased amounts and different types of mutagenic mycotoxins in crops, which could lead to mutated strains of fungi that are also capable of producing mutagenic mycotoxins, and so on, in a cyclical manner. The increase in UV radiation from CC-related temperature increases will also increase mutations.

7. Amelioration strategy

Speijers et al. (2010) mention that good agricultural practices (GAP) and good manufacturing practices are useful to implement for the control of mycotoxins. Preventative and corrective measures include GAP, plant breeding and detoxification. Hazard Analysis and Critical Control Point schemes for mycotoxin control need to be further introduced. The introduction of genetically modified (GM) crops could be considered. Training and capacity-building, with respect to mycotoxins, must be improved, especially in developing countries. It is recommended that in regions where more crops will be grown as a result of CC, mycotoxin analyses should be maintained at a sufficiently high level and, where fewer crops are grown, adequate levels of analyses should remain. Changing cropping patterns, aflatoxin management technologies and detoxification can all be considered (Magan et al., 2003) to avoid future exposure.

The Green Deal and mycotoxins

The recently launched Green Deal is the European Union’s plan to make the EU’s economy more sustainable, with the goal of becoming climate-neutral by 2050. Within this, governments will take ownership of their country-based targets for reducing greenhouse gas emissions and will work with the industry to achieve these, with a requirement that levels must be measured, verified and reported. This initiative will force the agriculture industry to focus on environmental sustainability in order for countries to meet their goals. Emphasizing the changing landscape, up to 40% of the Common Agriculture Policy (CAP) funding will support these aims moving forward.

Are mycotoxins a big deal within this?

Jouany (2007) described various pre- and post-harvest factors that will ultimately influence the level of mycotoxins in the final finished feed. Of the pre-harvest strategies — including seed variety, tillage methods, crop rotation and pesticide usage — all are known to affect the level of mycotoxin contamination in the next crop. Given the plans in the Green Deal to increase carbon capture through more ecologically friendly tillage practices and reductions in chemical use, the number of pre-harvest management strategies that help to decrease the mycotoxin risk will be reduced or removed from the farmer’s toolbox.

Therefore, it is difficult to predict, with any great certainty, exactly what the mycotoxin levels will be in the future — although, as noted above, changing weather patterns and agricultural practices do have the potential to increase the risk. As Jouany reflected, and as remains the case today, there is no one strategy that will render feed free of mycotoxins. Given the changing landscape, both from an environmental point of view but also, in the future, from a legislative point of view, it is inevitable that producers will have to adapt their businesses.

Novel methods for a mycotoxin management program

There have been positive developments, from biopesticides and biostimulants (Lagogianni and Tsitsigiannis, 2019) to competitive exclusion strategies using nontoxigenic strains of Aspergillus molds (Pitt, 2019). While these methods are not perfect, they do offer positive tools for the control of aflatoxin, which is of particular concern from a food safety and security standpoint (Medina et al., 2017).

Other post-harvest concepts include grain cleaning and processing, which has different connotations depending on the exact nature of the grain, mycotoxin and processing step. Generally speaking, processing steps — such as sieving, cleaning, thermal treatment and others — can positively affect the level of mycotoxins. Still, the outcomes vary and do not result in mycotoxin-free grains (Colovic et al., 2019).

In this area, Alltech continues to innovate via technologies that can help producers, both pre- and post-harvest. Alltech Crop Science products offer grain producers chemical-free alternatives to managing pests and improving crop health to help reduce the fungal load and mycotoxin contamination. Post-harvest, Alltech’s Mycosorb® product range offers livestock producers different solutions based on the species and mycotoxin risk, assisted by the Alltech® 37+ and Alltech® RAPIREAD™ analytical programs. A recent meta-analysis of published studies in which Mycosorb® was fed to laying hens consuming diets with and without mycotoxins demonstrated that the contribution that Mycosorb® makes to environmental sustainability is also significant, as calculated by Alltech® E-CO2. Based on the increased performance as a result of feeding Mycosorb®, it found that for every 100,000 layers, Mycosorb® helped reduce the overall carbon footprint by 3.76%, which is equal to the impact of removing 124 cars from the road, grounding 221 round round-trip transatlantic flights or planting 190 trees.

Conclusion and Planet of Plenty™

Mycotoxins are unavoidable, naturally occurring compounds in the field, because the fungi that produce them are common components of the epiphytic and endophytic microflora in staple crops. As a result of global warming and other changes in climate, some crops, such as maize, and mycotoxigenic fungi, like A. flavus, might change their geographic distribution, which would determine a greater presence of the mycotoxins they produce in other latitudes. Global warming and drought conditions could also favor the infection of crops by A. flavus in certain regions and could increase the risk of aflatoxin formation in the field. Elevated CO2 levels are likely to further contribute to increased mycotoxin production in crops infected by Aspergillus and Fusarium species by enhancing fungal colonization. Recent quantitative estimations have shown that increased DON and aflatoxin B1 contamination is expected in cereals in certain regions of Europe as a result of global warming.

To better align with the focus of the UN’s Sustainable Development Goals, as well as the push toward climate neutrality, Alltech officially launched its Planet of Plenty™ initiative in May 2019. While this program covers many different aspects, the work carried out by the Alltech® Mycotoxin Management platform and Alltech Crop Science specifically focuses on the reduction of mycotoxins in finished feed and their impact on animal health, performance and profitability, subsequently helping the global agricultural industry work toward a Planet of Plenty™.

*References available on request.