Ergot in Canadian cereals – relevance, occurrence, and current status

Abstract

Ergot is a fungal disease that occurs on cereals and grasses, including rye, oat, wheat, and barley. The ergot pathogen, Claviceps purpurea, infects the floret, and as infection progresses, it replaces individual kernels, appearing on the head as darkly coloured fungal bodies called sclerotia. Ergot is a grain-grading factor in Canada and can affect grain quality and value, as well as safety due to production of ergot alkaloids. Testing of durum fortified with ergot sclerotia showed that the presence of sclerotia resulted in black specks in semolina and pasta, but had no impact on milling performance or end-product quality. Surveillance performed as part of the Canadian Grain Commission’s annual Harvest Sample and Cargo Monitoring Programs provided insights into ergot incidence and severity in different grains, growing locations, and years, as well as the presence of ergot alkaloids. Analysis of more than 230 000 Harvest Sample Program grain samples from western Canada across 25 years showed the highest ergot incidence and severity occurred in rye, followed by bread and durum wheat, and then barley and oats. Ergot incidence and severity varied annually, but only incidence increased over time. Analyses of bulk grain shipments indicated that the presence of ergot alkaloids reflected the disease incidence observed in the harvest samples (median ergot alkaloid concentrations in wheat and durum > oats and barley). Data on ergot alkaloids from the Cargo Monitoring Program also showed that the Canadian bulk grain-handling system mitigated the variability in annual ergot incidence and severity observed in harvest samples.

Résumé

L’ergot est une maladie fongique qui s’attaque aux céréales et aux graminées, y compris le seigle, l’avoine, le blé et l’orge. L’agent pathogène, Claviceps purpurea, infecte la florule et, à mesure que l’infection progresse, il remplace chaque grain qui se forme sur l’épi par des organes fongiques foncés appelés sclérotes. Au Canada, l’ergot est un facteur de classement des grains et peut influencer leur qualité et leur valeur. Il constitue également un risque pour la santé à cause des alcaloïdes qu’il produit. Des tests effectués sur du blé dur enrichi de sclérotes d’ergot ont montré que ces derniers se sont retrouvés dans la semoule et les pâtes sous forme de mouchetures noires, mais qu’ils n’avaient aucun effet sur le rendement de la mouture ni sur la qualité des produits finis. La surveillance découlant du Programme d’échantillons de récolte de la Commission canadienne des grains et du Programme de surveillance de la qualité des cargaisons a fourni des indications sur l’incidence et la gravité de l’ergot chez différents grains, dans diverses régions de production et au fil des années, de même que sur la teneur en alcaloïdes de l’ergot. L’analyse, menée sur 25 années, de plus de 230 000 échantillons de grains de l’Ouest canadien issus du Programme d’échantillons de récolte a démontré que l’incidence et la gravité les plus élevées d’ergot se produisaient sur le seigle, suivi des blés tendre et dur, puis de l’orge et de l’avoine. L’incidence et la gravité de l’ergot ont varié annuellement, mais seule l’incidence s’est accrue au fil du temps. Les analyses des expéditions en vrac de céréales ont indiqué que la présence de l’ergot reflétait l’incidence de la maladie observée dans les échantillons de récolte (concentrations moyennes d’alcaloïdes d’ergot dans les blés tendre et dur > avoine et orge). Les données sur les alcaloïdes de l’ergot issues du Programme de surveillance de la qualité des cargaisons ont également montré que le système canadien de manutention des grains en vrac a réduit la variabilité de l’incidence et de la gravité annuelles de l’ergot observée dans les échantillons de récolte.

Keywords:

• cereals
• Claviceps purpurea
• ergot
• geographical distribution
• prairies

Mots clés:

• Claviceps purpurea
• céréales
• ergot
• répartition géographique
• prairies

Introduction

Ergot is a fungal disease of grasses, including cereals, and is caused by fungi in the Claviceps genus. Surveillance of ergot in Canada has identified several different fungal species that cause the disease (Liu et al. 2020), with the most common being Claviceps purpurea (Fr.) Tul. The pathogen C. purpurea is a homothallic ascomycete fungus, whose windborne ascospores infect the florets of susceptible hosts (Tenberge 1999). The species has been subdivided into several different lineages with different host ranges, with some lineages being capable of causing disease on many different cultivated and uncultivated grass hosts (Shoukouhi et al. 2019). Variation in disease resistance has also been observed across different grass species, with rye being particularly susceptible to disease and having higher reports of ergot toxins than other cereals (Scott et al. 1992; Tittlemier et al. 2015). Within cereal species, there is also variation in the levels of susceptibility across cultivars, indicating the potential to mitigate the disease through breeding (Menzies 2004). However, increases in fungal disease pressure are predicted as our cereal production systems intensify to meet the needs of a rising global population, and due to changes in environmental and climatic conditions.

Ergot is conspicuously present as dark-coloured bodies (ergot sclerotia) on plant spikes. These sclerotia develop in place of healthy kernels and lend the disease its name based on their physical similarity to cock’s spurs – ‘argot’ in French (Haarmann et al. 2009). During the disease cycle, ergot sclerotia germinate when soil moisture and temperature conditions facilitate release of wind-dispersed ascospores that infect florets during flowering. During the infection process, the ergot pathogen produces masses of conidia in a sugary matrix that results in material known as ‘honeydew’, which is exuded from infected florets. The conidia in the honeydew are then spread by rain splash and insects, resulting in secondary infections including movement from infected grasses to adjacent cereal crops. Ergot sclerotia develop from the infected florets during the growing season replacing kernels, and eventually fall down to the soil surface, and overwinter in the field, becoming a new source of ascospores the next year (Menzies and Turkington 2015). Sclerotia can also be collected along with healthy grain during the harvesting process.

Ergot is broadly distributed across North America (Bailey et al. 2003; Menzies and Turkington 2015; Tittlemier et al. 2015), South America (Piñeiro et al. 1996), Europe (Appelt et al. 2009; Orlando et al. 2017; Topi et al. 2017), Africa (Naudè et al. 2005), Asia (Blaney et al. 2006), and Australia (Bandyopadhyay et al. 1998; Blaney et al. 2009), and has been occurring since the Middle Ages (Haarmann et al. 2009; Ramos et al. 2011; Belser-Ehrlich et al. 2012) and potentially earlier (Schiff et al. 2006; Pitt and Miller 2017).

Cereal grain yield can be reduced due to the development of ergot sclerotia in place of healthy kernels. Harper and Seaman (1980b) studied the impact of ergot on yield losses for rye produced in Alberta in the mid 1970s. They reported a yield loss of 32% due to a lower number of healthy kernels on infected spikes combined with a lower weight of healthy kernels on infected spikes, as compared with uninfected spikes. Extrapolating these data to the field scale, rye crops with 0.5–3.3% infected spikes were estimated to have a 0.16–1.1% reduction in grain yield. Ponomareva et al. (2016) noted that the presence of 1 to 6 sclerotia on rye spikes reduced the amount of grain by 19–51%, as compared with healthy spikes on winter rye in central Russia.

One of the major concerns regarding ergot is the production of toxins by the fungus. Ergot alkaloids are secondary metabolites produced by C. purpurea, and share a common structural feature of a tetracyclic indole-quinoline ring system. Ergot alkaloids are present at concentrations in the parts per billion range in honeydew (Tittlemier et al. 2016) and the parts per million range in sclerotia (Appelt and Ellner 2009; Tittlemier et al. 2016; Orlando et al. 2017). The biosynthesis of ergot alkaloids, including the evolution of the genes involved, is well summarized by Florea et al. (2017).

Consumption of ergot alkaloid-contaminated grain in foods has caused ‘ergotism’, which is characterized by swelling of extremities, burning pain, and potential loss of limbs, as well as hallucinations, delirium, muscle spasms, and convulsions (Schiff 2006; Pitt and Miller 2017). With increased knowledge and vigilance in food safety in many areas, ergotism has become more of a livestock feed issue, but still affected lower socioeconomic populations in south Asia and northern Africa in the late twentieth century (Belser-Ehrlich et al. 2012). In animals, consumption of ergot alkaloid-contaminated feed has led to reduced growth, disruptions in milk production in cattle, circulatory issues that led to gangrene, as well as hyperthermia (Naudè et al. 2005; Belser-Ehrlich et al. 2012; Riet-Correa et al. 2013; Coufal-Majewski et al. 2016). In Canada, cases of ergotism due to contaminated livestock feed have been reported as recently as 2013 (Rance 2014).

Ergot also affects grain quality and functionality; the main impact on quality relates to colour and the presence of dark specks in grain products. Shuey et al. (1975) reported that the amount of white flour that was obtained from wheat during milling was reduced with an increase in the amount of ergot sclerotia present. They also noted changes in bread colour occurring with an increase in ergot sclerotia in wheat.

In Canada, ergot occurs in cereal crops including rye, barley, oats, bread wheat, durum wheat, and canary seed (Bailey et al. 2003; Menzies and Turkington 2015; Cholango-Martinez et al. 2019). These crops contribute significantly to the caloric and protein intake of humans and livestock; therefore, there is much interest in understanding the occurrence of ergot in Canada. In the Canadian grain handling system, the presence of ergot sclerotia is a grading factor (Canadian Grain Commission 2021) and is evaluated alongside other factors for a holistic assessment of grain quality.

Temporal and geospatial variation of ergot in Canada has been reported in the 1950s (Conners 1955) and 1970s (Harper and Seaman 1980a), but there has been recent interest in disease monitoring and research due to outbreaks beginning in the late 1990s (Menzies and Turkington 2015). Most studies on ergot were narrow in scope, with a limited number of samples, years, locations, or crop species examined. For several decades, the Canadian Grain Commission’s Harvest Sample Program and Cargo Monitoring Program have been gathering data on ergot and ergot alkaloids in cereal grains from across Canada. In this paper, we use data from these programs to describe trends in ergot incidence, severity, and ergot alkaloid presence across years and locations in Canada. Complementary research is also presented to provide insights into the effects of ergot sclerotia on quality of grain-based products.

Materials and methods

Ergot incidence and severity from 1995 to 2020, Canadian Grain Commission’s Harvest Sample Program

Harvest samples of hexaploid or bread wheat, tetraploid or Canada Western Amber Durum wheat (CWAD), rye, oats, and barley from across Canada were received from 1995 to 2020 as part of the annual Harvest Sample Program (Canadian Grain Commission 2022a). The Harvest Sample Program relies on voluntarily submitted representative grain samples from producers. Samples weighing approximately 800 g were manually inspected for the presence of ergot sclerotia. The presence/absence and percentage (on a mass basis) of ergot sclerotia in each sample was recorded. Ergot incidence was calculated as a ratio of the samples with presence of measurable levels of ergot to the total number of samples submitted in each Canadian province studied, as well as the crop districts within the provinces of Alberta, Saskatchewan, and Manitoba. Ergot severity was determined as the percentage by mass of ergot in each sample with measurable levels of ergot sclerotia.

Evaluation of the affects of ergot sclerotia on the quality of food products

To investigate the affect of ergot sclerotia on semolina speck count, a No. 1 Canadian Western Amber Durum (CWAD) wheat sample was spiked with ergot sclerotia at levels of 0.01, 0.02, 0.03, 0.04, and 0.1% (m/m). The fortified durum samples were then milled into semolina in duplicate (2.0 kg × 2) on a four-stand Allis-Chalmers laboratory mill in conjunction with a laboratory purifier following the mill flow previously described by Dexter et al. (1990). Semolina granules were prepared by adding the most refined flour stream(s) to semolina until 70% extraction was reached. Black specks in semolina were measured with RAR-SpecCnt(S) software developed by RAR Software Systems (Winnipeg, Manitoba). A semolina sample was compressed to a layer 1.0 cm in thickness in a sample holder with a glass top, and then scanned using a flatbed scanner to acquire a 10 cm × 10 cm image for processing. The image was used to identify potential black specks within the sample using object detection algorithms. Each detected object was then evaluated for the average darkness (% GL), the average colour of each component (% RGB), the average colour of each component within the darkest region of the object (% RGB Max), and the size (total area). The analysis was conducted on three or more scanned surfaces for each sample and black speck numbers were averaged and expressed as the number in 50 cm² of semolina surface.

Spaghetti was produced from each semolina sample in duplicate using a customized micro-extruder (Randcastle Extrusion Systems Inc., Cedar Grove, NJ) following Fu et al. (2013). Semolina was mixed with water in a high-speed asymmetric centrifugal mixer (DAC 400 FVZ SpeedMixer, FlackTec, Landum, SC) at constant water absorption of 31%. Vacuum was applied to eliminate the introduction of air bubbles and minimize oxidative degradation of yellow pigment, after which the dough crumbs were extruded through a four-hole Teflon-coated spaghetti die (1.8 mm). The fresh pasta was subsequently dried in a pilot pasta dryer (Bühler, Uzwil, Switzerland) coupled with a 325 min drying cycle and a maximum temperature of 85°C. For capturing pasta images and speck count, a 6.5 cm band of spaghetti strands was mounted on white cardboard using double-sided tape. The protocol used to identify the dark specks in the spaghetti strands was the same as described above.

Analysis of ergot alkaloids in cereals

Twelve ergot alkaloids (ergotamine, ergotaminine, ergocornine, ergocorninine, ergocryptine, ergocryptinine, ergocristine, ergocristinine, ergonovine, ergonovinine, ergosine, ergosinine) were analyzed in samples representing bulk wheat, durum, barley, and oat shipments exported between August 1, 2013 and July 31, 2020. Export shipments were sampled and prepared as described by Tittlemier et al. (2012, 2014). Ergot alkaloid analysis was performed using liquid chromatography with tandem mass spectrometry as described in Tittlemier et al. (2015), with minor adjustments to the method to include ergotaminine and ergonovinine. The minor adjustments were addition of pairs of transitions for ergotaminine (m/z 582.351 → 223.04, 582.351 → 297.117) and ergonovinine (m/z 326.032 → 207.963, 326.032 → 223.071), with the quantitation transition listed first, followed by the qualification transition.

In-house durum, wheat, and rye reference materials, as well as grain previously analyzed and found to be free of measurable amounts of ergot alkaloids, were used throughout ergot alkaloid monitoring to ensure accurate and precise analytical method performance over the multiple years of monitoring. In addition, the analytical method produced results that met the passing criteria for six independent wheat and rye proficiency tests between 2016 and 2021.

Results and discussion

Ergot incidence and severity vary in cereals by grain type and year

With a dataset derived from more than 230,000 grain samples across a 25-year period, this study presents the most robust survey of ergot in Canadian grain. The methods of sample collection, inspection, and recording have not changed over the course of the survey, although it is unclear if any of these changes would have impacted the findings of the survey. The majority of the data correspond to bread wheat and durum wheat, which similar to rye, has data for most years dating back to 1995 (Fig. 1). Data for barley is mostly from after 2010, while there were only two recent years of data for oat. Overall, the data indicate that the incidence of ergot in Canadian grain was variable between grain type and across years.

Fig. 1 Trends in annual ergot incidence (% of samples inspected in a year that contained ergot sclerotia) from 1995 to 2020 for Canadian cereal samples submitted to the Canadian Grain Commission Harvest Sample Program (Canadian Grain Commission 2022a).

Ergot incidence was greater in rye than in wheat, barley, or oat (Fig. 1) for all years. The severity of ergot within samples was also greatest in rye, with a median of 0.08% (Table 1). The increased levels of ergot observed in rye when compared with other cereals are consistent with previous reports of increased ergot susceptibility in rye (Menzies and Turkington 2015). The incidence of ergot in rye was greatest in 2013 and remained at or above 50% in all subsequent years (Fig. 1).

Table 1. Comparison of annual ergot incidence (% of samples inspected in a year that contained ergot sclerotia) and median severity (% mass sclerotia/mass sample inspected) between the two time periods of 1995–2009 and 2010–2020 for Canadian cereal samples submitted to the Canadian Grain Commission Harvest Sample Program (2022a).

Crop	Total N samples	1995–2009			2010–2020
		N samples	Ergot incidence (%)	Median ergot severity (%)	N samples	Ergot incidence (%)	Median ergot severity (%)
Bread wheat	177,831	117,557	4.2	0.02	60,274	19.5	0.02
Durum wheat	46,489	32,166	2.9	0.02	14,323	13.1	0.02
Barley	4,470	394	0.3	-	4,076	2.4	0.02
Rye	803	547	27.6	0.08	256	65.6	0.08
Oat	421	-	-	-	421	0.7	0.01

The incidence of ergot in wheat remained low prior to 2008, with the most significant event being a minor outbreak in 1999 of 9.8% and 3.9% incidence in bread and durum wheat, respectively. An outbreak in 1999 is consistent with outbreaks reported in other studies (Menzies and Turkington 2015). In 2008, there was an increase in incidence to 13.1% and 13.9% for bread and durum wheat, respectively (Fig. 2). The incidence levels in wheat remained variable after 2008, with a significant decrease in 2014 to 5.8% for bread wheat and 2.7% for durum wheat, but then increased to the highest observed levels during the study period of 28.7% for bread wheat in 2020 and 26.7% for durum wheat in 2016. In Canada, weather conditions prior to harvest in 2016 were wet and humid, especially during the key period for infection in late June and early July, which likely favoured sclerotial germination, production of fruiting structures and ascospores, and subsequent host infection and disease development. The year 2016 also corresponded with an epidemic year for another fungal disease, Fusarium head blight (Haile et al. 2019; Canadian Grain Commission 2022b). The patterns of ergot incidence were similar between bread and durum wheat, except in 2010 and 2017, when the incidence in durum wheat was noticeably lower than in bread wheat (Fig. 2). Additional research is required to clarify if these differences resulted from host resistance or the broader production area of bread wheat in regions that experienced increased moisture in both years, especially in 2017 (Agriculture and Agri-Food Canada 2020). The median severity of ergot within grain samples was also the same for both bread and durum wheat at 0.02% (Table 1 and Fig. 2).

Fig. 2 Annual distribution of ergot severity (% mass sclerotia/mass sample inspected) in durum wheat (a) and bread wheat (b) samples submitted to the Canadian Grain Commission Harvest Sample Program (Canadian Grain Commission 2022a). Annual incidence for a particular severity was determined as the percentage of samples inspected that contained ergot sclerotia in one year.

Variation was observed in the level of ergot in durum wheat by province and year, with a trend of increased incidence in recent years (Fig. 3a). In Alberta and Saskatchewan, lower levels of ergot in durum wheat were observed prior to 2008. Alberta experienced peaks of ergot incidence in 2013 (40.5%) and in 2016 (40.2%). Saskatchewan, which is where most Canadian durum is grown, also exhibited a higher incidence in 2016 (22.3%) and 2020 (20.6%), although these peaks are lower than those that were observed in Alberta. Durum wheat samples from Manitoba, which typically experiences increased moisture compared with Saskatchewan and Alberta, showed the greatest incidence of ergot in 2001 at 12.2%. However, durum production in Manitoba declined in the late 2000s, likely due to the combination of increased disease pressure from Fusarium head blight in their more moist growing conditions and the adoption of more diverse crops such as soybeans and pulses (Haile et al. 2019).

Fig. 3 Provincial and temporal trends of annual ergot incidence (% of samples inspected in a year that contained ergot sclerotia) in durum wheat (a) and bread wheat (b) samples submitted to the Canadian Grain Commission Harvest Sample Program (Canadian Grain Commission 2022a).

Bread wheat has a much broader production area than durum wheat. Spring wheat is grown throughout the Prairie Provinces and in the Peace River region of British Columbia. Similar to durum wheat, ergot incidence in bread wheat was variable across years and regions, with greater incidence in recent years (Fig. 3b). The highest levels of ergot incidence in British Columbia for bread wheat were observed in 2018, at 19.6%. Alberta had the greatest levels of ergot incidence in 2020, where ergot occurred in 41.8% of samples. Saskatchewan observed the greatest incidence of the disease in 2011, at 25.6%. The greatest level of ergot incidence in Manitoba was 30.7% in 2015. When subdividing the Prairie Provinces into crop districts (Fig. 4a), variation in ergot incidence was also observed within provinces (Fig. 4b). In some years, regional variation was prominent; for example, in 2020 District 1A in Saskatchewan had an incidence of 59.6%, while other districts had no incidences of ergot. This is in contrast with other years, such as 2011, in which the incidence of ergot was distributed more broadly across all districts in Saskatchewan. Similarly, in years of high incidence, such as in Alberta in 2013, ergot was not restricted to a particular crop district, but there was some regional variation ranging from 32.9% in District 7 to 59.2% in District 6. Altogether, ergot appears to be distributed broadly across western Canadian provinces and crop districts within provinces, particularly in years of high incidence.

Fig. 4 Annual ergot incidence (% of samples inspected in a year that contained ergot sclerotia) in bread wheat samples submitted to the Canadian Grain Commission Harvest Sample Program (Canadian Grain Commission 2022a) across crop districts within western Canadian provinces from 1995 to 2020. Provinces and crop districts (a) were analyzed separately for ergot incidence (%) for each crop year (b). Note that there were no data for crop district 10 in Manitoba.

In contrast to rye and wheat, both barley and oats did not have a significant incidence of ergot. From 1995 to 2009, only one of 394 barley samples, or 0.3%, had an incidence of ergot. The greatest incidence of ergot in barley was in 2012 at 5.2%. Similarly, levels in oat were low, 0.6% in 2017 and 0.7% in 2019. The median severity of ergot in barley and oat also remained low at 0.02% and 0.01%, respectively (Table 1).

While variable across years, there is a noticeable pattern of increased ergot incidence in the last decade. When comparing the periods of 1995–2009 and 2010–2020, rye, bread wheat, and durum wheat all showed an increase in ergot incidence. However, the median severity of ergot did not change between these periods, suggesting that the increase in the number of samples containing ergot did not translate into a corresponding increase in ergot sclerotia within samples (Table 1 and Fig. 1).

Impacts of ergot on grain value

The affect of ergot on grain quality and safety is largely controlled through grain grading and regulations around the allowable limits of the number of ergot sclerotia in grain. In Canada, ergot is visually assessed on a percentage mass basis by inspecting a minimum of 500 g of grain for the presence of fragments and whole ergot sclerotia (Canadian Grain Commission 2021). Current tolerances for ergot in selected Canadian cereals are provided in Table 2. Downgrading of cereal grain due to the presence of ergot sclerotia in grain in excess of tolerances will result in loss of value for producers. The economic impact to producers from downgrading of rye due to ergot was estimated to be a 3.5–18% reduction in selling price for grain from fields with ergot infection levels (percentage of infected spikes) of 0.5–3.3% (Harper and Seaman 1980b). Harper and Seaman used disease survey data from 1972 to 1976 (Harper and Seaman 1980a) to estimate downgrading and better assess the realistic economic impact for producers. Based on the low percentage (2.35%) of rye that would have been downgraded due to ergot in 1972, the estimated relative loss in value for producers was 0.08%. While the grain-grading system results in a financial penalty to producers, it is important to ensure that ergot levels remain within allowable levels for domestic and export food and feed markets.

Table 2. Current tolerances for ergot (% m/m) in selected Canadian cereal grains (Canadian Grain Commission 2021).

Grade	Canada Western Red Spring wheat	Canada Western Amber Durum wheat	Canada Eastern Soft Red Winter wheat	Rye	Barley	Oats
No. 1	0.04	0.02	0.04	0.05	0.02b	0.00
No. 2	0.04	0.02	0.04	0.20	-	0.03
No. 3	0.04	0.04	0.04	0.33	-	0.03
No. 4	-^a	0.04	0.10	-	-	0.05
No. 5	-	0.10	-	-	-	-
Feed	0.10	-	-	-	-	-

^aGrade is not relevant for that particular cereal grain.

^bApplies to Select Malting Canada Western/Canada Eastern two-row and six-row barley, including hulless barley grades.

Other jurisdictions have tolerances set for ergot sclerotia in cereals grains (Table 3). These tolerances influence grain handling, as exporters manage their grain stocks to ensure that shipments of Canadian grain to international customers meet the relevant ergot tolerances while meeting various quality specifications at the same time. Based on our monitoring data (Table 1), when ergot occurs in harvest samples of barley, durum wheat, and bread wheat, the median severity is 0.02%, which is below the limits set by Codex Alimentarius (Codex Alimentarius Commission 1995, 2019), the United States of America (USA; United States Department of Agriculture 2021), and the European Union (EU, EC 2021) (Table 3). This also falls within the limits of the Grade No. 1 crop, which would not result in a grading penalty to producers. For bread and durum wheat, very few grain samples (typically less than 5%) had a severity greater than 0.04 or 0.05%, which would result in downgrading to Grade No. 5 or feed (Fig. 1). Similarly, median severity in Canadian oat was 0.01%, which is below set limits for safety and trade, but above the limits for Grade No. 1 and would result in a downgrade to Grade No. 2 (Table 2). However, only 0.7% of oat samples were affected by this downgrade (Table 1). While median severity in rye is higher at 0.08%, this is still within the limits of the USA (United States Department of Agriculture 2021), but above the limits for the EU (EC 2021) and would result in a downgrade of most infected rye samples to Grade No. 2 (Table 2).

Table 3. Current international tolerances for ergot (% m/m) in cereal grains.

Grain	Codex^a	United States^b	European Union^c
Wheat	0.05	0.05	0.02
Durum	0.5	0.05	0.02
Rye	-^d	0.30	0.05
Barley	0.02	0.10	0.02
Oats	0.05	0.10	0.02

^aCodex Alimentarius Commission (1995) and World Food Program 2014 (2019).

^bUnited States Department of Agriculture (2021).

^cEU (2021).

^dNo tolerance has been set.

Ergot alkaloids in Canadian cereals

Analysis of ergot alkaloids in Canadian cereal grain, as represented by bulk shipments, reflected the relative presence of ergot observed in harvest samples (Table 1). With respect to the cereal grains exported in bulk between August 1, 2013, and July 31, 2020 (Table 4), ergot alkaloids were measured most frequently in durum (97% of shipments) and wheat (88%), followed by barley (60%) and oats (22%). Ergot sclerotia were observed in 13% and 20% of durum and wheat harvest samples, respectively, followed by barley (2.4%) and oats (0.7%).The more frequent occurrence of ergot alkaloids as compared with ergot sclerotia is likely a combination of different factors. The nature of the Canadian bulk cereal grain-handling system leads to the moderation of factors that vary in grain, such as the presence of ergot and ergot alkaloids. During handling, grain from different growing locations, as well as different years, can be combined to produce a volume of grain that meets particular quality and safety benchmarks. Such compositing of grain from harvest, through handling and blending, to a final product for export, will moderate the low and high concentrations that could be present in grain at the beginning of the grain-handling chain. In addition, handling and moving grain can break up ergot sclerotia, or create dust from abrasion, which distributes ergot alkaloids through a wider volume of grain (Franzmann et al. 2011).

Table 4. Sum of 12 ergot alkaloids (ΣEA₁₂) in all grades of bulk cereal grain shipments, exported between 2013 and 2020.

Grain	N cargos (all grades)	% > Limit of quantitation	Median ΣEA12 (mg/kg)	Range ΣEA12 (mg/kg)
Wheat	394	88	0.161	<0.01–0.666
Durum	159	97	0.183	<0.01–1.013
Barley	83	60	0.019	<0.01–0.532
Oats	58	22	<0.01	<0.01–0.224

However, the year-to-year variation in ergot incidence is not reflected in the ergot alkaloid concentrations in durum and red spring wheat bulk shipments (Fig. 5). Over the years, the frequency of ergot incidence in harvest samples varied by factors of approximately five and 10 for Canada Western Red Spring (CWRS) and CWAD wheat, respectively. The annual median sum total concentrations of 12 ergot alkaloids varied by factors of approximately only two and three for CWRS and CWAD wheat, respectively (Fig. 5). The visual trends in ergot incidence observed in Fig. 5 are not reflected in the sum total ergot alkaloid concentrations, suggesting that the handling that occurs over the grain value chain is moderating ergot alkaloid concentrations and mitigates the year-to-year variability in growing conditions that affect the presence of ergot.

Fig. 5 Year-to-year variation in the sum of 12 ergot alkaloids in bulk grain shipments (box and whisper plot; boxes represent 25–75th percentiles; whiskers represent 10–90th percentiles; centre line represents median) and frequency of ergot occurrence in harvest samples (line plot).

As discussed above, many jurisdictions have set tolerances for the presence of ergot sclerotia in grain. The only regulations on ergot alkaloids have recently been adopted by the EC (2021). These maximum limits restrict total concentrations of the commonly analyzed 12 ergot alkaloids in cereal milling products to 50–500 μg kg⁻¹, depending on the specific cereal grain, as well as limit the sum of the 12 ergot alkaloids to 20 μg kg⁻¹ in processed cereal-based foods for infants and young children (EC 2021).

These maximum limits for grain-based products do not apply to the bulk raw grain analyzed in this study, where the median concentrations of the sum of 12 ergot alkaloids ranged from <0.01 mg kg⁻¹ to 1.01 mg kg⁻¹ (Fig. 5). Based on previous research, it is expected that cleaning processes used in milling facilities as well as the milling process itself will reduce the amount of ergot alkaloids in milling products and grain-based foods (Fajardo et al. 1995; Franzmann et al. 2011; Tittlemier et al. 2019).

Ergot can affect visual quality

Figure 6 shows the presence of black specks in semolina, a granular product comprised starchy endosperm particles produced by milling CWAD containing varying amounts of ergot sclerotia. The presence of the black specks carried over into dried pasta prepared from the semolina (Fig. 6). The results demonstrate that increasing the amount of ergot sclerotia in durum results in a corresponding increase in the number of black specks that appear in semolina and pasta samples. Black speck counts in semolina increased from 2 to 11 per 50 cm² from the CWAD containing 0.01% ergot sclerotia to the CWAD test material containing 0.1% ergot sclerotia (Table 5). The scanned images of dried spaghetti showed black specks present both on the surface and inside the strands due to the translucent nature of the product. Therefore, it was impossible to count the number of black specks present on the surface of dried pasta only with the RAR-SpecCnt(S) software.

Table 5. Impact of varying ergot sclerotia content (% mass/mass basis) on Canada Western Amber Durum (CWAD) semolina speck counts in dried pasta.

CWAD test material	Mean number of black specks (per 50 cm^2)
0% ergot (cleaned No. 1 CWAD)	0.67 ± 0.58
0.01% ergot	1.67 ± 0.58
0.02% ergot	2.67 ± 0.58
0.03% ergot	4.00 ± 1.00
0.04% ergot	4.33 ± 1.15
0.1% ergot	10.67 ± 1.15

Fig. 6 Occurrence of dark specks (circles) in semolina (top row or a–c) and pasta (bottom row or d–f) due to the presence of varying amounts (% mass/mass) of ergot sclerotia in durum.

Consumer preference for high-quality pasta and couscous made from durum semolina is attributed to product appearance, which includes a bright yellow colour with little contaminating dark specks. Speck counting is often a mandatory quality control parameter, which ensures that the semolina meets customer specifications. Discoloured or diseased kernels resulting from smudge and black point as well as ergot, are largely responsible for the black specks and overall speck counts. The physical presence of the dark-coloured sclerotia, if not removed before milling, can negatively influence consumers’ acceptance of semolina and finished products. Other than the elevation in number of black specks in semolina and pasta, the addition of ergot sclerotia up to 0.1% level had no impact on durum wheat milling performance, semolina and dough characteristics, and pasta colour and texture (data not shown).

The impact of ergot sclerotia presence on semolina and pasta in this paper is similar to what has been reported by Shuey et al. (1975) for bread making. They reported that there was no notable change to physical dough nor baking properties in wheat fortified with ergot sclerotia, but that changes in the colour of bread loaf interiors occurred with an increase in ergot sclerotia in source wheat. Thus, while grain contaminated with ergot can be processed into food products, the milled grain and final grain products will have characteristics that are undesirable to consumers, such as discolouration and the presence of dark specks.

Conclusions

The incidence of ergot in Canada prior to 2008 remained low in barley, oat, and wheat, but has since increased. However, severity has not increased and harvested grain usually meets the ergot targets of the grain marketplace, with limited impact on the grain grade. In cases where grain has higher severity, the safeguards of the grain grading and handling system are effective at ensuring that any grain above the tolerances is identified and managed accordingly. The grain-grading system in Canada ensures that Canadian grain remains within allowable limits for ergot and that Canadian grain can be used for making high-quality and safe food products. Continued monitoring of ergot, ergot alkaloids, and the effects of ergot on grain quality are important to assess and mitigate the risks posed by ergot in our disease management and regulatory systems.

Annual differences in ergot incidence may be due to a combination of several factors, including yearly and regional variation in weather, pollen viability, as well as crop rotation and on-farm management practices. Weather, especially rainfall from mid-June to mid-July during the period influencing sclerotial germination, ascospore production and host infection. Factors influencing medium to long-term trends are more challenging, although climate variation and the increasing frequency of weather-related stress (e.g. high or low temperatures at head emergence and flowering) may be impacting pollen viability, especially in cereals such as wheat and barley (Boland et al. 2004; Menzies and Turkington 2015; Juroszek et al. 2019). Issues such as weather stress, copper and boron deficiencies, and late herbicide applications can affect pollen viability. These stresses in mainly self-pollinated cereals, such as wheat and barley, can result in a greater extent of floret opening facilitating access of ascospores to the internal flowering structures (Menzies and Turkington 2015). Long-term trends in crop rotation may also be playing a role, whereby the predominance of cereal/canola/cereal rotations would be promoting the build-up of inoculum not only within fields, but also in adjacent grassy areas (Menzies and Turkington 2015; Statistics Canada 2022). It is also unclear what the ergot-resistance profiles are among cultivars, as this resistance is not tested systematically for variety registration. Nonetheless, ergot resistance likely varies and may have changed over time.

Although this paper indicates an increasing incidence of ergot in Canada, Disease severity levels in harvest grain have remained similar. Nevertheless, ergot remains a serious issue for producers and end-use markets, and as Menzies and Turkington (2015) suggest, an integrated management approach using multiple strategies is needed. Ongoing annual monitoring initiatives such as the Harvest Sample Program (Canadian Grain Commission 2022a) and renewed consistent investment in research are needed to ensure ergot can be managed by producers and the grain-handling sector.

Acknowledgements

We would like to acknowledge the Industry Services Division of the Canadian Grain Commission for the inspection services and rating of ergot in samples from the Harvest Sample Program. We would also like to acknowledge former researchers and program managers from the Grain Research Laboratory of the Canadian Grain Commission for data collection and curation, namely Randy Clear, Tom Gräfenhan, Twylla McKendry, and Cherianne McClure.

Disclosure statement

No potential conflict of interest was reported by the author(s).