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© 2013 Plant Management Network.
Accepted for publication 3 February 2013. Published 22 May 2013.

Prevalence and Incidence of Sunflower Downy Mildew in North Dakota Between 2001 and 2011

Thomas Gulya, USDA-ARS Northern Crop Science Laboratory, Fargo, ND 58108; Hans Kandel, Department of Plant Sciences, Marcia McMullen and Janet Knodel, Department of Plant Pathology, Duane Berglund, Department of Plant Sciences, Febina Mathew and H. Arthur Lamey, Department of Plant Pathology, John Nowatzki, Department of Agricultural and Biosystems Engineering, and Samuel Markell, Department of Plant Pathology, North Dakota State University, Fargo, ND 58108

Corresponding author:Samuel Markell.

Gulya, T., Kandel, H., McMullen, M., Knodel, J., Berglund, D., Mathew, F., Lamey, H. A., Nowatzki, J., and Markell, S. 2013. Prevalence and incidence of sunflower downy mildew in North Dakota between 2001 and 2011. Online. Plant Health Progress doi:10.1094/PHP-2013-0522-01-RS.


Sunflower downy mildew, caused by Plasmopara halstedii, can be an economic problem in North Dakota, where approximately half of the United States sunflower crop is grown. Prevalence and incidence of downy mildew in North Dakota was assessed in mid-season and late-season surveys annually from 2001 to 2011. In aggregate, 2,772 fields were evaluated. Downy mildew levels fluctuated annually, and no clear connection between statewide rainfall or management tools available to growers could be made. Surveys at mid season enabled a two-fold higher detection in prevalence and incidence of downy mildew than in late-season surveys due to the disappearance of early infected plants by end of season. Both surveys identified years with relatively higher levels of downy mildew but were inconsistent when lower levels of the pathogen were recorded. The results of this study suggest that mid-season assessment of downy mildew more accurately estimates disease pressure than late-season assessment.


Sunflower (Helianthus spp.) is native to North America, but cultivated sunflowers (Helianthus annuus) only emerged as a modern field crop in the United States in the 1970s (19). Approximately one million hectares of sunflowers are planted annually in the US (18). Production is concentrated in the Great Plains states of North Dakota, South Dakota, Minnesota, Nebraska, Colorado, Kansas, and Texas, with North Dakota producing approximately 50% of the crop (2,18). Approximately 80% of the sunflowers planted in North Dakota are oilseed hybrids, while the remainder are consumed as seed (confection) (2).

Downy mildew is an economically important disease, caused by Plasmopara halstedii (Farl.) Berl and de Toni, an obligate Oomycete pathogen, which is indigenous to North America and can infect H. annuus and other Helianthus species (14). Primary infection occurs when zoospores of P. halstedii infect seedling roots, causing a systemic infection with signs and symptoms that include systemic chlorosis and prolific production of zoosporangia on leaves (Fig. 1), severe stunting (Fig. 2), post emergence damping-off, and horizontal and unproductive heads on surviving plants (4,10). Water-saturated soils soon after planting favor systemic infection by providing the environment for motile zoospores to reach seedling roots. As such, low-lying areas in fields where water collects can have a high incidence of infected plants and result in fields with large bare spots and/or areas with little to no yield (4,10). Secondary infection by airborne sporangia can cause discrete lesions on foliage (Fig. 3), but they are rarely of economic concern.


Fig. 1. Plasmopara halstedii sporulation on the underside of an infected sunflower leaf.


Fig. 2. Sunflowers systemically infected with Plasmopara halstedii (center), resulting in severe stunting; surrounded by healthy sunflowers.


Fig. 3. Secondary infection of Plasmopara halstedii resulting in discrete foliar lesions.

Management of downy mildew relies mainly on genetic resistance and fungicidal seed treatments (10). However, the variability of P. halstedii has repeatedly challenged management options. Plasmopara halstedii isolates resistant to FRAC 4 fungicides (metalaxyl and mefenoxam) were identified in the late 1990s and found to be widespread and predominant in North Dakota by the 2000s (8). Currently, only FRAC 11 seed-applied fungicides azoxystrobin (Dynasty, Syngenta Crop Protection, Greensboro, NC) and fenamidone (Idol, Bayer CropScience, Research Triangle Park, NC), are used in the US to suppress/manage downy mildew, but are considered at high risk for fungicide resistance development (17). Similarly, races of the pathogen that are virulent on the most widely used resistance genes available in commercial hybrids (Pl6 and Pl7) were identified in 2009 (7).

Since the early 2000s, prevalence and incidence of downy mildew in North Dakota sunflower production were monitored as part of two different survey efforts, namely: (i) the North Dakota State University-Integrated Pest Management (NDSU-IPM) survey, a mid-season survey whose objective is to monitor diseases and insect pests in three to five field crops (16); and (ii) the National Sunflower Association Crop Survey, a late-season survey with the objective of collecting yield and agronomic data and identifying which insect, weed, and disease problems affect production (13). The objectives of this study are to report on the prevalence and incidence of downy mildew in North Dakota between 2001 and 2011, compare results of the two surveys and discuss factors that may have influenced the occurrence of downy mildew in the past and may have effects in the future.

Mid-season Survey Methods

The Cooperative Extension Service at North Dakota State University (NDSU) coordinates a formal and annual survey (hereafter, "mid-season survey") of insects and diseases of field crops between late May and mid August (12,16). The survey is conducted by five to six personnel, made up primarily of junior and senior undergraduate students majoring in an agricultural discipline who are trained to identify and report disease incidence and severity and insect density in five crops, namely: barley, canola, soybean, sunflower, and wheat. Surveyors are located at four Research Extension Centers around the state and the NDSU main campus at Fargo, and survey eight to twelve specific counties in their regions; all North Dakota counties are surveyed. In general, surveyors evaluate fields in one county each day of the week, visiting as many as 12 fields per day, and surveying every county in a 2-week time period. The number of fields per crop surveyed in each county is roughly proportional to hectareage, but fields chosen within each county are arbitrarily selected. For example, in a county planted to 50% wheat, 20% barley, and 10% each sunflower, soybean, and canola: five, two, one, one, and one field(s) of each crop would be arbitrarily selected and surveyed. Approximately 1,800 to 2,000 fields are annually surveyed, of which 5-10% are sunflower fields. The incidence of plants exhibiting signs and/or symptoms of downy mildew is recorded by examining 40 plants in two-row pairs at five points along a W pattern for a total of 200 plants per field.

Late-season Survey Methods

The National Sunflower Association sponsors an annual survey of sunflower fields across major production areas in the US at the end of the growing season, typically mid September to mid October (hereafter, "late-season survey") (3,11,13). The survey is coordinated by the NDSU Cooperative Extension Service and is conducted by volunteer professionals from universities, seed and chemical companies, crop consultants, and other knowledgeable individuals. Prior to surveying, volunteers attend an all-day training event, which includes weed, insect, and disease identification and logistic instruction. Survey teams of two to four volunteers are created by maximizing the volunteers’ diversity of expertise. In North Dakota, 12 to 18 survey teams survey sunflower fields during the last two weeks of September.

The number of sunflower fields surveyed in each county is proportional to the previous year’s sunflower hectacreage in that county as estimated by the USDA. Initially, one field/2,000 ha in a county was surveyed, but was later decreased to one field/5,000 ha. Within each county, sunflower fields are arbitrarily selected, although a minimum distance of 3 km between each field is encouraged. Two locations representative of the field are selected. The incidence of sunflowers infected with downy mildew is recorded by examining a minimum of 25 plants each in two rows in different parts of each field.

Data Collection, Interpretation, and Analysis

For the purpose of this paper, prevalence is defined as the percent of fields with downy mildew and incidence is defined as the percentage of plants infected in each field (15). Incidence is categorized into three "yield impact categories": minimal (1-10%), low (10-20%), and moderate (>20%). Although individual plants infected with downy mildew frequently die and/or do not produce any yield (4,10), no literature on the relationship between incidence of downy mildew in a field and yield loss could be found. As such, studies relating stand reduction to yield were used to determine yield impact categories. According to data compiled for crop insurance adjustors, which assumes that random plant loss within seven weeks post-emergence, stand reductions of less than 10% result in no yield loss, 10 to 20% stand reduction results in a 1 to 3% yield loss and stand reductions of 30, 40, and 50% result in an 8, 11, and 12% yield loss (1).

Rainfall data between 15 May and 15 June, when 90% of the North Dakota sunflower crop is planted (2), was collected by North Dakota Agriculture Weather Network (NDAWN, weather stations each year of the survey. Pearson Correlation coefficients for rainfall and disease incidence were calculated in SAS v 9.2 (SAS Institute Inc., Cary, NC) using the PROC CORR procedure for 11 years of NSA and NDSU survey data to analyze potential relationships between downy mildew and rainfall.

Mid-season Survey Results

A total of 1,558 sunflower fields were scouted in the eleven-year survey, with a high of 205 fields in 2008 and a low of 79 in 2001 (Table 1, Fig. 4). Prevalence of downy mildew averaged 33.9%, with a range from 1.6% to 70.3% in 2006 and 2011, respectively (Table 1, Fig. 5). The mean incidence was 2.1%, ranging from 0.02% in 2006 to 7.1% in 2011. In each year, the majority of fields infected with downy mildew had incidence values less than 10% and thus were categorized as having minimal yield impact. In 2005 and 2011, the percentage of the fields infected with downy mildew had greater than 10% incidence and were categorized as having moderate yield impact were 21.3 and 23%, respectively.


Fig. 4. Location of 1,558 sunflower fields in North Dakota surveyed by the mid-season survey between 2001 and 2011.



Fig. 5. Prevalence of sunflower fields with downy mildew as detected by mid-season and late-season surveys and total rainfall between 15 May and 15 June from 2001 to 2011.


Table 1. Number of fields, prevalence and incidence of downy mildew between 2001 and 2011 as identified by the mid-season survey.

Year Number
of fields surveyed
Prevalence of infected
Percent fields with trace-10% incidence Percent fields with 11-20% incidence Percent fields with >20% incidence Mean incidence across all fields
2001 79 32.9 29.1 2.5 1.3 1.5
2002 197 16.2 14.7 1.0 0.5 0.6
2003 123 20.3 18.7 0.8 0.8 0.7
2004 164 58.5 56.1 1.8 0.6 1.6
2005 80 58.8 37.5 12.5 8.8 5.9
2006 128 1.6 1.6 0.0 0.0 0.02
2007 130 21.5 19.2 0.8 1.5 1.3
2008 205 19.1 16.6 2.0 0.5 1.3
2009 182 48.4 42.9 4.9 0.5 2.6
2010 152 25.7 24.3 0.0 1.3 0.9
2011 118 70.3 47.4 11.0 12.0 7.1
Mean 141 33.9 28.0 3.4 2.5 2.1

Late-season Survey Results

A total of 1,214 fields were surveyed from 2001 to 2011 (survey not done in 2004), with a high of 266 fields in 2001 and a low of 77 in 2007, 2008, and 2011 (Table 2, Fig. 6). The mean prevalence of downy mildew was 17%, with a low of 1.5% in 2001 and a high of 47.5% in 2005 (Fig. 5). The mean incidence was 1.2%, with a low of 0.01% in 2001 and a high of 4.5% in 2005 (Table 2). The proportion of infected fields with a moderate yield impact was high in 2005 and 2008, where disease incidence values were 26.3% and, 24.8%, respectively.


Fig. 6. Location of 1,214 sunflower fields in North Dakota surveyed by the late-season survey between 2001 and 2011.


Table 2. Number of fields, prevalence and incidence of downy mildew between 2001 and 2011 as identified by the late-season survey.

Year Number
of fields surveyed
Prevalence of infected fields Percent fields with trace-10% incidence Percent fields with 11-20% incidence Percent fields with >20% incidence Mean incidence across all fields
2001 266 1.5 1.1 0.4 0.0 0.01
2002 252 4.0 3.6 0.0 0.4 0.5
2003 118 9.3 6.8 1.7 0.8 0.7
2004 na na na na na na
2005 80 47.5 35.0 9.0 3.6 4.5
2006 84 2.4 2.4 0.0 0.0 0.08
2007 77 22.1 20.8 1.3 0.0 0.7
2008 77 20.8 15.6 2.6 2.6 1.6
2009 87 12.6 11.5 0.0 1.1 0.5
2010 96 9.4 9.4 0.0 0.0 0.5
2011 77 40.2 33.7 3.9 2.6 2.9
Mean 121.4 17.0 14.0 1.9 1.1 1.2

Comparison of Survey Techniques and Results

Although the survey methods varied in the number of plants examined and number of locations surveyed per field, comparisons among the two timings were made. The greatest difference between the mid-season and late-season surveys was the time at which the survey is conducted. The mid-season survey examined sunflower fields from late June until mid August, which correlates approximately with the end of the vegetative growth stages (approximately V8 to V12) to the beginning of the bloom stage (R5) (20), whereas the late-season survey was conducted near physiological maturity. As neither survey was designed specifically for downy mildew, both surveys may underestimate the prevalence and incidence of downy mildew, because severely infected plants may die prior to fields being surveyed. However, the mid-season survey has a greater likelihood of more accurately assessing early infection, as fields are scouted when plants that have died may still be visible.

Downy mildew prevalence results from the mid-season survey were approximately twice as high as the late-season survey, although year to year variation existed. Disease levels from 2004 were omitted, as the late-season survey was not conducted that year. Data from both surveys identified 2005 and 2011 as the years with high prevalence. However, surveys disagreed on years with the lowest prevalence. Similarly, results from the mid-season survey generally reported higher incidence and higher percentages of fields where incidence exceeded 10%. Mean incidence values in the mid-season survey (2.1%) were approximately double the mean incidence values in the late-season survey (1.2%). However, both surveys identified 2005, 2008, and 2011 as having the highest proportion of downy mildew infected fields with incidence values exceeding 10%. Data from both surveys suggest that yield loss due to downy mildew was most significant in 2011, followed by 2005 and 2008.

Geographic Distribution of Downy Mildew

Downy mildew was observed in 51 of 53 counties in North Dakota between 2001 and 2011. The disease was not observed in Divide and Williams counties. Sunflower in those counties is limited and only nine total fields were surveyed. Distribution of the most severely affected fields did not appear to follow any geographic pattern and fields with > 10% incidence were scattered throughout the state (Fig. 7).


Fig. 7. Location of 92 sunflower fields surveyed between 2001 and 2011 with downy mildew incidence greater than 10% as detected by the mid-season survey (triangles) and the late-season survey (circles).


Impact of Rainfall on Downy Mildew

Statewide rainfall totals were not significantly correlated (P ≤ 0.05) to disease incidence for either of the surveys (data not presented); which does not support the assumption widely held that downy mildew is higher when it rains during the general planting time (approximately 15 May to 15 June), and is only a limited problem when it is relatively dry. Because saturated soil for only a brief time period immediately after planting is needed for infection, brief localized thunderstorms and/or field topography creating wet spots can result in significant infection even in a relatively dry spring. Conversely, a dry period immediately after planting may limit the development of downy mildew in a wet spring. It is likely that correlations may be drawn between rainfall and downy mildew if specific planting dates and rainfall history of each field is known, but this was beyond the scope of this study.

Management of Downy Mildew: Past, Present and Future

Downy mildew has been a frequent problem of sunflower in North Dakota, but levels of the disease fluctuates annually. Although micro-environment may be the primary reason levels fluctuate, the fluctuation may be partially related to the disease management tools available to growers. In the early 1980s, resistant hybrids were available, but new races of the pathogen continued to evolve (10) and disease prevalence ranged from 23% in 1981 to 59% in 1984 (5). After the federal registration of the fungicide seed treatment metalaxyl (Apron, Syngenta Crop Protection) in 1985, downy mildew incidence declined and seed companies relied more on chemical control rather than developing resistant hybrids. A late-season survey conducted in 1991 found downy mildew prevalence and incidence to be 16% and 0.05%, respectively, and a 1995 survey found prevalence and incidence to be 18% and 0.5%, respectively (5). In the late 1990s, resistance to FRAC 4 fungicides developed in P. halstedii populations and by 1999, 91% of the P. halstedii isolates tested in North Dakota were insensitive to the registered rates of either metalaxyl or mefenoxam (Apron XL, Syngenta Crop Protection) (6,8).

From the late 1990s to 2002, neither effective seed treatments nor resistant hybrids were available to growers. However, downy mildew levels were relatively low during this period. In 2003, the fungicide azoxystrobin was registered as a sunflower seed treatment and hybrids with the Pl6 resistance gene became available, providing growers with two new management tools (L. Kleingartner, personal communication). During this period, downy mildew prevalence and incidence fluctuated from very high (2005) to very low (2006), and remained relatively low until 2011. This may indicate that the availability of new management techniques in 2003 did not immediately alter the occurrence of the disease in the state. However, it is possible that widespread prevalence and high incidence in 2005 resulted in greater adoption of resistant hybrids and fungicide seed treatments in 2006 and in subsequent years, resulting in lower disease levels. This could partly explain why high levels of rainfall in 2007 and 2008 did not correlate with high disease pressure.

In 2009, P. halstedii races virulent on Pl6 were identified in multiple locations in North Dakota (9), leaving FRAC 11 fungicide treatments, which now included azoxystrobin and fenamidone (17), as the primary management tool for the pathogen. In 2011, the prevalence and incidence of downy mildew increased dramatically over recent years, which may have been a partly a result of new pathogen races, which comprised 14% of isolates characterized between 2009 and 2011 (9).

Future management of downy mildew will depend on staying one step ahead of pathogen variability, which includes the deployment of new resistance genes into commercial hybrids and the registration of effective fungicide seed treatments that are not FRAC 11 or FRAC 4. Resistance genes effective against the new P. halstedii races that confer virulence on Pl6 are in a limited number of commercial hybrids, but are available in released USDA germplasm (9). However, the identification of new resistance genes is important. Virulence changes in the pathogen occur, and it is likely that the currently effective resistance genes will be overcome in the near future. FRAC 11 seed treatments are currently still effective, but the risk for the development of pathogen resistance to this chemistry is high (17). As such, effective fungicide seed treatments of additional FRAC groups will be important for management of the disease in the future.


Downy mildew is an important sunflower disease in North Dakota, but annual fluctuations in prevalence and incidence occur. These fluctuations could not be easily correlated with statewide rainfall patterns at the time of planting or management tools available to growers. However, monitoring prevalence and incidence remains an important tool for assessing disease pressure and may indicate possible changes in pathogen virulence or sensitivity to fungicides. In this study, assessment of downy mildew in a mid-season survey identified greater prevalence and incidence than in a late-season survey, indicating mid-season assessment may be a more effective way to monitor downy mildew levels in the future.


The authors thank the many participants in both surveys, including surveyors and survey coordinators. The authors also thank the National Sunflower Association, the North Dakota State Cooperative Extension Service, and the United States Department of Agriculture – Agriculture Research Service for logistical support and/or funding, and Drs. Michael Wunsch and Jared LeBoldus for critical review of the manuscript.

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