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© 2013 Plant Management Network.
Accepted for publication 31 January 2013. Published 29 May 2013.


Climatic and Environmental Trends Observed During Epidemic and Non-epidemic Years of Soybean Sudden Death Syndrome in Iowa


Leonor F. S. Leandro, Alison E. Robertson, Daren S. Mueller, and Xiao-Bing Yang, Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA 50011


Corresponding author: L. F. S. Leandro. lleandro@iastate.edu


Leandro, L. F. S., Robertson, A. E., Mueller, D. S., and Yang, X.-B. 2013. Climatic and environmental trends observed during epidemic and non-epidemic years of soybean sudden death syndrome in Iowa. Online. Plant Health Progress doi:10.1094/PHP-2013-0529-01-RS.


Abstract

Soybean yield losses due to sudden death syndrome (SDS) have varied from year to year in Iowa since the disease was first reported in 1993. An SDS epidemic in 2010 resulted in significant yield losses and raised numerous concerns by farmers and agronomists regarding the potential for future outbreaks. Since infection and SDS development is highly dependent on temperature and soil moisture, our hypothesis was that SDS epidemics occur in years with above-average rainfall and below-average temperatures. To test this hypothesis, environmental conditions in southeast and central Iowa were compared among epidemic and non-epidemic years. Mean total precipitation and number of days with precipitation during each month of the growing season (April through August) tended to be greater in epidemic years (10.4 to 26.3 inches, 10 to 15 days) than non-epidemic years (8.9 to 15.4 inches, 9 to 12 days). Soil temperatures in April through July averaged less in epidemic years (9.0 to 24.7°C) than non-epidemic years (10.4 to 26.6°C). The widespread 2010 SDS epidemic in Iowa likely resulted from the concurrence of several weather conditions that were particularly favorable for disease. To reduce risk of yield losses in future years, soybean farmers should use an integrated disease management for SDS, focusing on using resistant varieties, avoiding soil compaction, and avoiding planting in cool wet soils.


Introduction

Sudden death syndrome (SDS) of soybean is one of the greatest threats to soybean production in the US. The disease is caused by a soilborne fungus, Fusarium virguliforme O'Donnell & T. Aoki (2), and is characterized by the sudden development of foliar chlorosis and necrosis, followed by premature defoliation (Fig. 1 A-C) (23). The potential for considerable yield losses from SDS has been a concern in Iowa, the largest producer of soybean in the nation (18). The fungus infects soybean roots, causing poor root growth, brownish discoloration of the cortical tissue, and sometimes blue spore masses on the root surface (Fig. 1D) (23). Foliar symptoms are caused by pathogen toxins that are transported in the vascular system from the roots to the leaves (11).

Infection and disease development are highly dependent on environmental conditions. Root infection by F. virguliforme is favored by cool soil temperatures (15 to 17°C) (8,26), whereas the expression of foliar symptoms is favored by temperatures around 25°C (26). In fields, root infection can occur in young seedlings, but the appearance of foliar symptoms typically occurs after flowering (23,24). It is not known why infected plants do not express foliar symptoms earlier in the growing season, but physiological changes during reproductive stages may be involved (24). Soil moisture also plays a major role in occurrence and severity of SDS (26), with foliar symptoms being more severe in irrigated fields and during wet seasons when soils are saturated (14,19,22).



A
 
B

C
 
D

Fig. 1. Typical symptoms of soybean sudden death syndrome: (A) Interveinal chlorosis and necrosis on leaves; (B) leaves with dry and torn areas between the veins; (C) severely defoliated plants with green stems and attached petioles; and (D) roots with blue masses of conidia on the surface.


History of SDS Distribution and Severity in Iowa

Sudden death syndrome was first observed in Iowa in 1993 in eastern and central Iowa (33). In a survey conducted in 1994 and 1995, Yang and Lundeen (32) confirmed the presence of the disease in 13 Iowa counties (Fig. 2), with the greatest severity and prevalence in the east-central district, in Scott and Clinton counties. Interestingly, in areas of the state where disease prevalence was low, fields showing symptoms belonged to the same farmer, suggesting pathogen spread by movement of soil with farm equipment (32). During the 17 years following the first detection of SDS in Iowa, the disease was detected in additional counties usually confined to the eastern and central parts of the state. Disease occurrence during this period was sporadic and severity ranged from low to severe in individual fields based on observations reported by Iowa State University Extension and Outreach (ISUEO) state and field specialists. The 10 ISUEO field specialists are trained by Extension Plant Pathologists to estimate prevalence and severity of SDS in the regions of Iowa for which they are responsible. A later survey conducted in Iowa in 2006 also showed SDS distribution limited to the eastern half of the state (A. Robertson and F. W. Nutter, unpublished). Again, there were no reports in the western counties (Fig. 2); however, due to low disease severity during 2006, it is possible that prevalence of the disease was underestimated in the study.


 

Fig. 2. Prevalence of soybean sudden death syndrome in Iowa counties based on surveys conducted in 1994-1995 (Yang and Lundeen, 1997) and 2006 (Robertson and Nutter, unpublished).

 

In 2010, an SDS outbreak occurred in Iowa revealing that the pathogen was more widespread (Fig. 3) than previously reported (Fig. 2). Reports of plants with SDS symptoms by ISUEO field specialists were received in the third week in July in east central and southwest Iowa. In early August, moderate to severe SDS was reported in several areas of the state. In central and eastern Iowa, the epidemic quickly progressed, with large patches of defoliated plants becoming visible from roadsides and highways (Fig. 4). By 20 August, it was difficult to find a field with no SDS symptoms in parts of the state. Estimates of SDS prevalence and severity based on reports from ISUEO state and field specialists indicated that SDS was present in almost every county of the state at the end of season, including the most western and northern parts of the state, where the disease had not been previously observed. The disease developed in fields planted to either susceptible or resistant varieties and in both early (late April) and late planted (late May) fields. The extensive distribution of SDS in Iowa in 2010 suggests that F. virguliforme may have been present in most Iowa soils in previous years, but had not been detected because of low inoculum densities and/or unfavorable environmental conditions.


 

Fig. 3. Prevalence and severity of SDS in Iowa in 2010 based on observations of Iowa State University field agronomists.

 


A
 
B

Figs. 4A and 4B. Soybean fields in Iowa with severe defoliation and chlorosis caused by sudden death syndrome in 2010.


Since SDS is favored by cool, wet conditions (26), we hypothesized that epidemics of the disease would be associated with years with above-average rainfall and below-average temperatures. To this end, environmental conditions were compared among years in which SDS was prevalent and severe, and years when the disease was infrequently observed. The data will be useful in predicting future SDS epidemics in Iowa, as well as furthering research on epidemiology of this economically important disease of soybean.


Environmental Conditions Favorable for SDS in Epidemic Years

To investigate what environmental conditions contribute to SDS epidemic conditions in Iowa, total precipitation, number of rainfall days, air temperature and soil temperatures for April through August were compared in four years when SDS epidemics were most prevalent and severe (1993, 1998, 2008, and 2010) and five years when SDS prevalence and severity was low or unreported (2001, 2004, 2005, 2007, and 2011). Weather data were obtained from stations in southeast and central Iowa, which have the longest history of SDS in the state, and compared among the SDS epidemic years and non-epidemic years. Data were obtained from the Iowa Environmental Mesonet database (mesonet.agron.iastate.edu) for Crawfordsville (soil temperatures) and Mount Pleasant (precipitation and air temperature) in southeast Iowa (locations 18 miles apart), and for Ames (soil temperatures, precipitation, and air temperature) in central Iowa. The monthly 30-year means for total precipitation, number of rainfall days, and air temperature were calculated for Ames and Mount Pleasant, and the monthly 25-year means for soil temperature were calculated for Ames and Crawfordsville.

Total precipitation and number of days with precipitation were typically greater in SDS epidemic years than non-epidemic years (Table 1). This trend was particularly consistent in June, when total precipitation was 7.9 to 20.0 cm above a 30-year average in epidemic years and 1.6 to 4.8 cm below average in non-epidemic years, except in 2011. Precipitation in July was 4 to 25 cm greater than average in three of the four epidemic years, and at or below average in non-epidemic years. Precipitation in April, May, and August was not consistently associated with SDS epidemic years (Table 1). This suggests that precipitation in June, and possibly July, is more critical to SDS development in Iowa than precipitation in other months. It is interesting to note that June precipitation in 2010 was the highest recorded for any year compared and 2.6 times greater than the 30-year mean. It is therefore possible that this excessive precipitation in June played a key role in the record SDS outbreak in 2010.


Table 1. Total precipitation and number of days with precipitation in four years with high SDS prevalence (1993, 1998, 2008, and 2010) and five years with low SDS prevalence (2001, 2004, 2005, 2007, and 2011). Values are means of two locations: Ames (central Iowa) and Mount Pleasant (southeastern Iowa).

Year Total Precipitation (cm) # days with precipitation SDS incidence
Apr May Jun Jul Aug Apr May Jun Jul Aug
1993 7.9 15.7 27.6 37.6 23.1 11 16 15 19 13 First report
1998 10.3 11.4 20.3 5.1 11.6 16 11 14 9 8 High
2001 8.4 23.3 7.6 7.5 5.0 12 19 9 7 8 Low
2004 4.9 15.2 9.9 9.7 15.4 5 12 10 8 13 Low
2005 8.1 8.8 10.8 8.9 12.7 8 7 11 8 8 Low
2007 14.8 15.7 8.4 12.6 22.5 10 10 7 6 13 Low
2008 12.8 17.4 24.9 19.0 5.3 14 13 12 11 9 High
2010 10.7 16.0 32.3 16.1 18.8 12 12 19 13 10 Very high
2011 8.6 14.1 20.8 5.9 5.4 15 15 15 15 10 Low
Mean
SDS yr
10.4 15.1 26.3 19.5 14.7 13 13 15 13 10
Mean non-
SDS yr
8.9 15.4 11.5 8.9 12.2 10 12 10 9 10
30-yr
meanx
9.0 12.2 12.4 12.2 11.2 10 11 10 9 9

 x Mean for the period of 1981 to 2010 at Ames and Mount Pleasant.


The importance of high soil moisture during vegetative growth stages compared to reproductive stages had been previously observed in field studies (22) where SDS was more severe in plots where irrigation started at V3 compared to those where irrigation started at V8. In another study, Neto et al. (19) found that irrigating during mid to late reproductive stages resulted in more severe SDS symptoms than irrigating during vegetative stages alone. Irrigating at both vegetative and reproductive stages resulted in the most severe expression of symptoms. Natural rainfall during vegetative stages was believed to be sufficient for root infection, thus contributing to the lack of disease response to irrigation during vegetative stages (19).

Excessive rainfall throughout the 2010 season was compounded by heavy snowfall in the winter of 2009 (data not shown). Floods that occurred in central Iowa on 11 August 2010 totaled 19.3 cm in Ames. This coincided with the start of widespread reports of severe SDS. Interestingly, the first report and two of the most severe outbreaks of SDS recorded in Iowa also occurred in years when floods occurred: 1993, when the disease was first reported (17); 2008, when a severe outbreak occurred; and 2010, when the most severe and widespread SDS epidemic on record occurred. This suggests that waterlogged soils may be particularly conducive for SDS development. Flooding is known to increase diseases caused by several soybean pathogens (12,13). The effect of flooding on SDS has not been studied; however, excessive rainfall suggests that waterlogged soils may be particularly conducive for SDS development. It is possible that reduced soil aeration in saturated soils predisposes roots to infection (15) and/or favors production of pathogen toxins. Additional research is currently underway to examine these hypotheses.

The importance of soil temperature on SDS outbreaks in Iowa is not as clear as that of soil moisture/precipitation. Previous studies have shown that cool soil temperatures (optimum 15-17°C) favor infection during vegetative growth stages (8,26) and that cooler than average seasons are generally more favorable for SDS development (23). Consistent with these reports, mean soil temperatures in April through August in epidemic years were lower than in non-epidemic years (Table 2). However, the data do not provide strong evidence for a consistent effect of low soil temperatures on SDS outbreaks in Iowa. For example, mean soil temperatures in 2010 were similar to that of some non-epidemic years (12.5°C and 16.5°C in April and May 2005, respectively), while cooler soil temperatures at planting (May) did not result in an SDS outbreak in 2005 (Fig. 5 and Table 2).


Table 2. Mean air and soil temperatures in four years with high prevalence of sudden death syndrome (SDS) of soybeans (1993, 1998, 2008, and 2010) and five years with low SDS prevalence (2001, 2004, 2005, 2007, and 2011). Values are means of two locations: Ames (central Iowa) and Mount Pleasant (southeastern Iowa) for air temperature, and Ames and Crawfordsville (southeastern Iowa) for soil temperature.

Year Mean air temp. (C) Mean soil temp. (C) SDS incidence
Apr May Jun Jul Aug Apr May Jun Jul Aug
1993 8.3 16.1 20.3 22.8 22.8 5.5 14.4 19.5 22.9 23.4 First report
1998 10.6 19.2 20.3 23.9 23.6 10.3 18.7 20.7 26.5 25.6 High
2001 13.9 17.2 21.1 25.0 23.6 11.6 16.7 21.7 27.1 25.4 Low
2004 11.9 17.8 20.6 22.2 20.0 11.8 18.1 23.4 25.6 22.5 Low
2005 13.1 16.1 23.3 25.0 23.3 12.5 16.5 24.7 28.0 26.2 Low
2007 9.4 19.4 22.2 23.6 25.0 8.4 18.4 23.6 27.1 26.0 Low
2008 9.7 15.6 21.7 23.3 21.7 8.0 14.6 21.2 23.6 22.8 High
2010 14.4 16.9 22.8 24.7 24.4 12.4 16.7 23.0 25.6 24.5 Very high
2011 9.4 16.1 21.7 26.1 22.8 7.9 14.3 19.9 25.2 24.8 Low
Mean
SDS yr
10.8 16.9 21.3 23.7 23.1 9.0 16.1 21.1 24.7 24.1
Mean non-SDS yr 11.6 17.3 21.8 24.4 22.9 10.4 16.8 22.7 26.6 25.0
30(25)-yr meanx 10.9 16.6 21.6 23.7 22.6 9.8 16.3 22.1 25.1 24.1

 x Mean for the period of 1981 to 2010 for air temperature at Ames and Mount pleasant, and for the period of 1986 to 2010 for soil temperature at Ames and Crawfordsville.


 

Fig. 5. Soil temperature in April and May in years with high SDS prevalence (left) and years with low SDS prevalence (right). Soil temperature was calculated as the mean of soil temperatures in Ames and Crawfordsville, IA. The dashed line shows the 10-year mean based on years 2000-2009 and the solid line shows temperature for that year. The arrows show time when approximately 10% (dashed arrow) and 50% (solid arrow) of soybean planting had been completed in Iowa. Data for 2011 not shown.

 

Planting times in relation to fluctuations in soil temperature may be more meaningful for predicting conditions that favor F. virguliforme infection. Early soybean planting has been associated with increased SDS severity (10,28,30,32). Mid-May plantings resulted in higher SDS severity than mid-June through early July plantings in Kentucky (10) and Missouri (30). In Iowa, a survey conducted in 1994 (32) found that SDS was only detected in fields that had been planted before May. In addition, progressively less SDS has been observed in soybeans planted in early May, mid May, and mid June in Iowa (28). In the present study, the comparison of soybean planting progress in Iowa in SDS epidemic years and non-epidemic years showed that soybean planting started earlier than average in 2010, with 13% and 44% of soybean acres planted by 26 April and 3 May, respectively (Table 3). The early planting was prompted by above-average soil temperatures and optimum seedbed conditions in April. However, early planting was not consistently associated with severe SDS epidemics in the state. In 2008 and 1993, planting occurred later than usual, with 34% of soybean acres planted by 17 May and 24 May, respectively (Table 3). Conversely, in 2004 and 2005, when SDS was not severe, planting occurred comparatively early with 45% and 51% of the acres planted by 10 May (Table 3).


Table 3. Percent of completed soybean planting in Iowa for four years with high SDS prevalence and four years with low prevalence.

Year 26
Apr
3
May
10
May
17
May
24
May
31
May
7
Jun
14
Jun
SDS
incidence
1993 0 0 5 15 34 45 60 80 First report
1998 0 14 62 85 90 97 98 99 High
2001 0 5 13 47 60 73 81 91 Low
2004 0 9 51 76 87 92 95 99 Low
2005 3 26 45 70 87 97 99 100 Low
2007 0 4 24 61 87 93 98 100 Low
2008 0 0 4 34 72 82 86 88 High
2010 13 44 53 75 91 95 97 97 Very high
2011 0 0 10 47 78 87 94 98 Low

 x Data source: Annual planting progress reports from the USDA-NASS Agricultural Statistics Board.


Comparison of epidemic and non-epidemic years did not show a consistent pattern between planting date and daily fluctuations in soil temperature during the months of April and May (Fig. 5). As discussed above, SDS epidemics tended to occur in cooler years, but considerable variation in soil temperature occurred during the planting period (mid April to end of May), with temperature dropping below 12.8°C (55°F) in both epidemic and non-epidemic years. This lack of association between soil temperature and SDS severity suggests that low soil temperatures at planting are not necessary for an SDS outbreak. It is noteworthy, however, that 2010 was the only year when temperature dropped below 12°C (53.6°F) for seven consecutive days, coinciding with a period when approximately 50% of soybean acres were planted. Soybean germination is reduced at temperatures below 10°C (21). In growth chamber studies, seedlings grown at cooler soil temperatures were susceptible to infection for a longer period of time than seedlings grown in warmer soil (8). It is possible that the extended drop to 10°C during seed germination and emergence was one of the factors that contributed to the 2010 SDS outbreak.

Despite the increased risk of SDS in earlier planted soybeans, delayed planting is not recommended as a management practice in Iowa, because maximum yield potential is achieved with earlier plantings (4). Recommended planting dates for soybean in Iowa are 25 April in the southern two thirds of the state, and 1 May in the northern third of the state (21). Previous reports (9,21) and our findings suggest that soybean planting date decisions should be based on soil conditions and not the planting date itself. Commercially available fungicide seed treatments are not currently effective against SDS (3,29), so there is not the option of applying treatments to protect seedlings when planting early. Since the cool wet soil conditions that increase root infection are more likely to occur in April than May in Iowa, farmers may choose to plant soybean fields with a history of SDS last in their planting sequence to minimize risk of SDS. However, this decision must take into consideration the risk of compromising yield potential.

Although the comparisons conducted in this study suggests that low soil temperatures at planting are not necessary for an SDS epidemic, it is important to note the limitations of generalizing weather and planting date information over the state, as these may not represent the conditions that occurred at the individual fields or at the regional level. An additional limitation of this study is that information about SDS incidence and prevalence was based on subjective observations of disease. This type of data revealed general climate trends associated with SDS epidemics, but is not adequate for a more predictive analysis of disease risk. Future studies to model climate and environmental variables in relation to SDS, such as those conducted by Del Ponte et al. (5,6,7) on soybean rust, could offer valuable tools for predicting risk of future SDS epidemics.


Summary and Conclusions

Sudden death syndrome is a complex disease that is determined by the interaction of many environmental and biological factors. Analyses of the climate patterns of SDS epidemics in Iowa compared to non-epidemic years suggest that no single climatic factor determines development of the disease. Planting in cool soils may not be problematic if the remainder of the growing season is dry, and SDS outbreaks can be severe even when average soil temperatures are above average at planting. The climatic factor that was consistently associated with epidemics of SDS was rainfall in June, which in Iowa corresponds to the onset of flowering. The mechanisms behind the importance of this period may be related to physiological changes when plants are transitioning to reproductive stages (24), possibly including changes in patterns of root growth during that time. It is also possible that excess soil moisture, leading to waterlogged soils, may enhance disease development.

The widespread nature and high disease severity in 2010 generated major concerns about potential yield losses in Iowa. Many concerned farmers inquired if anything could be done to reduce damage from the disease, how much impact it would have on their yield, and how likely this type of outbreak would occur in future years. While no disease management practice is completely effective at reducing the disease, farmers can reduce risk of an SDS outbreak in their fields by integrating several tactics (23). The primary measures should include planting the most resistant varieties available, managing soil moisture to improve drainage, and avoiding planting in cool wet soils (23). Alternative practices, such as seed treatments (16,20,27) and crop rotation (1,25,31), should continue to be investigated for their effectiveness as additional tools for integrated management of SDS. In addition, future work focused on modeling climate and environmental variables in relation to disease variables (5,6,7) may offer useful tools for predicting the risk of SDS epidemics.


Acknowledgments

We thank the Iowa Soybean Association for funding. We also thank the Iowa State University Extension Field Agronomists for reports on SDS progress in the state, Daryl Herzmann from the Iowa Environmental Mesonet for assistance with weather data, and Donna Halloum for creating the disease prevalence maps.


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