An Aerobiological Assessment of Soybean Rust Threat to North America Scott Isard (UI) & Roger Magarey, Bob Griffin (CPHST/APHIS) Joe Russo (ZedX) & Stuart Gage (MSU) Glen Hartman & Monte Miles (ARS & NSRL) World-Wide SBR Distribution Fungicide treated field José Tadashi Yorinori, Embrapa Soja 2003 Untreated field potential to be the most destructive foliar disease of soybean in the U.S. has caused significant yield losses worldwide yield losses in Brazil exceeded 5% of the annual production (Miles et al. 2003) Soybean rust resistant / tolerant cultivars unavailable Only a few fungicides that control the rust are registered for U.S. foliar application on soybean Foliar fungicides require frequent applications and thus can add significantly to production costs. In 2002: 355,000 U.S farms grew soybean 72.1 M acres of soybean were harvested 23% of harvested crops were soybean USDA ERS 10% yield losses are possible in any U.S. soybean-growing region. In southeastern states where climatic conditions favor the spread, development, and over-seasoning of the disease, 50% losses are conceivable (Yang 1996).

Contributors Scott Isard (UI) & Roger Magarey, Bob Griffin (CPHST/APHIS) Joe Russo (ZedX) & Stuart Gage (MSU) Charlie Main, Thomas Keever (NCSU) Glen Hartman & Monte Miles (ARS & NSRL)

Phakospora pachyrhizi Not seedborne Moved easily by wind (short and long distance) Characterized by local epidemics caused by multi-cyclic foci and copious production of urediniospores Very aggressive and yield limiting

Pathways Natural spread –Prevailing winds –Land bridge –Extreme weather events Trade –Contaminated seed, grain, meal –Human movements Unauthorized imports or releases –Smuggled propagative material –Scientific material

Risk Factors Probability Low for meal because of processing Medium for grain and seed because of; –projecting substantial increases in volume –difficulty of detection –likelihood of being able to establish

Assessment of relative likelihood that an epidemic will be initiated by SBR spores blown from the current source region in South America (stratified by U.S. agriculture region and period of year) Ecological and Environmental Factors Impact Horizontal Transport Descent and Landing Pre- conditioning Takeoff and Ascent Aerobiology Process Model SourceDestination Created an index for each component 1. Spore production (source region) 2. Transport (atmosphere) 3. Host distribution 4. Epidemic development (destination region) Created a composite index as product of component indexes

Turbulent Transport and Dilution in the Atmosphere Conceptual Model of Soybean Rust Transport Process Synoptic Scale Airflows Govern Transport Direction and Speed Turbulent Diffusion and Wind Shear Govern Dilution Survival of Spores while Airborne Deposition of Spores into a Soybean Crop Dry Deposition Due to Wind and Turbulence Wet Deposition Due to Washout by Precipitation Escape of Spores from Canopy Spore Production Colonization of Soybean Crop Ultraviolet Radiation Temperature and Relative Humidity Soybean Plant Growth Stage of Disease Weather Vertical Distribution of Spores in Canopy Canopy Density & Structure Wind & Turbulence Time of Spore Release Soybean Crop Growth Stage Temperature & Leaf Wetness

Venezuela Guyana Suriname French Guiana Brazil Argentina Uruguay Paraguay Colombia Equador Peru Chile Bolivia The Spread of Soybean Rust in Latin America Widespread soybean cultivation Scattered soybean cultivation The Spread of Soybean Rust in Latin America Widespread soybean cultivation Scattered soybean cultivation 2001 Initial discovery of soybean rust The Spread of Soybean Rust in Latin America Widespread soybean cultivation Scattered soybean cultivation 2001 Initial discovery of soybean rust 2002 Confirmed soybean rust infestation area The Spread of Soybean Rust in Latin America Widespread soybean cultivation Scattered soybean cultivation 2001 Initial discovery of soybean rust 2002 Confirmed soybean rust infestation area 2003 Confirmed soybean rust infestation area The Spread of Soybean Rust in Latin America Widespread soybean cultivation Scattered soybean cultivation 2001 Initial discovery of soybean rust 2002 Confirmed soybean rust infestation area 2003 Confirmed soybean rust infestation area 2004 Confirmed soybean rust infestation area The Spread of Soybean Rust in Latin America Widespread soybean cultivation Scattered soybean cultivation 2001 Initial discovery of soybean rust 2002 Confirmed soybean rust infestation area 2003 Confirmed soybean rust infestation area 2004 Confirmed soybean rust infestation area 2004 Likely (unconfirmed) soybean rust infestation area ?

Percent of Brazilian State Area Planted to Soybean 0 < – – – – 6.0 Equator SBR Source Strength and Timing USDA Foreign Agricultural Service _expansion/index.htm May-June planting dates Late Nov-Dec planting dates with some double cropping

Calendar Showing Relative P. pachyrhizi Source Strength in South America 10 8 Divided year into 6 two-month periods based on spore production in South America and U.S. soybean growing season Month of Year FMAMJJASONDJ Spore Production Equatorial Brazil Southern Brazil Composite Low risk Moderate risk High risk Very high risk

Release from current source area in South America ,000 1,000 Spore Concentration Height of SBR spore production (mid-March) End of SBR major spore production (mid-May) Start of second peak of SBR spore production (mid-July) Second peak of SBR spore production (mid-Aug) (22 years) Late- March Mid- May Mid- July Late- Aug Release from current source area ,000 1,000 Spore Concentration Distribution after first week Height of SBR spore production (mid-March) End of SBR major spore production (mid-May) Start of second peak of SBR spore production (mid-July) Second peak of SBR spore production (mid-Aug) Late- March Mid- May Mid- July Late- Aug Release from current source area Late- March Mid- May Mid- July Late- Aug Distribution after first week ,000 1,000 Spore Concentration Distribution after second week Height of SBR spore production (mid-March) End of SBR major spore production (mid-May) Start of second peak of SBR spore production (mid-July) Second peak of SBR spore production (mid-Aug) Late- March Mid- May Mid- July Late- Aug Release from current source area Late- March Mid- May Mid- July Late- Aug Distribution after first week Late- March Mid- May Mid- July Late- Aug Distribution after second week ,000 1,000 Spore Concentration Distribution after third week Height of SBR spore production (mid-March) End of SBR major spore production (mid-May) Start of second peak of SBR spore production (mid-July) Second peak of SBR spore production (mid-Aug)

2004? 2004 Benin Burkina Faso Cameroon Cote d’Ivoire Liberia Nigeria Burundi Congo, Dem Rep Gabon Madagasca Rwanda South Africa Tanzania Uganda Zamibia Zimbabwe Thousands of Hectare Harvested Soybean Production 2002 In 2003, Brazil harvested 16 Million ha of soybean while South America as a whole harvested 30 M ha. Source: FAOSTAT Agricultural Data website What is the likelihood that SBR spores will be blown from Africa to North America? South America SBR source strength is at least 1000 time greater than that of Africa SBR source region

Spore Concentration Jan 4 Feb 2 Jun 1 Jul ,000 10,000 Release from Current Source Areas in Africa Spore production period in west Africa (June 1)Spore production period in west Africa (July 14) Spore production period in southern Africa (Jan 4)Spore production period in southern Africa (Feb 2) Jan 4 Feb 2 Jun 1 Jul ,000 1,000 Distribution After First Week Spore production period in west Africa (June 1)Spore production period in west Africa (July 14) Spore production period in southern Africa (Jan 4)Spore production period in southern Africa (Feb 2) Spore Concentration ,000 1,000 Distribution After Second Week Spore production period in west Africa (June 1)Spore production period in west Africa (July 14) Spore production period in southern Africa (Jan 4)Spore production period in southern Africa (Feb 2) Spore Concentration ,000 1,000 Jan 4 Feb 2 Jun 1 Jul 14 Distribution After Second Week ,000 1,000 Distribution After Third Week Spore production period in west Africa (June 1)Spore production period in west Africa (July 14) Spore production period in southern Africa (Jan 4)Spore production period in southern Africa (Feb 2) Spore Concentration

Dec 1991 – Jan 1992 Estimating the Likelihood of Aerial Transport to U.S. Agricultural Regions Pacific Mountain Northern Plains Southern Plains Delta Southeast Northeast Appalachia Great Lakes Corn Belt Counted dots to create a 3 dimensional data matrix: Agricultural region (10) Time of year (6 two-month periods) Year (10 years from ) Spore Production Calendar

Percentage of County Area Planted to Soybean (average for 2001 & 2002) U.S. Soybean Production U.S. Department of Agriculture National Agriculture Statistics Service

May 27 – Jun 27 Planting Dates (most active period) Harvesting Dates (beginning of harvest) May 25 – Jun 25 May 25 – Jun 20 May 30–Jun 28 Jun 14-Jul 14 May 20 –Jun 10 May 28–Jun 26 May 20–Jun 30 May 30–Jun 25 May 15 – Jun 15 Apr 25 – May 25 May 27 – Jun 27 May 15 – Jun 15 May 25 – Jul 1 May 25 – Jun 20 May 18 – Jun 22 May 3 – Jun 14 May 18 – Jun 4 May 20 – Jun 6 May 19 – May 29 May 16 – Jun 3 May 14 – Jun 2 May 15 – Jun9 May 15 – Jun 5 May 10 – Jun 7 May 18 – Jun 3 May 15 – Jun 20 May 25 – Jun 25 Oct 20 Sep 28 Sep 25 Oct 5 Oct 1 Oct 5 Oct 10 Oct 5 Sep 15 Aug 15 Oct 1 Sep 25 Sep 20 Sep 17 Aug 13 Sep 19 Sep 21 Sep 16 Sep 25 Sep 21 Sep 23 Sep 25 Sep 21 Sep 30 Oct 1 Soybean: Usual Planting and Harvesting Dates Agricultural Statistics Board NASS USDA

Percentage of County Area Covered with Kudzu No data 0 > >2.5 – 5.0 >5.0 U.S. Kudzu Distribution CORN SOYBEAN KUDZU

U.S. Kudzu Distribution Source: Reports by US extension agents compiled by Darryl Jewett. About 2 million acres reported Percentage of County Area Covered with Kudzu No data 0 > >2.5 – 5.0 >5.0

Simple infection model (Wang and Engel 1998) based on a temperature response function scaled to the pathogen’s wetness duration requirements (T min = 13 o C, T max = 28 o C, T opt = 20 o C, W min = 8 hr, W opt = 12 hr) Hatched areas are major soybean growing regions We estimated the number of days that might be expected to be favorable for soybean rust development during June - August from 30 years of daily temperature and leaf wetness data. Number of years out of last 30 having >15 days with conditions conducive to infestation Hatched areas represent major soybean production regions Calculated probability that a cohort of spores arriving at the beginning of each month would cause an epidemic that year. Average over past 10 years for each U.S. agricultural region. Soybean Rust Epidemiology Model

Assessment of relative likelihood that an epidemic will be initiated by SBR spores blown from the current source region in South America (stratified by U.S. agriculture region and period of year) Ecological and Environmental Factors Impact Horizontal Transport Descent and Landing Pre- conditioning Takeoff and Ascent Aerobiology Process Model SourceDestination Created an index for each component 1. Spore production (source region) 2. Transport (atmosphere) 3. Host distribution 4. Epidemic development (destination region) Created a composite index as product of component indexes

Northeast Lake States Corn Belt Northern Plains Appalachia Southeast Delta States Southern Plains Mountains Pacific Dec-Jan Feb-Mar Apr-May Oct-Nov Jun-Jul Aug-Sep Composite Index Relative risk on a scale of 0 to 1

Soybean Rust Epidemic Index Kudzu Area Sub-Index Soybean Area Sub-Index Host Distribution Index Transport Index Source Strength Index Dec-Jan Feb-Mar Apr-May Oct-Nov Jun-Jul Aug-Sep Component Indexes NE LS CB NP A SE DS GP M P NE = NortheastSE = Southeast LS = Lake StatesDS = Delta States CB = Corn BeltGP = Great Plains NP = Northern PlainsM = Mountain States A = AppalachiaP = Pacific States D-J F-M A-M J-J A-S O-N Percent

Northeast Lake States Corn Belt Northern Plains Appalachia Southeast Delta States Southern Plains Mountains Pacific Dec-Jan Feb-Mar Apr-May Oct-Nov Jun-Jul Aug-Sep Composite Index Relative risk on a scale of 0 to 1 Relative likelihood that an epidemic will be initiated by SBR spores blown from the current source region in South America Provides guidance on where and when to scout.