Emergence and integrated management of thrips-transmitted Tomato spotted wilt virus (TSWV) in California crops

UCCE-Monterey County; 2015 Plant Disease Seminar November 4, 2015; County of Monterey Agricultural Center; Salinas, California

Ozgur Batuman Department of Plant Pathology, UC Davis California Processing Tomatoes And Peppers

• Today, California grows 95 percent of the USA’s processing tomatoes and approximately 30 percent of the world processing tomatoes production!

• California produced 60 and 69 percent of the bell peppers and chile peppers, respectively, grown in the USA in 2014! Pepper-infecting viruses • ~70 viruses known to infect peppers worldwide • ~10 of these known to occur in California • Most are not seed-transmitted • Difficult to identify based on symptoms • Mixed infections are common • Transmitted from plant-to-plant by various insects, primarily aphids and thrips • Best managed by an IPM approach

TSWV Key viruses affecting peppers in CA production areas

• Alfalfa mosaic virus (AMV) Alfamovirus • Cucumber mosaic virus (CMV) Cucumovirus • Pepper mottle virus (PepMoV) Potyvirus Aphid • Potato virus Y (PVY) Potyvirus • Tobacco etch virus (TEV) Potyvirus

• Pepper mild mottle virus (PMMV) Tobamovirus • Tobacco mosaic virus (TMV) Tobamovirus Seed & Mechanical • Tomato mosaic virus (ToMV) Tobamovirus

• Tomato spotted wilt virus (TSWV) Tospovirus Thrips • Impatient necrotic spot virus (INSV) Tospovirus

• Beet curly top virus (BCTV) Curtovirus Leafhopper

*Whitefly-transmitted geminiviruses in peppers are not present in CA The incidence of thrips and Tomato spotted wilt virus (TSWV) in vegetable crops in California has increased! • Tomato spotted wilt disease has been in CA for >75 years. • Until 2005, it did not cause major economic losses • It has now emerged as a major constraint on production of lettuce, pepper and tomato!

Western flower thrips (Frankliniella occidentalis) Tomato spotted wilt disease caused by Tomato spotted wilt virus Symptoms of TSWV in peppers vary depending on the stage of growth plants are infected and cultivar Symptoms of TSWV in peppers TSWV-Thrips interaction and transmission

ACQUISITION TRANSMISSION BY LARVAE IS CRUCIAL Egg

X 1st instar

2nd instar VIRUS PASSAGE VIRUS PASSAGE

Only adults that acquire as larvae can transmit. Pupal Stages Do Not Feed (Whitfield et.al., 2005) Overall Objectives

• Develop an understanding of when and where thrips and TSWV gain entry into California peppers • Determine dynamics of thrips populations and spotted wilt disease development • Identify potential inoculum sources • Apply knowledge of thrips and TSWV to develop a regional integrated pest management (IPM) program • Minimize economic losses due to thrips and TSWV Locations of Monitored Fields

Northern counties (2009-2013) Gene Miyao (Solano, Yolo, Colusa, Sutter and Sacramento)

Brenna Aegerter San Joaquin County (2013-2014)

Merced County (2008-2012) Scott Stoddard Fresno and Kings Counties (2007-2012)

Tom Turini Coastal Counties (2015) >230 monitored fields Steve Koike since the start of the

Michelle Le Strange program Monitoring transplants (2007-2010)

Tomato/pepper transplant greenhouses -Greenhouse operations monitored for thrips and TSWV -Yellow sticky cards for monitoring thrips -Indicator plants and visual inspection for TSWV

TSWV was not detected on indicator plants or in transplants in any of the monitored greenhouses Average 2000 1800 1600 thrips 1400 1200 populations 1000 800 600 inside 400 2010 200 Transplant 0 2009 Aug Houses Jul 2008 Jun 2007-2010 May 2007 Apr Mar

Average 2000 1800 1600 thrips 1400 1200 populations 1000 800 600 outside 400 200 Transplant 0 2010 Houses 2009 Sep Oct Aug Jul 2007-2010 2008 Jun May 2007 Apr Mar Transplants were not a major source of thrips or TSWV  Relatively low thrips populations (especially in closed greenhouses) were on transplants

 No evidence of TSWV infection of transplants in monitored greenhouses

 Transplants are not bringing in TSWV or substantial thrips populations into fields Monitoring thrips and TSWV in pepper fields

• Thrips are monitored with yellow sticky cards • Virus incidence is determined by visual inspections • TSWV infection is confirmed with immunostrips or RT-PCR

777bp 777bp Average Thrips Populations in Pepper Fields in 2015 (thrips/card/2 weeks)

Winter 2015 1-Dec 15-Dec 1-Jan 15-Jan 1-Feb 15-Feb 7500 30 7000 6500 20 6000 10 5500 0 5000 4500 4000 3500 3000 2500 2000 1500 1000 500 0

Coastal Area Yolo/Solano Co. San Joaquin Co. Thrips populations in monitored pepper fields in 2013-2015 4000 3500 3000 2500 2000 1500 1000 thrips/card/two weeks thrips/card/two 500 0 April May June July August September October 2013 2014 2015 Late-planted and/or red pepper fields had higher TSWV incidences! TSWV Incidences (%) in monitored pepper fields in 2013-2015 2013 2014 2015

15

10 * R * * 5 TSWV TSWV % 2015 2014 0 2013 Year 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Pepper Fields

* Part of this pepper field was kept for red pepper harvest R TSWV resistant pepper varieties Communicating with Growers

Adult thrips Larval thrips • It is important that thrips management be implemented prior to or immediately following initial TSWV findings • Critical to reduce the number of virus-carrying adults by controlling larvae early in the season • Thrips insecticide trials have been conducted at Westside Exp. Station, based on 2007-2011 trials the best materials were: Radiant (spinetoram) Success (spinosad) Dimethoate (organophosphate) Lannate (methomyl) Mustang+Beleaf (pyrethroid + flonicamid)

• However, the effect was not long-lasting (4-7 days) Potential thrips/TSWV reservoirs • Almonds -thrips populations were low in almond orchards (yellow sticky cards) and in flowers -TSWV not detected in thrips from almond (almond is not a reported host for TSWV) by rina thompson

• Weeds -a variety of common weeds were collected throughout the growing season in areas known to have TSWV outbreaks -most weeds were negative for TSWV rough-Weedsseeded buttercup (Ranunculus 85%No.(>150) Symptoms+ Weed survey results for muricatus) positive/no tested (+/-) Bermuda buttercup (Oxalis pes-caprae) 0/18 - TSWV incidence during London rocket (Sisymbrium irio) 1/29 + 2007-2013 bindweed (Convolvulaceae sp.) 4/218 + burclover (Medicago polymorpha) 0/24 - pigweed (Amaranthus retroflexus) 0/39 - black nightshade (Solanum americanum) 5/73 + curly dock (Rumex crispus) 0/17 - dodder (Cuscuta sp.) 0/30 - turkey mullein (Eremocarpus setigerus) 0/14 - lamb's quarter/goosefoot (Chenopodium 0/68 - purslane (Portulaca oleracea) 0/38 - album) black mustard (Brassica nigra) 0/87 - Malva (Malva neglecta and M. parviflora) 3/168 - Russian thistle (Salsola tragus) 0/65 - velvetleaf (Abutilon theophrasti) 0/28 - buckhorn plantain (Plantago lanceolata) 0/16 - prickly lettuce (Lactuca serriola) 8/217 + pennywort (Hydrocotyle ranunculoides) 0/5 - groundsel (Senecio vulgaris) 0/47 - filaree (Erodium spp.) 0/48 - wild radish (Raphanus raphanistrum) 0/53 - knotweed (Polygonum aviculare) 0/23 - sowthistle (Sonchus oleraceus) 15/191 + poison hemlock (Conium maculatum) 0/26 - ground cherry (Physalis acutifolia) 1/36 + redmaids (Calandrinia ciliate) 0/24 - tree tobacco (Nicotiana glauca) 0/35 - chickweed (Stellaria media) 0/43 - barnyard grass (Echinochloa sp.) 0/39 - miner's lettuce (Claytonia perfoliata) 0/37 - pineapple weed (Matricaria discoidea) 5/118 + Datura (jimsonweed: Datura stramonium) 3/28 + nettle (Urtica sp.) 0/61 - Other tree and shrub/plant species (i.e, Nerium 0/(>100) - common sunflower (Helianthus annuus) 0/65 - oleander, olive, oak, laurel, sage, cotton etc.) fiddleneck (Amsinckia menziesii) 0/74 - Total 45/2,159 shepherd’s-purse (Capsella bursa-pastoris) 0/57 - ~2% A special case 1: New Potentially Important TSWV Weed Host Identified in San Joaquin and Northern Counties: BUTTERCUP!

Rough-seeded buttercup (Ranunculus muricatus) weeds infected with TSWV A special case 2: Weeds in fallow fields where weeds can harbor high levels of thrips/TSWV

• High populations of weeds can develop in fallow fields previously cultivated to TSWV hosts (e.g., lettuce)

• Some of these weeds (e.g., sowthistle and prickly lettuce) may develop high populations of thrips and TSWV

• In 2008, the first outbreaks of TSWV in tomato were in fields near fallow fields that had high populations of weeds and were previously planted with lettuce Bridge crops Red leaf chicory (Cichorium intybus, Asteraceae), •Bridge crops are those grown during winter monthsAKA Italianand chicory that serve as potential sources of thrips/TSWV for spring-planted peppers/tomatoes

•Examples of thrips/TSWV bridge crops include radicchio, lettuce and fava bean

•Examples of thrips bridge crops include alfalfa, onion and wheat

Lettuce in Fresno County Radicchio in Merced County

Bridge crops

Yolo and Yolo Colusa Co. Colusa Pepper/ Tomato Fava beans Fava beans August September October November December January February March April May June July August September October November

Pepper/ Tomato Kings Co. Kings

Fresno and and Fresno Spring Lettuce Fall Lettuce Fall Lettuce Fallow August September October November December January February March April May June July August September October November

Pepper/ Tomato

Merced Co. Merced Spring Radicchio Fall Radicchio Fall Radicchio Fallow August September October November December January February March April May June July August September October November Can we predict thrips development in peppers?

Controlling TSWV through use of a phenology model predicting the thrips lifecycle

• Thrips development is temperature dependent, the insects will only mature within a range of temperatures delineated by upper and lower thresholds. • The time spent at temperatures within these thresholds is called degree days. • During degree days thrips mature, outside them their development will be much slower or static. • During the pepper growing season degree days can accrue very quickly, making a prediction model linking thrips growth to specific weather conditions a useful tool. Overview of the model and population data

9 Adults 35000 10 35000 Egg 9 Fresno Co. 8 Yolo Co. 30000 30000 8 7 OW thrips/card 25000 7 25000 6 6 5 20000 20000 5 4 15000 4 15000 3 10000 3 10000 2 2 5000 5000 1 1 0 0 0 0 11/3 12/23 2/11 4/1 5/21 7/10 8/29 10/18 12/7 11/3 12/23 2/11 4/1 5/21 7/10 8/29 10/18

10 25000 10 35000 traps) (card count thrips 9 Merced Co. 9 Kings Co. 30000 8 20000 8 7 7 25000 6 15000 6

Predicted thrips generation peak generation thrips Predicted 20000 5 5 Cumulative 15000 4 10000 4 3 3 10000 2 5000 2 5000 1 1 0 0 0 0 11/3 12/23 2/11 4/1 5/21 7/10 8/29 10/18 12/23 2/11 4/1 5/21 7/10 8/29 10/18 Fresno example: Early control delays thrips build-up

10 Adults 35000 9 Egg 7 weeks delay 30000 8 OW 7 25000 thrips/card 6 20000 Initial population 5 increase 15000

4 thrips traps) (card thrips count 3 1 month delay 10000 2 5000

1

Predicted thrips generation generation peak thrips Predicted Cumulative Cumulative 0 0 11/3 12/23 2/11 4/1 5/21 7/10 8/29 10/18 Development of TSWV in Processing Tomato Fields in the Central Valley of California TSWV overwinters at Infections with TSWV – Potential for higher Persistence in weeds, low levels in weeds, low incidences, incidence/epidemics reservoir hosts, bridge bridge crops and thrips depending on and economic losses in crops (i.e., radicchio populations of virus late-planted crops. and lettuce) carrying thrips Viruliferous adult thrips emerging from soil Dormant viruliferous thrips Amplification in susceptible crops pupae stay in soil (dependent on initial inoculum and thrips populations)

TSWV incidence Winter Early-Mid Season Late Season Late Fall Western Flower Thrips Population Dynamics in the Central Valley of California

Thrips overwinter at Thrips populations Peak populations Populations decrease very low levels increase Increased viruliferous thrips populations Pupae can stay in soil Pupae can stay in soil

Target: early adult thrips generations

Thrips Populations December January February March April May June July August September October November Tomato spotted wilt virus Risk Index for Peppers-2015 Pepper Variety1 Examples Risk Index Points a,b,c suceptible varieties 50 p,q,r with Tsw gene -35 Planting Date2 Can we predict Early-planted First planted fields in any given region 5 Late-planted week or two later than first planted fields 25 TSWV development Red pepper latest planted field/or left for red harvest 35 Plant Population in peppers? Less than 7000 plant per acre single row 35 Between 7000 to 9000 plant per acre double row 15 More than 9000 plants per acre double row but more dense 5 •Based on the Planting Method Direct seeded 10 current pepper Transplanted 5 Proximity to Known Bridge Crops TRI, the fields adjacent radicchio, lettuce, fava, weed/fallow field, pepper or tomato 25 were assigned less than 1 mile radius distance (if TSWV confirmed add 20 more points) 15 1-2 mile radius distance (if TSWV confirmed add 10 more points) 10 high, moderate greater than 2 mile or None (if TSWV confirmed add 5 more points) 5 Proximity to Thrips Source and low risk adjacent wheat, pea, alfalfa or weedy patches etc. 20 less than 1 mile radius distance 15 1-2 mile radius distance 10 •In 2014, TRI None 5 At-Plant Insecticide correlated well None 15 with actual TSWV for other pests (+ thrips) 10 specifically for thrips 5 incidences! Weed situation/Herbicide use w/out herbicide but weedy In-field ONLY weed population 15 w/out herbicide but not so weedy 10 •TRI modified and w/out pre emergence herbicide or NO weed 5 Total Points (0-225) Risk of Losses Due to TSWV evaluated again in Less than or equal to 95 Low Greater than 100 or equal to 150 Moderate 2015. Greater than 150 High Example: TRI in Monitored Pepper Fields in 2014

Solano Co. TSWV % TSWV Risk Index (TRI) HM 2 140 PH 2 150 Si* 14 170 TR** 8 200

135 BU 2 Legends

HK <2 150 Less than or equal to 95 Low San Joaquin Greater than 100 or equal to 150 County Moderate AR 2 125 Greater than 150 MC*** <1 45 High Monitored Peppers in 2015 Solano/Yolo Co. TSWV % TSWV Risk Index (TRI) YO 2 120 120 SI 3 130 130 PS 2 165 165 HC** 1 125 125 HC Red 4 195 195 PR 2 125 125 OD** 2 145 145 OD Red 5 195 195 KY* 0 75 75 San Joaquin Co. SE* 0 70 70 SA 1 95 95 BX 4 205 205 Coastal Counties H15 1 110 110 L9 2 135 135 MaR 7 165 165 Yes We Can predict thrips and TSWV development in processing tomatoes and peppers!

http://ucanr.edu/sites/TSWVfieldriskindex/Field_Risk_Index/ http://ucanr.edu/sites/TSWVfieldriskindex/Thrips_Population_Projections/ IPM strategy for thrips and TSWV in peppers Before planting • determine the risk index for the field • evaluate planting location and time • use TSWV- and thrips-free transplants • plant TSWV resistant varieties (if risk index is high!) • implement weed management During the season • monitor fields for thrips (with yellow sticky cards and/or projections) • manage thrips • rotate insecticides • monitor fields for TSWV and remove infected plants • implement weed management After harvest • promptly remove and destroy plants after harvest • avoid planting bridge crops • control weeds/volunteers Acknowledgements Thank you! UC Davis Dr. Robert Gilbertson Dr. Neil McRoberts Dr. Diane Ullman Dr. Li-Fang Chen Thrips counters UCCE Farm Advisors Michelle LeStrange Gene Miyao TSWV Team Scott Stoddard Tom Turini Brenna Aegerter Steven Koike California growers and PCAs California Tomato Research Institute (CTRI) California Pepper Commission